Research ArticleThe Relevance of Interoception in Chronic Tinnitus AnalyzingInteroceptive Sensibility and Accuracy
Pia Lau1 Miriam Miesen12 Robert Wunderlich13 Alwina Stein1
Alva Engell1 Andreas Wollbrink1 Alexander L Gerlach4 Markus Junghoumlfer1
Thomas Ehring5 and Christo Pantev1
1 Institute for Biomagnetism and Biosignalanalysis University Hospital of Munster Malmedyweg 15 48149 Munster Germany2Institute of Psychology University of Munster Fliednerstraszlige 21 48149 Munster Germany3Institute for Physiological Psychology University of Bielefeld Universitatsstraszlige 25 33615 Bielefeld Germany4Institute of Clinical Psychology and Psychotherapy University of Cologne Pohligstraszlige 1 50969 Cologne Germany5Department of Psychology LMUMunich Leopoldstraszlige 13 80802 Munich Germany
Correspondence should be addressed to Christo Pantev pantevuni-muensterde
Received 17 April 2015 Accepted 22 July 2015
Academic Editor Aage R Moslashller
Copyright copy 2015 Pia Lau et al This is an open access article distributed under the Creative Commons Attribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
In order to better understand tinnitus and distress associated with tinnitus psychological variables such as emotional and cognitiveprocessing are a central element in theoretical models of this debilitating condition Interoception that is the perception of internalprocesses may be such a psychological factor relevant to tinnitus Against this background 20 participants suffering from chronictinnitus and 20matched healthy controls were testedwith questionnaires assessing interoceptive sensibility and participated in twotasks assessing interoceptive accuracy the Schandry task a heartbeat estimation assignment and a skin conductance fluctuationsperception task assessing the participantsrsquo ability to perceive phasic increases in sympathetic activation were used To test stressreactivity a construct tightly connected to tinnitus onset we also included a stress induction No differences between the groupswere found for interoceptive accuracy and sensibility However the tinnitus group tended to overestimate the occurrence of phasicactivation Loudness of the tinnitus was associated with reduced interoceptive performance under stress Our results indicatethat interoceptive sensibility and accuracy do not play a significant role in tinnitus However tinnitus might be associated witha tendency to overestimate physical changes
1 Introduction
Tinnitus affects up to 40of the population inWestern coun-tries at least temporarily [1] One to three percent of the gen-eral population report a significant reduction in their qualityof life due to their tinnitus for example through its effect onsleep andor mood [2] It is widely assumed that tinnitus is aresult of maladaptive cortical plasticity [3] Yet psychologicalconstructs are believed to mediate this process and are espe-cially tied to the distress perceived because of the tinnitus [4ndash6] Current psychological models of tinnitus assume a neu-ronal basis of the tinnitus and in addition focus on theinterplay of different psychological processes explaining theperceived distress [7] For example McKenna et al [7]
propose that tinnitus distress starts with the detection oftinnitusThen a vicious cycle of negative automatic thoughtsdetrimental safety behaviors selective attention and mon-itoring is triggered This model draws distinctively frommodels of other mental disorders such as panic disorder Inthe case of panic attacks small internal changes for exampleof the heartbeat trigger a similar dysfunctional circuit andin the end result in panic attacks (cf [8]) Hence one riskfactor for panic disorder is interoception [9] Interoception isdefined as sensitivity to internal stimuli which originate fromthe body itself [10] Interoception is also connected to othermental disorders including general anxiety disorder bulimianervosa anorexia nervosa and somatoform disorders [11ndash14] In addition interoception has been shown to be linked
Hindawi Publishing CorporationBioMed Research InternationalVolume 2015 Article ID 487372 9 pageshttpdxdoiorg1011552015487372
2 BioMed Research International
to psychological variables such as emotional experienceemotionalmemory processes and alexithymia [14ndash16] whichare also discussed in the context of tinnitus (eg [17 18])
Tinnitus per se is a process of interoception as it isattention toward internal perceptWhether interoception canbe assumed to be a dysfunctional factor for chronic tinnitushowever is still obscure Next to the overlap of etiologicalmodels psychotherapeutic aspects for mental disorders andtinnitus have common characteristics an important inter-vention in evidence-based treatment of panic disorder isinteroceptive exposure which includes purposely evokinginternal stimuli (eg hyperventilating and running steps toincrease the heartbeat) in order to make the patients learnthat those internal signals are not harmful [19] Similarlyintentionally focusing on the tinnitus is a strategy used in cur-rent treatments for tinnitus [20] This intervention showeda significant reduction in tinnitus related distress [21] whichpoints towards a meaningful connection between interocep-tion and chronic tinnitus
More evidence for a connection between chronic tinnitusand interoception comes from the field of neuroscience theright anterior insula is activated in interoceptive processeslikewise in tinnitus sufferers especially if they are highlydistressed [22ndash26] Taken together the current research con-cerning tinnitus offers hints for a connection between chronictinnitus and interoception but this question has never beenaddressed directly Hence this study can be seen as a first steptowards a better understatement of the putative role of inter-oception in tinnitus
Current research suggests that interoception exhibits athreefold structure interoceptive sensibility accuracy andawareness [27] Interoceptive sensibility is regarded as thesubjective perception of interoception measured throughquestionnaires or interviews Interoceptive accuracy some-times also named sensitivity is the objective measurement ofthe accurate detection of internal processes Finally intero-ceptive awareness is described as higher-order component ininteroception and covers more a metacognitive understand-ing of interoception for example the knowledge about theaccuracy of the own interoceptive perception As the latteris difficult to measure (cf [28]) and our study focused onthe basic aspects of interoception we collected data on thefirst two components namely interoceptive sensibility andaccuracy
A standard procedure to operationalize interoceptiveaccuracy is using the Schandry task [29] Participants have toreport on all heartbeats felt during a signaled period of timeThe participants have to rely solely on their feeling while noauxiliary means are allowed To also account for the accuracyof the perception of internal stimuli other than the heartbeatAndor et al [30] introduced a novel interoceptive accuracytask looking at the perception of spontaneous skin conduc-tance fluctuations In this task phases with stable skin con-ductance (no nonspecific skin conductance fluctuations) thusrepresenting the absence of internal arousal as well as non-specific skin conductance fluctuations (NSCF) representingcurrent phasic sympathetic arousal are recorded Partici-pants have to decide if an acoustic signal was preceded byeither phasic arousal or a period of stable skin conductance
This method allows the use of signal detection methodologyand thus the calculation of a perception bias to estimatewhether participants spuriously perceive bodily symptoms(cf Katzer et al [31] for the concept of illusory bodilysymptoms and its relevance to the understanding of somaticsymptom disorder)
In an attempt to explore interoception as clinically rele-vant construct to tinnitus we conducted an a priori poweranalysis based on effect sizes from a review paper on anxietydisorders [32] Sample size was chosen to be able to detecta momentous clinically relevant difference between thegroups We reasoned that in order to establish interoceptionin tinnitus as a valid and meaningful construct effect sizesshould be comparable to for example panic disorder
A multimethod assessment of interoception includinginteroceptive sensibility through questionnaire measures andinteroceptive accuracy through the Schandry task and theskin conductance task was used We hypothesized that agroup with tinnitus sufferers exhibits higher levels of intero-ceptive sensibility and accuracy compared to a group ofhealthy controls Based on findings in studies trying to betterunderstand somatic symptom disorder such as health anxiety[28] we also expected an interoceptive bias and postulatedthat the tinnitus group shows a more liberal bias towardsthe perception of internal processes for example phasicsympathetic arousal irrespective of its actual occurrence
Tinnitus sufferers regularly associate stress with tinnitus[33] For example in a study by Baigi et al [34] stress wasrelated to worsening of the tinnitus Hebert and Lupien [35]found higher cortisol levels in a tinnitus group compared toa control group after stress induction Since stress appears tobe associated with tinnitus we hypothesized that the tinnitusgroup shows higher interoceptive accuracy under inducedstress whereas the performance of the control group shouldbe less affected To rule out a better performance based onan increased cardiac output due to the stress we includeda control condition where the participants had to reach ele-vated levels of cardiac output through movement on anergometer
2 Methods and Materials
21 Participants Groups were matched with respect to agegender and level of education Unexpectedly the groupsdiffer in the Body Mass Index (BMI) (Table 1) The studyprotocol was approved by the ethics committee of theDepart-ment of Psychology at the University of Munster and wasconducted according to the Declaration of Helsinki Recruit-ment was conducted through advertisements in local news-papers an announcement on the institutersquos website and thedistribution of information brochures and posters through-out the university and in different locations in town Par-ticipants were paid 20C for their attendance Exclusioncriteria were high blood pressure cardiac diseases asthmaand pregnancy as the stress induction might have beendisadvantageous for individuals showing any of these con-ditions Pulsatile tinnitus medication with cardiovascular orpsychopharmacological effects and any diagnosis of mentaldisorder were additional exclusion criteria The absence of
BioMed Research International 3
Table 1 Demographic description and mean scores of the questionnaires of tinnitus group and control group
Tinnitus group (n = 20) Control group (n = 20)119905(38) 119901
M SD M SDAge (in Years) 428 131 417 129 026 080BMI (kgm2) 250 39 223 32 232 003lowast
Physical exercise per week (hours) 36 25 39 28 minus034 074Baseline heart rate (beats per minute) 758 157 703 119 126 022BAQ 6875 1167 6560 1637 minus070 024PBCS 1195 3734 1185 432 minus008 047MAIA 300 039 291 054 minus061 027SOMS 5905 1011 5865 1187 minus046 065PANAS-PA 3065 568 3150 609 043 067PANAS-NA 1185 139 1155 284 012 091THQ 2218 1601 mdash mdashTHI 2380 1373 mdash mdashBMI BodyMass Index BAQ Body Awareness Questionnaire PBCS Private Body Consciousness Scale MAIAMultidimensional Assessment of InteroceptiveAwareness SOMS Screening for Somatoform Disorders PANAS-PA Positive Affect Scale of the Positive and Negative Affect Scale PANAS-NA NegativeAffect Scale of the Positive and Negative Affect Scale THQ Tinnitus Handicap Questionnaire THI Tinnitus Handicap Inventory lowast119901 lt 005
mental disorders was ensured by assessing all participantswith the structured clinical interview formental disorders forDSM-IV (SCID German version [36])
22 Procedure All potential participants were prescreenedfor the above-mentioned exclusion criteria via telephone Ane-mail including the study information sheet was sent toindividuals meeting all inclusion criteria On the day of theappointment each participant gave written informed consentprior to participating in the experiments The assessmentstarted with the SCID to ensure absence of any mental dis-order which was the case for all participants
221 Questionnaires Following the suggestion by Mehlinget al [37] different questionnaires to assess interoceptivesensibility were utilized We used the Body Awareness Ques-tionnaire (BAQ [38]) a scale covering the perception of non-emotive normal body processes for example rhythms of thebody and anticipating body reactions Furthermore we usedthe first questionnaire dealing with interoception the PrivateBody Consciousness Scale (PBCS [39]) which measures adisposition to focus on internal processes a sensitivity forbodily changes and the awareness of interoceptive feedbackAdditionally we handed out the Multidimensional Assess-ment of Interoceptive Awareness (MAIA [40]) an eight-dimensional questionnaire covering noticing notdistractingnot-worrying attention regulation emotional awarenessself-regulation body listening and trusting For all threequestionnaires reliability and valditiy could be shown [3841 42] Positive affectivity and negative affectivity were mea-sured with the Positive and Negative Affect Scale (PANAS[43]) and somatization with the Screening for SomatoformDisorders (SOMS-7T [44]) The tinnitus group additionallycompleted the TinnitusHandicapQuestionnaire (THQ [45])
NSCF No NSCF
tone
Arousal signaldetection of arousal
Nonarousal signaldetection of arousal
t
Figure 1 Description of the skin conductance task as measure ofinteroceptive accuracy as depicted in Andor et al (2008) NSCFnonspecific skin conductance fluctuation 119905 = time
and the Tinnitus Handicap Inventory (THI [46]) to quan-tify their tinnitus distress as well as visual analogue scales(VAS) covering the topics of perceived loudness annoyancedistress and handicap of their tinnitus
222 Skin Conductance Task Skin conductance was mea-sured with a Varioport (Becker Meditec Karlsruhe Ger-many) with a sampling rate of 16Hz Two silversilver chlo-ride electrodes with a contact surface area of 2 cm2 to whichisotonic paste was applied were used [47] The electrodeswere attached to the palm of the nondominant hand [48]The Variotest system (Gerhard Mutz Cologne Germany)identified online periods of stable skin conductance (noNSCF) and periods of phasic sympathetic activation (NSCF)for amore detailed description Andor et al [30] Participantswere instructed to focus on their body arousal during theentire task and indicate after each tone whether a tone waspreceded by an occurrence of body arousal (see Figure 1for an illustration of the task procedure) The algorithmwhether the program was scanned for a stable phase or afluctuation was pseudorandomized with the restriction thatthe two different types of phases were not signaled morethan two times in a row The same sequence was used for
4 BioMed Research International
Baseline Stressinduction
Stress conditionof the
Schandry task
Physicalexercise
Baselinecondition of theSchandry task
Exercisecondition
of the Schandrytask
Figure 2 Procedure of the Schandry task
all participants The search window for a stable phase or afluctuation was 150 s If the intended event occurred withinthis time frame the tone was presented otherwise no tonewas presented and the program continued with the next trialIf more than five trials were missed the subject was excludedfrom data analysis and the time window was shortened to30 sThe latter intended to ensure that all participants startedwith the same feeling into the second task for examplethey did not notice that the task was cancelled Usuallyparticipants are relaxed during this task and show only a fewfluctuations in the skin conductance In order to increasethe arousal level of the participants that is provoke morefluctuations two one-minute breaks were included in thetask in which participants were asked to talk about their lastvacation book or movie As participants are usually morearoused in the beginning of an experimental session than inlater phases we chose to conduct the skin conductance taskalways first before the Schandry task
223 Schandry Task In the second task interoceptive accu-racy was measured using the Schandry task [29] Participantswere instructed to count their heartbeat for an indicatedamount of timeThe electrocardiogram (ECG) wasmeasuredwith a technical device (NeXus-10 Mark II Mind MediaBV Herten Netherlands) using three silversilver chlorideelectrodes attached to the torso according to Einthoven leadII The ECG was sampled at a rate of 256Hz The trials werepresented with Presentation (Neurobehavioral Systems IncBerkeley CA USA)
Three within-subject conditions existed for this task abaseline condition with the classic Schandry task a conditionfollowing a social stress induction and a control conditionfollowing physical exercise on an ergometer (see Figure 2)Each condition consisted of five consecutive trials of differentlength (20 25 30 35 and 40 s) which were presented inrandomized order After each trial participants had 10 s toreport their heartbeat count to the investigator A 30-secondpause followed each trial The beginning and the end of eachtrial weremarked by a tone (onset tone 800Hz 300ms offsettone 500Hz 300ms)
Before the baseline Schandry task participantswere givenfive minutes to get used to the ECG and afterwards filled outthe good-and-badmood and agitation-tranquility scale of theMultidimensional Questionnaire of Mental State (Mehrdi-mensionaler BefindlichkeitsfragebogenMDBF [49] cf [50])to report on their current mental state Afterwards theSchandry task was presented Participants were asked to situpright with their back of the hands resting on their thighsThis and the explicit instruction to avoid any other auxiliarymeans (eg measuring the pulse with the fingertips) wereintended to ensure that the participants relied on their
interoception solely One test trial was conducted to makethe participants familiar with the task Then the baselineSchandry task with its five trials was presented followed bythe stress induction Here the participants performed thecognitive stress task of the Trier Social Stress Test [51] For fiveminutes participants had to repeatedly subtract 13 starting at1022 They were told to do this mental arithmetic task as fastand as accurate as possible In case of an error participantswere interrupted and told to start again at 1022 To furtherincrease stress the investigator said ldquoPlease calculate fasterrdquoMoreover participants were told that also the voice and theposture during this mathematical task would be analyzedand therefore he or she was videotaped during the task Toenhance stress levels through the additional factor of self-awareness participants could see themselves on a screenAfter the stress induction period participants again filled outthe MDBF The second block of five trials of the Schandrytask was presented followed by another completion of theMDBF Finally the last condition of the Schandry task startedheartbeat perception after physical exercise (five minutescycling on an ergometer)The investigator instructed the par-ticipant to either speed up or slowdown their cycling to adjusttheir average heart rate to the heart ratemeasured in the stressinduction phase Finally the third block of the Schandry taskwas conducted At the end of the experiment participantswere informed about the purpose of the experiment includ-ing the function of the stress induction
23 Analysis
231 Skin Conductance Task According to participantsrsquo abil-ity to detect NSCFs the sensitivity index 1198891015840 was calculated asfollows119885(hit rate) ndash119885(false alarm rate) If the hit rate equalsthe false alarms rate the index is zero implicating low sensi-tivity The higher 1198891015840 is the better the participants were ableto detect phasic internal arousal correctly Furthermore anindex to quantify bias C as response behavior was calculatedminus05lowast (119885(false alarm rate) +Z(hit rate)) It describes whetherthe participant had a conservative response behavior that isreporting more often no arousal than arousal or a liberalone that is reporting more often arousal irrespective of itsoccurrence The first is represented through an index higherthan 0 and the latter below 0 an index around 0 reflectsthat there is no tendency for example a balanced answeringbehavior
232 Schandry Task Data from the NeXus (including thetriggers from Presentation) was imported to the Polymanprogram (Bob Kemp amp Marco Roessen Den Haag Nether-lands) to quantify the participantsrsquo heartbeat Based on thisdata (recorded heartbeat) and the answers given by the
BioMed Research International 5
Tinnitus groupControl group
Bias
C (m
ean)
060
040
020
0
minus020
Figure 3Mean score for biasC in the control and the tinnitus groupError bars indicate the standard error
participants (counted heartbeat) during the experiment theheartbeat perception score was calculated (HBP HBP = 1 minus15 sum(|recorded heartbeats minus counted heartbeats|recordedheartbeats) (cf [11 52 53]))The better the performance thatis the accuracy of the given answers the higher the HBPThemaximal value is 1
3 Results
Twenty participants with chronic tinnitus (M= 428 years SD= 131 40 female) and twenty healthy control participantswithout tinnitus (M = 417 years SD = 129 40 female)were tested Groupswerematchedwith respect to age genderand level of education Unexpectedly the groups differ in theBody Mass Index (BMI) see Table 1
31 Questionnaires The 119905-test for independent samplesrevealed no significant differences between the two groupsregarding the self-report measures of interoception BAQ119905(38) =minus070119901 = 024 PBCS 119905(38) =minus008119901 = 047MAIA119905(38) =minus061119901 = 027The same is true for the SOMS 119905(38) =012 119901 = 091 PANAS-PA 119905(38) = minus046 119901 = 065 andPANAS-NA 119905(38) = 043 119901 = 067 (see Table 1)
32 Skin Conductance Task Due to too few spontaneous skinconductance fluctuations (less than 5) 12 participants hadto be excluded from the analysis yielding 15 participants inthe tinnitus group and 13 in the control group We found nodifference of the sensitivity index 1198891015840 between the groups in a119905-test for independent samples 119905(26) = 059 119901 = 028 and 119889= 022 (tinnitus groupM= minus014 SD = 130 and control groupM = 016 SD = 151) A trend was found for the bias C 119905(26)= 153 119901 = 007 119889 = 058 (see Figure 3 tinnitus group M =minus019 SD = 071 and control group M = 022 SD = 070)
ExerciseStressBaseline
700
600
500
400
MD
BF (s
um sc
ore)
Condition
Tinnitus groupControl group
Figure 4 Current mood throughout the Schandry task conditionsfor both groups Error bars indicate standard error MDBF Multidi-mensional Questionnaire of Mental State
33 Schandry Task All participants were included in theanalysis In order to check if we successfully implemented thethree conditions we compared the three consecutive currentmental state scores A repeated measures ANOVA with thefactors Condition (baseline versus stress versus exercise)and Group (tinnitus versus control) showed a significantdifference between the three conditions 119865(276) = 5312 119901 lt0001 and 1205782 = 067 (see Figure 4)
Simple contrasts revealed that the current mental stateafter the stress induction was significantly reduced comparedto baseline 119865(138) = 6221 119901 lt 0001 and the exercisecondition119865(138) = 7426119901 lt 0001Therewas no significantinteraction between group and condition 119865(276) = 147 119901 =024 and 1205782 = 004
Besides the self-report measure of mood we also evalu-ated heart rate in the three different conditions The lowestheart rate was found in the baseline condition (M = 7304SD = 1401) followed by the stress (M = 8590 SD = 1753) andthe exercise condition (M = 8820 SD = 1594) An ANOVAfor repeated measure with the factors Condition and Groupshowed again a significant difference for the conditions forthe heart rate values 119865(276) = 6068 119901 lt 0001 and 1205782 =062 Simple contrasts showed a significant difference in heartrate between baseline condition and both stress condition119865(138) = 4559 119901 lt 0001 and exercise condition 119865(138) =10611 119901 lt 0001 and a significant difference between thestress condition and the exercise condition 119865(138) = 653119901 = 002There was no significant interaction of group 119909 con-dition 119865(276) = 005 119901 = 096 and 1205782 = 000
Using a repeated measures ANOVA on the HBP valueswith the factors Condition and Group no main effect for
6 BioMed Research International
SportStressBaseline
HBP
(mea
n)068
064
060
056
052
ConditionTinnitus groupControl group
Figure 5 Heartbeat perception score (HBP) of the tinnitus andcontrol group in the three conditions (baseline stress and exercise)of the Schandry task Error bars indicate the standard error
groups with regard to HBP 119865(276) = 190 119901 = 016 nor aninteraction effect 119865(276) = 030 119901 = 073 was found (seeFigure 5)
34 Post Hoc Analysis An analysis of covariance (ANCOVA)for the performance in the Schandry task in the three condi-tions within the tinnitus group was conducted using tinnitusloudness as a covariate Bonferroni correction for multipletesting was appliedThis analysis revealed a significant differ-ence between the three conditions when controlling tinnitusloudness 119865(236) = 516 119901 = 002 as well as the interactioncondition 119909 loudness 119865(236) = 439 119901 = 004 (see Figure 6)A simple linear regression analysis to predict the performancein the Schandry task for the stress condition compared to thebaseline condition revealed a significant influence of tinnitusloudness119865(118) = 855119901 lt 001 and1198772 = 028 Amarginallysignificant effect was found for the influence of loudness onthe performance in the exercise condition 119865(118) = 399119901 = 006 and 1198772 = 018 Quiet tinnitus went along with anenhanced performance in the Schandry task especially inthe stress and exercise condition whereas loud tinnitus isaccompanied with a decreased performance in the stress andexercise task
A second ANCOVA for repeated measures for the per-formance in the Schandry task with BMI as covariate didnot reach significance level 119865(274) = 037 119901 gt 099 (againBonferroni corrected for multiple comparisons)
4 Discussion
We evaluated whether interoceptive sensibility and accuracyas key factors of interoception differed in a sample with
000
025
050
075
100
25 50 75
HBP
ConditionBaselineStressExercise
Tinnitus loudness
Figure 6 Correlation between the heart beat perception (HBP)score and tinnitus loudness The correlation is plotted separately forthe three conditions of the Schandry task Colored lines representthe linear regression lines for each condition
chronic tinnitus and healthy control subjects We found noclinically relevant differences between the groups neitherusing questionnaires (interoceptive sensibility) nor usingexperimental tasks (the Schandry task and a skin conduc-tance task interoceptive accuracy) However a trend in thebias measure C towards a more liberal perception of arousalthat is a higher preparedness to expect internal arousal in thetinnitus group was detected Furthermore tinnitus loudnessinfluenced performance on the Schandry task in the chronictinnitus group
In order to detect a clinically relevant influence of intero-ception on tinnitus we based our a priori power calculationson the averaged effect size from a review [32] for the Schandrytask which is the most field-tested and standardized taskfor interoception However our results show that changesin interoception in chronic tinnitus are not comparable toanxiety disorders
Our hypothesis that the tinnitus group might performbetter in interoceptive accuracy when stressed that is tryingto roughly simulate the cooccurrence of stress and tinnitusonset was not supported by the obtained experimentalresults Given the comparable heart frequency we assumedthat the origin of the heart beat differences stress or exercisemight have an influence on interoception Yet there was nodifference between performance in the two conditions noran interaction effect between group and condition Heartbeat elevation and the self-report of mental state after thestress induction reflect a successful manipulation Yet wedo not know how long the elevated stress level after theinduction lasted At least before the beginning of the exercisecondition the stress levels went back to normal It mightbe worth to enhance the stress level more persistently orldquorefreshrdquo the stress level between each trial in order to come
BioMed Research International 7
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
to psychological variables such as emotional experienceemotionalmemory processes and alexithymia [14ndash16] whichare also discussed in the context of tinnitus (eg [17 18])
Tinnitus per se is a process of interoception as it isattention toward internal perceptWhether interoception canbe assumed to be a dysfunctional factor for chronic tinnitushowever is still obscure Next to the overlap of etiologicalmodels psychotherapeutic aspects for mental disorders andtinnitus have common characteristics an important inter-vention in evidence-based treatment of panic disorder isinteroceptive exposure which includes purposely evokinginternal stimuli (eg hyperventilating and running steps toincrease the heartbeat) in order to make the patients learnthat those internal signals are not harmful [19] Similarlyintentionally focusing on the tinnitus is a strategy used in cur-rent treatments for tinnitus [20] This intervention showeda significant reduction in tinnitus related distress [21] whichpoints towards a meaningful connection between interocep-tion and chronic tinnitus
More evidence for a connection between chronic tinnitusand interoception comes from the field of neuroscience theright anterior insula is activated in interoceptive processeslikewise in tinnitus sufferers especially if they are highlydistressed [22ndash26] Taken together the current research con-cerning tinnitus offers hints for a connection between chronictinnitus and interoception but this question has never beenaddressed directly Hence this study can be seen as a first steptowards a better understatement of the putative role of inter-oception in tinnitus
Current research suggests that interoception exhibits athreefold structure interoceptive sensibility accuracy andawareness [27] Interoceptive sensibility is regarded as thesubjective perception of interoception measured throughquestionnaires or interviews Interoceptive accuracy some-times also named sensitivity is the objective measurement ofthe accurate detection of internal processes Finally intero-ceptive awareness is described as higher-order component ininteroception and covers more a metacognitive understand-ing of interoception for example the knowledge about theaccuracy of the own interoceptive perception As the latteris difficult to measure (cf [28]) and our study focused onthe basic aspects of interoception we collected data on thefirst two components namely interoceptive sensibility andaccuracy
A standard procedure to operationalize interoceptiveaccuracy is using the Schandry task [29] Participants have toreport on all heartbeats felt during a signaled period of timeThe participants have to rely solely on their feeling while noauxiliary means are allowed To also account for the accuracyof the perception of internal stimuli other than the heartbeatAndor et al [30] introduced a novel interoceptive accuracytask looking at the perception of spontaneous skin conduc-tance fluctuations In this task phases with stable skin con-ductance (no nonspecific skin conductance fluctuations) thusrepresenting the absence of internal arousal as well as non-specific skin conductance fluctuations (NSCF) representingcurrent phasic sympathetic arousal are recorded Partici-pants have to decide if an acoustic signal was preceded byeither phasic arousal or a period of stable skin conductance
This method allows the use of signal detection methodologyand thus the calculation of a perception bias to estimatewhether participants spuriously perceive bodily symptoms(cf Katzer et al [31] for the concept of illusory bodilysymptoms and its relevance to the understanding of somaticsymptom disorder)
In an attempt to explore interoception as clinically rele-vant construct to tinnitus we conducted an a priori poweranalysis based on effect sizes from a review paper on anxietydisorders [32] Sample size was chosen to be able to detecta momentous clinically relevant difference between thegroups We reasoned that in order to establish interoceptionin tinnitus as a valid and meaningful construct effect sizesshould be comparable to for example panic disorder
A multimethod assessment of interoception includinginteroceptive sensibility through questionnaire measures andinteroceptive accuracy through the Schandry task and theskin conductance task was used We hypothesized that agroup with tinnitus sufferers exhibits higher levels of intero-ceptive sensibility and accuracy compared to a group ofhealthy controls Based on findings in studies trying to betterunderstand somatic symptom disorder such as health anxiety[28] we also expected an interoceptive bias and postulatedthat the tinnitus group shows a more liberal bias towardsthe perception of internal processes for example phasicsympathetic arousal irrespective of its actual occurrence
Tinnitus sufferers regularly associate stress with tinnitus[33] For example in a study by Baigi et al [34] stress wasrelated to worsening of the tinnitus Hebert and Lupien [35]found higher cortisol levels in a tinnitus group compared toa control group after stress induction Since stress appears tobe associated with tinnitus we hypothesized that the tinnitusgroup shows higher interoceptive accuracy under inducedstress whereas the performance of the control group shouldbe less affected To rule out a better performance based onan increased cardiac output due to the stress we includeda control condition where the participants had to reach ele-vated levels of cardiac output through movement on anergometer
2 Methods and Materials
21 Participants Groups were matched with respect to agegender and level of education Unexpectedly the groupsdiffer in the Body Mass Index (BMI) (Table 1) The studyprotocol was approved by the ethics committee of theDepart-ment of Psychology at the University of Munster and wasconducted according to the Declaration of Helsinki Recruit-ment was conducted through advertisements in local news-papers an announcement on the institutersquos website and thedistribution of information brochures and posters through-out the university and in different locations in town Par-ticipants were paid 20C for their attendance Exclusioncriteria were high blood pressure cardiac diseases asthmaand pregnancy as the stress induction might have beendisadvantageous for individuals showing any of these con-ditions Pulsatile tinnitus medication with cardiovascular orpsychopharmacological effects and any diagnosis of mentaldisorder were additional exclusion criteria The absence of
BioMed Research International 3
Table 1 Demographic description and mean scores of the questionnaires of tinnitus group and control group
Tinnitus group (n = 20) Control group (n = 20)119905(38) 119901
M SD M SDAge (in Years) 428 131 417 129 026 080BMI (kgm2) 250 39 223 32 232 003lowast
Physical exercise per week (hours) 36 25 39 28 minus034 074Baseline heart rate (beats per minute) 758 157 703 119 126 022BAQ 6875 1167 6560 1637 minus070 024PBCS 1195 3734 1185 432 minus008 047MAIA 300 039 291 054 minus061 027SOMS 5905 1011 5865 1187 minus046 065PANAS-PA 3065 568 3150 609 043 067PANAS-NA 1185 139 1155 284 012 091THQ 2218 1601 mdash mdashTHI 2380 1373 mdash mdashBMI BodyMass Index BAQ Body Awareness Questionnaire PBCS Private Body Consciousness Scale MAIAMultidimensional Assessment of InteroceptiveAwareness SOMS Screening for Somatoform Disorders PANAS-PA Positive Affect Scale of the Positive and Negative Affect Scale PANAS-NA NegativeAffect Scale of the Positive and Negative Affect Scale THQ Tinnitus Handicap Questionnaire THI Tinnitus Handicap Inventory lowast119901 lt 005
mental disorders was ensured by assessing all participantswith the structured clinical interview formental disorders forDSM-IV (SCID German version [36])
22 Procedure All potential participants were prescreenedfor the above-mentioned exclusion criteria via telephone Ane-mail including the study information sheet was sent toindividuals meeting all inclusion criteria On the day of theappointment each participant gave written informed consentprior to participating in the experiments The assessmentstarted with the SCID to ensure absence of any mental dis-order which was the case for all participants
221 Questionnaires Following the suggestion by Mehlinget al [37] different questionnaires to assess interoceptivesensibility were utilized We used the Body Awareness Ques-tionnaire (BAQ [38]) a scale covering the perception of non-emotive normal body processes for example rhythms of thebody and anticipating body reactions Furthermore we usedthe first questionnaire dealing with interoception the PrivateBody Consciousness Scale (PBCS [39]) which measures adisposition to focus on internal processes a sensitivity forbodily changes and the awareness of interoceptive feedbackAdditionally we handed out the Multidimensional Assess-ment of Interoceptive Awareness (MAIA [40]) an eight-dimensional questionnaire covering noticing notdistractingnot-worrying attention regulation emotional awarenessself-regulation body listening and trusting For all threequestionnaires reliability and valditiy could be shown [3841 42] Positive affectivity and negative affectivity were mea-sured with the Positive and Negative Affect Scale (PANAS[43]) and somatization with the Screening for SomatoformDisorders (SOMS-7T [44]) The tinnitus group additionallycompleted the TinnitusHandicapQuestionnaire (THQ [45])
NSCF No NSCF
tone
Arousal signaldetection of arousal
Nonarousal signaldetection of arousal
t
Figure 1 Description of the skin conductance task as measure ofinteroceptive accuracy as depicted in Andor et al (2008) NSCFnonspecific skin conductance fluctuation 119905 = time
and the Tinnitus Handicap Inventory (THI [46]) to quan-tify their tinnitus distress as well as visual analogue scales(VAS) covering the topics of perceived loudness annoyancedistress and handicap of their tinnitus
222 Skin Conductance Task Skin conductance was mea-sured with a Varioport (Becker Meditec Karlsruhe Ger-many) with a sampling rate of 16Hz Two silversilver chlo-ride electrodes with a contact surface area of 2 cm2 to whichisotonic paste was applied were used [47] The electrodeswere attached to the palm of the nondominant hand [48]The Variotest system (Gerhard Mutz Cologne Germany)identified online periods of stable skin conductance (noNSCF) and periods of phasic sympathetic activation (NSCF)for amore detailed description Andor et al [30] Participantswere instructed to focus on their body arousal during theentire task and indicate after each tone whether a tone waspreceded by an occurrence of body arousal (see Figure 1for an illustration of the task procedure) The algorithmwhether the program was scanned for a stable phase or afluctuation was pseudorandomized with the restriction thatthe two different types of phases were not signaled morethan two times in a row The same sequence was used for
4 BioMed Research International
Baseline Stressinduction
Stress conditionof the
Schandry task
Physicalexercise
Baselinecondition of theSchandry task
Exercisecondition
of the Schandrytask
Figure 2 Procedure of the Schandry task
all participants The search window for a stable phase or afluctuation was 150 s If the intended event occurred withinthis time frame the tone was presented otherwise no tonewas presented and the program continued with the next trialIf more than five trials were missed the subject was excludedfrom data analysis and the time window was shortened to30 sThe latter intended to ensure that all participants startedwith the same feeling into the second task for examplethey did not notice that the task was cancelled Usuallyparticipants are relaxed during this task and show only a fewfluctuations in the skin conductance In order to increasethe arousal level of the participants that is provoke morefluctuations two one-minute breaks were included in thetask in which participants were asked to talk about their lastvacation book or movie As participants are usually morearoused in the beginning of an experimental session than inlater phases we chose to conduct the skin conductance taskalways first before the Schandry task
223 Schandry Task In the second task interoceptive accu-racy was measured using the Schandry task [29] Participantswere instructed to count their heartbeat for an indicatedamount of timeThe electrocardiogram (ECG) wasmeasuredwith a technical device (NeXus-10 Mark II Mind MediaBV Herten Netherlands) using three silversilver chlorideelectrodes attached to the torso according to Einthoven leadII The ECG was sampled at a rate of 256Hz The trials werepresented with Presentation (Neurobehavioral Systems IncBerkeley CA USA)
Three within-subject conditions existed for this task abaseline condition with the classic Schandry task a conditionfollowing a social stress induction and a control conditionfollowing physical exercise on an ergometer (see Figure 2)Each condition consisted of five consecutive trials of differentlength (20 25 30 35 and 40 s) which were presented inrandomized order After each trial participants had 10 s toreport their heartbeat count to the investigator A 30-secondpause followed each trial The beginning and the end of eachtrial weremarked by a tone (onset tone 800Hz 300ms offsettone 500Hz 300ms)
Before the baseline Schandry task participantswere givenfive minutes to get used to the ECG and afterwards filled outthe good-and-badmood and agitation-tranquility scale of theMultidimensional Questionnaire of Mental State (Mehrdi-mensionaler BefindlichkeitsfragebogenMDBF [49] cf [50])to report on their current mental state Afterwards theSchandry task was presented Participants were asked to situpright with their back of the hands resting on their thighsThis and the explicit instruction to avoid any other auxiliarymeans (eg measuring the pulse with the fingertips) wereintended to ensure that the participants relied on their
interoception solely One test trial was conducted to makethe participants familiar with the task Then the baselineSchandry task with its five trials was presented followed bythe stress induction Here the participants performed thecognitive stress task of the Trier Social Stress Test [51] For fiveminutes participants had to repeatedly subtract 13 starting at1022 They were told to do this mental arithmetic task as fastand as accurate as possible In case of an error participantswere interrupted and told to start again at 1022 To furtherincrease stress the investigator said ldquoPlease calculate fasterrdquoMoreover participants were told that also the voice and theposture during this mathematical task would be analyzedand therefore he or she was videotaped during the task Toenhance stress levels through the additional factor of self-awareness participants could see themselves on a screenAfter the stress induction period participants again filled outthe MDBF The second block of five trials of the Schandrytask was presented followed by another completion of theMDBF Finally the last condition of the Schandry task startedheartbeat perception after physical exercise (five minutescycling on an ergometer)The investigator instructed the par-ticipant to either speed up or slowdown their cycling to adjusttheir average heart rate to the heart ratemeasured in the stressinduction phase Finally the third block of the Schandry taskwas conducted At the end of the experiment participantswere informed about the purpose of the experiment includ-ing the function of the stress induction
23 Analysis
231 Skin Conductance Task According to participantsrsquo abil-ity to detect NSCFs the sensitivity index 1198891015840 was calculated asfollows119885(hit rate) ndash119885(false alarm rate) If the hit rate equalsthe false alarms rate the index is zero implicating low sensi-tivity The higher 1198891015840 is the better the participants were ableto detect phasic internal arousal correctly Furthermore anindex to quantify bias C as response behavior was calculatedminus05lowast (119885(false alarm rate) +Z(hit rate)) It describes whetherthe participant had a conservative response behavior that isreporting more often no arousal than arousal or a liberalone that is reporting more often arousal irrespective of itsoccurrence The first is represented through an index higherthan 0 and the latter below 0 an index around 0 reflectsthat there is no tendency for example a balanced answeringbehavior
232 Schandry Task Data from the NeXus (including thetriggers from Presentation) was imported to the Polymanprogram (Bob Kemp amp Marco Roessen Den Haag Nether-lands) to quantify the participantsrsquo heartbeat Based on thisdata (recorded heartbeat) and the answers given by the
BioMed Research International 5
Tinnitus groupControl group
Bias
C (m
ean)
060
040
020
0
minus020
Figure 3Mean score for biasC in the control and the tinnitus groupError bars indicate the standard error
participants (counted heartbeat) during the experiment theheartbeat perception score was calculated (HBP HBP = 1 minus15 sum(|recorded heartbeats minus counted heartbeats|recordedheartbeats) (cf [11 52 53]))The better the performance thatis the accuracy of the given answers the higher the HBPThemaximal value is 1
3 Results
Twenty participants with chronic tinnitus (M= 428 years SD= 131 40 female) and twenty healthy control participantswithout tinnitus (M = 417 years SD = 129 40 female)were tested Groupswerematchedwith respect to age genderand level of education Unexpectedly the groups differ in theBody Mass Index (BMI) see Table 1
31 Questionnaires The 119905-test for independent samplesrevealed no significant differences between the two groupsregarding the self-report measures of interoception BAQ119905(38) =minus070119901 = 024 PBCS 119905(38) =minus008119901 = 047MAIA119905(38) =minus061119901 = 027The same is true for the SOMS 119905(38) =012 119901 = 091 PANAS-PA 119905(38) = minus046 119901 = 065 andPANAS-NA 119905(38) = 043 119901 = 067 (see Table 1)
32 Skin Conductance Task Due to too few spontaneous skinconductance fluctuations (less than 5) 12 participants hadto be excluded from the analysis yielding 15 participants inthe tinnitus group and 13 in the control group We found nodifference of the sensitivity index 1198891015840 between the groups in a119905-test for independent samples 119905(26) = 059 119901 = 028 and 119889= 022 (tinnitus groupM= minus014 SD = 130 and control groupM = 016 SD = 151) A trend was found for the bias C 119905(26)= 153 119901 = 007 119889 = 058 (see Figure 3 tinnitus group M =minus019 SD = 071 and control group M = 022 SD = 070)
ExerciseStressBaseline
700
600
500
400
MD
BF (s
um sc
ore)
Condition
Tinnitus groupControl group
Figure 4 Current mood throughout the Schandry task conditionsfor both groups Error bars indicate standard error MDBF Multidi-mensional Questionnaire of Mental State
33 Schandry Task All participants were included in theanalysis In order to check if we successfully implemented thethree conditions we compared the three consecutive currentmental state scores A repeated measures ANOVA with thefactors Condition (baseline versus stress versus exercise)and Group (tinnitus versus control) showed a significantdifference between the three conditions 119865(276) = 5312 119901 lt0001 and 1205782 = 067 (see Figure 4)
Simple contrasts revealed that the current mental stateafter the stress induction was significantly reduced comparedto baseline 119865(138) = 6221 119901 lt 0001 and the exercisecondition119865(138) = 7426119901 lt 0001Therewas no significantinteraction between group and condition 119865(276) = 147 119901 =024 and 1205782 = 004
Besides the self-report measure of mood we also evalu-ated heart rate in the three different conditions The lowestheart rate was found in the baseline condition (M = 7304SD = 1401) followed by the stress (M = 8590 SD = 1753) andthe exercise condition (M = 8820 SD = 1594) An ANOVAfor repeated measure with the factors Condition and Groupshowed again a significant difference for the conditions forthe heart rate values 119865(276) = 6068 119901 lt 0001 and 1205782 =062 Simple contrasts showed a significant difference in heartrate between baseline condition and both stress condition119865(138) = 4559 119901 lt 0001 and exercise condition 119865(138) =10611 119901 lt 0001 and a significant difference between thestress condition and the exercise condition 119865(138) = 653119901 = 002There was no significant interaction of group 119909 con-dition 119865(276) = 005 119901 = 096 and 1205782 = 000
Using a repeated measures ANOVA on the HBP valueswith the factors Condition and Group no main effect for
6 BioMed Research International
SportStressBaseline
HBP
(mea
n)068
064
060
056
052
ConditionTinnitus groupControl group
Figure 5 Heartbeat perception score (HBP) of the tinnitus andcontrol group in the three conditions (baseline stress and exercise)of the Schandry task Error bars indicate the standard error
groups with regard to HBP 119865(276) = 190 119901 = 016 nor aninteraction effect 119865(276) = 030 119901 = 073 was found (seeFigure 5)
34 Post Hoc Analysis An analysis of covariance (ANCOVA)for the performance in the Schandry task in the three condi-tions within the tinnitus group was conducted using tinnitusloudness as a covariate Bonferroni correction for multipletesting was appliedThis analysis revealed a significant differ-ence between the three conditions when controlling tinnitusloudness 119865(236) = 516 119901 = 002 as well as the interactioncondition 119909 loudness 119865(236) = 439 119901 = 004 (see Figure 6)A simple linear regression analysis to predict the performancein the Schandry task for the stress condition compared to thebaseline condition revealed a significant influence of tinnitusloudness119865(118) = 855119901 lt 001 and1198772 = 028 Amarginallysignificant effect was found for the influence of loudness onthe performance in the exercise condition 119865(118) = 399119901 = 006 and 1198772 = 018 Quiet tinnitus went along with anenhanced performance in the Schandry task especially inthe stress and exercise condition whereas loud tinnitus isaccompanied with a decreased performance in the stress andexercise task
A second ANCOVA for repeated measures for the per-formance in the Schandry task with BMI as covariate didnot reach significance level 119865(274) = 037 119901 gt 099 (againBonferroni corrected for multiple comparisons)
4 Discussion
We evaluated whether interoceptive sensibility and accuracyas key factors of interoception differed in a sample with
000
025
050
075
100
25 50 75
HBP
ConditionBaselineStressExercise
Tinnitus loudness
Figure 6 Correlation between the heart beat perception (HBP)score and tinnitus loudness The correlation is plotted separately forthe three conditions of the Schandry task Colored lines representthe linear regression lines for each condition
chronic tinnitus and healthy control subjects We found noclinically relevant differences between the groups neitherusing questionnaires (interoceptive sensibility) nor usingexperimental tasks (the Schandry task and a skin conduc-tance task interoceptive accuracy) However a trend in thebias measure C towards a more liberal perception of arousalthat is a higher preparedness to expect internal arousal in thetinnitus group was detected Furthermore tinnitus loudnessinfluenced performance on the Schandry task in the chronictinnitus group
In order to detect a clinically relevant influence of intero-ception on tinnitus we based our a priori power calculationson the averaged effect size from a review [32] for the Schandrytask which is the most field-tested and standardized taskfor interoception However our results show that changesin interoception in chronic tinnitus are not comparable toanxiety disorders
Our hypothesis that the tinnitus group might performbetter in interoceptive accuracy when stressed that is tryingto roughly simulate the cooccurrence of stress and tinnitusonset was not supported by the obtained experimentalresults Given the comparable heart frequency we assumedthat the origin of the heart beat differences stress or exercisemight have an influence on interoception Yet there was nodifference between performance in the two conditions noran interaction effect between group and condition Heartbeat elevation and the self-report of mental state after thestress induction reflect a successful manipulation Yet wedo not know how long the elevated stress level after theinduction lasted At least before the beginning of the exercisecondition the stress levels went back to normal It mightbe worth to enhance the stress level more persistently orldquorefreshrdquo the stress level between each trial in order to come
BioMed Research International 7
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
Table 1 Demographic description and mean scores of the questionnaires of tinnitus group and control group
Tinnitus group (n = 20) Control group (n = 20)119905(38) 119901
M SD M SDAge (in Years) 428 131 417 129 026 080BMI (kgm2) 250 39 223 32 232 003lowast
Physical exercise per week (hours) 36 25 39 28 minus034 074Baseline heart rate (beats per minute) 758 157 703 119 126 022BAQ 6875 1167 6560 1637 minus070 024PBCS 1195 3734 1185 432 minus008 047MAIA 300 039 291 054 minus061 027SOMS 5905 1011 5865 1187 minus046 065PANAS-PA 3065 568 3150 609 043 067PANAS-NA 1185 139 1155 284 012 091THQ 2218 1601 mdash mdashTHI 2380 1373 mdash mdashBMI BodyMass Index BAQ Body Awareness Questionnaire PBCS Private Body Consciousness Scale MAIAMultidimensional Assessment of InteroceptiveAwareness SOMS Screening for Somatoform Disorders PANAS-PA Positive Affect Scale of the Positive and Negative Affect Scale PANAS-NA NegativeAffect Scale of the Positive and Negative Affect Scale THQ Tinnitus Handicap Questionnaire THI Tinnitus Handicap Inventory lowast119901 lt 005
mental disorders was ensured by assessing all participantswith the structured clinical interview formental disorders forDSM-IV (SCID German version [36])
22 Procedure All potential participants were prescreenedfor the above-mentioned exclusion criteria via telephone Ane-mail including the study information sheet was sent toindividuals meeting all inclusion criteria On the day of theappointment each participant gave written informed consentprior to participating in the experiments The assessmentstarted with the SCID to ensure absence of any mental dis-order which was the case for all participants
221 Questionnaires Following the suggestion by Mehlinget al [37] different questionnaires to assess interoceptivesensibility were utilized We used the Body Awareness Ques-tionnaire (BAQ [38]) a scale covering the perception of non-emotive normal body processes for example rhythms of thebody and anticipating body reactions Furthermore we usedthe first questionnaire dealing with interoception the PrivateBody Consciousness Scale (PBCS [39]) which measures adisposition to focus on internal processes a sensitivity forbodily changes and the awareness of interoceptive feedbackAdditionally we handed out the Multidimensional Assess-ment of Interoceptive Awareness (MAIA [40]) an eight-dimensional questionnaire covering noticing notdistractingnot-worrying attention regulation emotional awarenessself-regulation body listening and trusting For all threequestionnaires reliability and valditiy could be shown [3841 42] Positive affectivity and negative affectivity were mea-sured with the Positive and Negative Affect Scale (PANAS[43]) and somatization with the Screening for SomatoformDisorders (SOMS-7T [44]) The tinnitus group additionallycompleted the TinnitusHandicapQuestionnaire (THQ [45])
NSCF No NSCF
tone
Arousal signaldetection of arousal
Nonarousal signaldetection of arousal
t
Figure 1 Description of the skin conductance task as measure ofinteroceptive accuracy as depicted in Andor et al (2008) NSCFnonspecific skin conductance fluctuation 119905 = time
and the Tinnitus Handicap Inventory (THI [46]) to quan-tify their tinnitus distress as well as visual analogue scales(VAS) covering the topics of perceived loudness annoyancedistress and handicap of their tinnitus
222 Skin Conductance Task Skin conductance was mea-sured with a Varioport (Becker Meditec Karlsruhe Ger-many) with a sampling rate of 16Hz Two silversilver chlo-ride electrodes with a contact surface area of 2 cm2 to whichisotonic paste was applied were used [47] The electrodeswere attached to the palm of the nondominant hand [48]The Variotest system (Gerhard Mutz Cologne Germany)identified online periods of stable skin conductance (noNSCF) and periods of phasic sympathetic activation (NSCF)for amore detailed description Andor et al [30] Participantswere instructed to focus on their body arousal during theentire task and indicate after each tone whether a tone waspreceded by an occurrence of body arousal (see Figure 1for an illustration of the task procedure) The algorithmwhether the program was scanned for a stable phase or afluctuation was pseudorandomized with the restriction thatthe two different types of phases were not signaled morethan two times in a row The same sequence was used for
4 BioMed Research International
Baseline Stressinduction
Stress conditionof the
Schandry task
Physicalexercise
Baselinecondition of theSchandry task
Exercisecondition
of the Schandrytask
Figure 2 Procedure of the Schandry task
all participants The search window for a stable phase or afluctuation was 150 s If the intended event occurred withinthis time frame the tone was presented otherwise no tonewas presented and the program continued with the next trialIf more than five trials were missed the subject was excludedfrom data analysis and the time window was shortened to30 sThe latter intended to ensure that all participants startedwith the same feeling into the second task for examplethey did not notice that the task was cancelled Usuallyparticipants are relaxed during this task and show only a fewfluctuations in the skin conductance In order to increasethe arousal level of the participants that is provoke morefluctuations two one-minute breaks were included in thetask in which participants were asked to talk about their lastvacation book or movie As participants are usually morearoused in the beginning of an experimental session than inlater phases we chose to conduct the skin conductance taskalways first before the Schandry task
223 Schandry Task In the second task interoceptive accu-racy was measured using the Schandry task [29] Participantswere instructed to count their heartbeat for an indicatedamount of timeThe electrocardiogram (ECG) wasmeasuredwith a technical device (NeXus-10 Mark II Mind MediaBV Herten Netherlands) using three silversilver chlorideelectrodes attached to the torso according to Einthoven leadII The ECG was sampled at a rate of 256Hz The trials werepresented with Presentation (Neurobehavioral Systems IncBerkeley CA USA)
Three within-subject conditions existed for this task abaseline condition with the classic Schandry task a conditionfollowing a social stress induction and a control conditionfollowing physical exercise on an ergometer (see Figure 2)Each condition consisted of five consecutive trials of differentlength (20 25 30 35 and 40 s) which were presented inrandomized order After each trial participants had 10 s toreport their heartbeat count to the investigator A 30-secondpause followed each trial The beginning and the end of eachtrial weremarked by a tone (onset tone 800Hz 300ms offsettone 500Hz 300ms)
Before the baseline Schandry task participantswere givenfive minutes to get used to the ECG and afterwards filled outthe good-and-badmood and agitation-tranquility scale of theMultidimensional Questionnaire of Mental State (Mehrdi-mensionaler BefindlichkeitsfragebogenMDBF [49] cf [50])to report on their current mental state Afterwards theSchandry task was presented Participants were asked to situpright with their back of the hands resting on their thighsThis and the explicit instruction to avoid any other auxiliarymeans (eg measuring the pulse with the fingertips) wereintended to ensure that the participants relied on their
interoception solely One test trial was conducted to makethe participants familiar with the task Then the baselineSchandry task with its five trials was presented followed bythe stress induction Here the participants performed thecognitive stress task of the Trier Social Stress Test [51] For fiveminutes participants had to repeatedly subtract 13 starting at1022 They were told to do this mental arithmetic task as fastand as accurate as possible In case of an error participantswere interrupted and told to start again at 1022 To furtherincrease stress the investigator said ldquoPlease calculate fasterrdquoMoreover participants were told that also the voice and theposture during this mathematical task would be analyzedand therefore he or she was videotaped during the task Toenhance stress levels through the additional factor of self-awareness participants could see themselves on a screenAfter the stress induction period participants again filled outthe MDBF The second block of five trials of the Schandrytask was presented followed by another completion of theMDBF Finally the last condition of the Schandry task startedheartbeat perception after physical exercise (five minutescycling on an ergometer)The investigator instructed the par-ticipant to either speed up or slowdown their cycling to adjusttheir average heart rate to the heart ratemeasured in the stressinduction phase Finally the third block of the Schandry taskwas conducted At the end of the experiment participantswere informed about the purpose of the experiment includ-ing the function of the stress induction
23 Analysis
231 Skin Conductance Task According to participantsrsquo abil-ity to detect NSCFs the sensitivity index 1198891015840 was calculated asfollows119885(hit rate) ndash119885(false alarm rate) If the hit rate equalsthe false alarms rate the index is zero implicating low sensi-tivity The higher 1198891015840 is the better the participants were ableto detect phasic internal arousal correctly Furthermore anindex to quantify bias C as response behavior was calculatedminus05lowast (119885(false alarm rate) +Z(hit rate)) It describes whetherthe participant had a conservative response behavior that isreporting more often no arousal than arousal or a liberalone that is reporting more often arousal irrespective of itsoccurrence The first is represented through an index higherthan 0 and the latter below 0 an index around 0 reflectsthat there is no tendency for example a balanced answeringbehavior
232 Schandry Task Data from the NeXus (including thetriggers from Presentation) was imported to the Polymanprogram (Bob Kemp amp Marco Roessen Den Haag Nether-lands) to quantify the participantsrsquo heartbeat Based on thisdata (recorded heartbeat) and the answers given by the
BioMed Research International 5
Tinnitus groupControl group
Bias
C (m
ean)
060
040
020
0
minus020
Figure 3Mean score for biasC in the control and the tinnitus groupError bars indicate the standard error
participants (counted heartbeat) during the experiment theheartbeat perception score was calculated (HBP HBP = 1 minus15 sum(|recorded heartbeats minus counted heartbeats|recordedheartbeats) (cf [11 52 53]))The better the performance thatis the accuracy of the given answers the higher the HBPThemaximal value is 1
3 Results
Twenty participants with chronic tinnitus (M= 428 years SD= 131 40 female) and twenty healthy control participantswithout tinnitus (M = 417 years SD = 129 40 female)were tested Groupswerematchedwith respect to age genderand level of education Unexpectedly the groups differ in theBody Mass Index (BMI) see Table 1
31 Questionnaires The 119905-test for independent samplesrevealed no significant differences between the two groupsregarding the self-report measures of interoception BAQ119905(38) =minus070119901 = 024 PBCS 119905(38) =minus008119901 = 047MAIA119905(38) =minus061119901 = 027The same is true for the SOMS 119905(38) =012 119901 = 091 PANAS-PA 119905(38) = minus046 119901 = 065 andPANAS-NA 119905(38) = 043 119901 = 067 (see Table 1)
32 Skin Conductance Task Due to too few spontaneous skinconductance fluctuations (less than 5) 12 participants hadto be excluded from the analysis yielding 15 participants inthe tinnitus group and 13 in the control group We found nodifference of the sensitivity index 1198891015840 between the groups in a119905-test for independent samples 119905(26) = 059 119901 = 028 and 119889= 022 (tinnitus groupM= minus014 SD = 130 and control groupM = 016 SD = 151) A trend was found for the bias C 119905(26)= 153 119901 = 007 119889 = 058 (see Figure 3 tinnitus group M =minus019 SD = 071 and control group M = 022 SD = 070)
ExerciseStressBaseline
700
600
500
400
MD
BF (s
um sc
ore)
Condition
Tinnitus groupControl group
Figure 4 Current mood throughout the Schandry task conditionsfor both groups Error bars indicate standard error MDBF Multidi-mensional Questionnaire of Mental State
33 Schandry Task All participants were included in theanalysis In order to check if we successfully implemented thethree conditions we compared the three consecutive currentmental state scores A repeated measures ANOVA with thefactors Condition (baseline versus stress versus exercise)and Group (tinnitus versus control) showed a significantdifference between the three conditions 119865(276) = 5312 119901 lt0001 and 1205782 = 067 (see Figure 4)
Simple contrasts revealed that the current mental stateafter the stress induction was significantly reduced comparedto baseline 119865(138) = 6221 119901 lt 0001 and the exercisecondition119865(138) = 7426119901 lt 0001Therewas no significantinteraction between group and condition 119865(276) = 147 119901 =024 and 1205782 = 004
Besides the self-report measure of mood we also evalu-ated heart rate in the three different conditions The lowestheart rate was found in the baseline condition (M = 7304SD = 1401) followed by the stress (M = 8590 SD = 1753) andthe exercise condition (M = 8820 SD = 1594) An ANOVAfor repeated measure with the factors Condition and Groupshowed again a significant difference for the conditions forthe heart rate values 119865(276) = 6068 119901 lt 0001 and 1205782 =062 Simple contrasts showed a significant difference in heartrate between baseline condition and both stress condition119865(138) = 4559 119901 lt 0001 and exercise condition 119865(138) =10611 119901 lt 0001 and a significant difference between thestress condition and the exercise condition 119865(138) = 653119901 = 002There was no significant interaction of group 119909 con-dition 119865(276) = 005 119901 = 096 and 1205782 = 000
Using a repeated measures ANOVA on the HBP valueswith the factors Condition and Group no main effect for
6 BioMed Research International
SportStressBaseline
HBP
(mea
n)068
064
060
056
052
ConditionTinnitus groupControl group
Figure 5 Heartbeat perception score (HBP) of the tinnitus andcontrol group in the three conditions (baseline stress and exercise)of the Schandry task Error bars indicate the standard error
groups with regard to HBP 119865(276) = 190 119901 = 016 nor aninteraction effect 119865(276) = 030 119901 = 073 was found (seeFigure 5)
34 Post Hoc Analysis An analysis of covariance (ANCOVA)for the performance in the Schandry task in the three condi-tions within the tinnitus group was conducted using tinnitusloudness as a covariate Bonferroni correction for multipletesting was appliedThis analysis revealed a significant differ-ence between the three conditions when controlling tinnitusloudness 119865(236) = 516 119901 = 002 as well as the interactioncondition 119909 loudness 119865(236) = 439 119901 = 004 (see Figure 6)A simple linear regression analysis to predict the performancein the Schandry task for the stress condition compared to thebaseline condition revealed a significant influence of tinnitusloudness119865(118) = 855119901 lt 001 and1198772 = 028 Amarginallysignificant effect was found for the influence of loudness onthe performance in the exercise condition 119865(118) = 399119901 = 006 and 1198772 = 018 Quiet tinnitus went along with anenhanced performance in the Schandry task especially inthe stress and exercise condition whereas loud tinnitus isaccompanied with a decreased performance in the stress andexercise task
A second ANCOVA for repeated measures for the per-formance in the Schandry task with BMI as covariate didnot reach significance level 119865(274) = 037 119901 gt 099 (againBonferroni corrected for multiple comparisons)
4 Discussion
We evaluated whether interoceptive sensibility and accuracyas key factors of interoception differed in a sample with
000
025
050
075
100
25 50 75
HBP
ConditionBaselineStressExercise
Tinnitus loudness
Figure 6 Correlation between the heart beat perception (HBP)score and tinnitus loudness The correlation is plotted separately forthe three conditions of the Schandry task Colored lines representthe linear regression lines for each condition
chronic tinnitus and healthy control subjects We found noclinically relevant differences between the groups neitherusing questionnaires (interoceptive sensibility) nor usingexperimental tasks (the Schandry task and a skin conduc-tance task interoceptive accuracy) However a trend in thebias measure C towards a more liberal perception of arousalthat is a higher preparedness to expect internal arousal in thetinnitus group was detected Furthermore tinnitus loudnessinfluenced performance on the Schandry task in the chronictinnitus group
In order to detect a clinically relevant influence of intero-ception on tinnitus we based our a priori power calculationson the averaged effect size from a review [32] for the Schandrytask which is the most field-tested and standardized taskfor interoception However our results show that changesin interoception in chronic tinnitus are not comparable toanxiety disorders
Our hypothesis that the tinnitus group might performbetter in interoceptive accuracy when stressed that is tryingto roughly simulate the cooccurrence of stress and tinnitusonset was not supported by the obtained experimentalresults Given the comparable heart frequency we assumedthat the origin of the heart beat differences stress or exercisemight have an influence on interoception Yet there was nodifference between performance in the two conditions noran interaction effect between group and condition Heartbeat elevation and the self-report of mental state after thestress induction reflect a successful manipulation Yet wedo not know how long the elevated stress level after theinduction lasted At least before the beginning of the exercisecondition the stress levels went back to normal It mightbe worth to enhance the stress level more persistently orldquorefreshrdquo the stress level between each trial in order to come
BioMed Research International 7
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
all participants The search window for a stable phase or afluctuation was 150 s If the intended event occurred withinthis time frame the tone was presented otherwise no tonewas presented and the program continued with the next trialIf more than five trials were missed the subject was excludedfrom data analysis and the time window was shortened to30 sThe latter intended to ensure that all participants startedwith the same feeling into the second task for examplethey did not notice that the task was cancelled Usuallyparticipants are relaxed during this task and show only a fewfluctuations in the skin conductance In order to increasethe arousal level of the participants that is provoke morefluctuations two one-minute breaks were included in thetask in which participants were asked to talk about their lastvacation book or movie As participants are usually morearoused in the beginning of an experimental session than inlater phases we chose to conduct the skin conductance taskalways first before the Schandry task
223 Schandry Task In the second task interoceptive accu-racy was measured using the Schandry task [29] Participantswere instructed to count their heartbeat for an indicatedamount of timeThe electrocardiogram (ECG) wasmeasuredwith a technical device (NeXus-10 Mark II Mind MediaBV Herten Netherlands) using three silversilver chlorideelectrodes attached to the torso according to Einthoven leadII The ECG was sampled at a rate of 256Hz The trials werepresented with Presentation (Neurobehavioral Systems IncBerkeley CA USA)
Three within-subject conditions existed for this task abaseline condition with the classic Schandry task a conditionfollowing a social stress induction and a control conditionfollowing physical exercise on an ergometer (see Figure 2)Each condition consisted of five consecutive trials of differentlength (20 25 30 35 and 40 s) which were presented inrandomized order After each trial participants had 10 s toreport their heartbeat count to the investigator A 30-secondpause followed each trial The beginning and the end of eachtrial weremarked by a tone (onset tone 800Hz 300ms offsettone 500Hz 300ms)
Before the baseline Schandry task participantswere givenfive minutes to get used to the ECG and afterwards filled outthe good-and-badmood and agitation-tranquility scale of theMultidimensional Questionnaire of Mental State (Mehrdi-mensionaler BefindlichkeitsfragebogenMDBF [49] cf [50])to report on their current mental state Afterwards theSchandry task was presented Participants were asked to situpright with their back of the hands resting on their thighsThis and the explicit instruction to avoid any other auxiliarymeans (eg measuring the pulse with the fingertips) wereintended to ensure that the participants relied on their
interoception solely One test trial was conducted to makethe participants familiar with the task Then the baselineSchandry task with its five trials was presented followed bythe stress induction Here the participants performed thecognitive stress task of the Trier Social Stress Test [51] For fiveminutes participants had to repeatedly subtract 13 starting at1022 They were told to do this mental arithmetic task as fastand as accurate as possible In case of an error participantswere interrupted and told to start again at 1022 To furtherincrease stress the investigator said ldquoPlease calculate fasterrdquoMoreover participants were told that also the voice and theposture during this mathematical task would be analyzedand therefore he or she was videotaped during the task Toenhance stress levels through the additional factor of self-awareness participants could see themselves on a screenAfter the stress induction period participants again filled outthe MDBF The second block of five trials of the Schandrytask was presented followed by another completion of theMDBF Finally the last condition of the Schandry task startedheartbeat perception after physical exercise (five minutescycling on an ergometer)The investigator instructed the par-ticipant to either speed up or slowdown their cycling to adjusttheir average heart rate to the heart ratemeasured in the stressinduction phase Finally the third block of the Schandry taskwas conducted At the end of the experiment participantswere informed about the purpose of the experiment includ-ing the function of the stress induction
23 Analysis
231 Skin Conductance Task According to participantsrsquo abil-ity to detect NSCFs the sensitivity index 1198891015840 was calculated asfollows119885(hit rate) ndash119885(false alarm rate) If the hit rate equalsthe false alarms rate the index is zero implicating low sensi-tivity The higher 1198891015840 is the better the participants were ableto detect phasic internal arousal correctly Furthermore anindex to quantify bias C as response behavior was calculatedminus05lowast (119885(false alarm rate) +Z(hit rate)) It describes whetherthe participant had a conservative response behavior that isreporting more often no arousal than arousal or a liberalone that is reporting more often arousal irrespective of itsoccurrence The first is represented through an index higherthan 0 and the latter below 0 an index around 0 reflectsthat there is no tendency for example a balanced answeringbehavior
232 Schandry Task Data from the NeXus (including thetriggers from Presentation) was imported to the Polymanprogram (Bob Kemp amp Marco Roessen Den Haag Nether-lands) to quantify the participantsrsquo heartbeat Based on thisdata (recorded heartbeat) and the answers given by the
BioMed Research International 5
Tinnitus groupControl group
Bias
C (m
ean)
060
040
020
0
minus020
Figure 3Mean score for biasC in the control and the tinnitus groupError bars indicate the standard error
participants (counted heartbeat) during the experiment theheartbeat perception score was calculated (HBP HBP = 1 minus15 sum(|recorded heartbeats minus counted heartbeats|recordedheartbeats) (cf [11 52 53]))The better the performance thatis the accuracy of the given answers the higher the HBPThemaximal value is 1
3 Results
Twenty participants with chronic tinnitus (M= 428 years SD= 131 40 female) and twenty healthy control participantswithout tinnitus (M = 417 years SD = 129 40 female)were tested Groupswerematchedwith respect to age genderand level of education Unexpectedly the groups differ in theBody Mass Index (BMI) see Table 1
31 Questionnaires The 119905-test for independent samplesrevealed no significant differences between the two groupsregarding the self-report measures of interoception BAQ119905(38) =minus070119901 = 024 PBCS 119905(38) =minus008119901 = 047MAIA119905(38) =minus061119901 = 027The same is true for the SOMS 119905(38) =012 119901 = 091 PANAS-PA 119905(38) = minus046 119901 = 065 andPANAS-NA 119905(38) = 043 119901 = 067 (see Table 1)
32 Skin Conductance Task Due to too few spontaneous skinconductance fluctuations (less than 5) 12 participants hadto be excluded from the analysis yielding 15 participants inthe tinnitus group and 13 in the control group We found nodifference of the sensitivity index 1198891015840 between the groups in a119905-test for independent samples 119905(26) = 059 119901 = 028 and 119889= 022 (tinnitus groupM= minus014 SD = 130 and control groupM = 016 SD = 151) A trend was found for the bias C 119905(26)= 153 119901 = 007 119889 = 058 (see Figure 3 tinnitus group M =minus019 SD = 071 and control group M = 022 SD = 070)
ExerciseStressBaseline
700
600
500
400
MD
BF (s
um sc
ore)
Condition
Tinnitus groupControl group
Figure 4 Current mood throughout the Schandry task conditionsfor both groups Error bars indicate standard error MDBF Multidi-mensional Questionnaire of Mental State
33 Schandry Task All participants were included in theanalysis In order to check if we successfully implemented thethree conditions we compared the three consecutive currentmental state scores A repeated measures ANOVA with thefactors Condition (baseline versus stress versus exercise)and Group (tinnitus versus control) showed a significantdifference between the three conditions 119865(276) = 5312 119901 lt0001 and 1205782 = 067 (see Figure 4)
Simple contrasts revealed that the current mental stateafter the stress induction was significantly reduced comparedto baseline 119865(138) = 6221 119901 lt 0001 and the exercisecondition119865(138) = 7426119901 lt 0001Therewas no significantinteraction between group and condition 119865(276) = 147 119901 =024 and 1205782 = 004
Besides the self-report measure of mood we also evalu-ated heart rate in the three different conditions The lowestheart rate was found in the baseline condition (M = 7304SD = 1401) followed by the stress (M = 8590 SD = 1753) andthe exercise condition (M = 8820 SD = 1594) An ANOVAfor repeated measure with the factors Condition and Groupshowed again a significant difference for the conditions forthe heart rate values 119865(276) = 6068 119901 lt 0001 and 1205782 =062 Simple contrasts showed a significant difference in heartrate between baseline condition and both stress condition119865(138) = 4559 119901 lt 0001 and exercise condition 119865(138) =10611 119901 lt 0001 and a significant difference between thestress condition and the exercise condition 119865(138) = 653119901 = 002There was no significant interaction of group 119909 con-dition 119865(276) = 005 119901 = 096 and 1205782 = 000
Using a repeated measures ANOVA on the HBP valueswith the factors Condition and Group no main effect for
6 BioMed Research International
SportStressBaseline
HBP
(mea
n)068
064
060
056
052
ConditionTinnitus groupControl group
Figure 5 Heartbeat perception score (HBP) of the tinnitus andcontrol group in the three conditions (baseline stress and exercise)of the Schandry task Error bars indicate the standard error
groups with regard to HBP 119865(276) = 190 119901 = 016 nor aninteraction effect 119865(276) = 030 119901 = 073 was found (seeFigure 5)
34 Post Hoc Analysis An analysis of covariance (ANCOVA)for the performance in the Schandry task in the three condi-tions within the tinnitus group was conducted using tinnitusloudness as a covariate Bonferroni correction for multipletesting was appliedThis analysis revealed a significant differ-ence between the three conditions when controlling tinnitusloudness 119865(236) = 516 119901 = 002 as well as the interactioncondition 119909 loudness 119865(236) = 439 119901 = 004 (see Figure 6)A simple linear regression analysis to predict the performancein the Schandry task for the stress condition compared to thebaseline condition revealed a significant influence of tinnitusloudness119865(118) = 855119901 lt 001 and1198772 = 028 Amarginallysignificant effect was found for the influence of loudness onthe performance in the exercise condition 119865(118) = 399119901 = 006 and 1198772 = 018 Quiet tinnitus went along with anenhanced performance in the Schandry task especially inthe stress and exercise condition whereas loud tinnitus isaccompanied with a decreased performance in the stress andexercise task
A second ANCOVA for repeated measures for the per-formance in the Schandry task with BMI as covariate didnot reach significance level 119865(274) = 037 119901 gt 099 (againBonferroni corrected for multiple comparisons)
4 Discussion
We evaluated whether interoceptive sensibility and accuracyas key factors of interoception differed in a sample with
000
025
050
075
100
25 50 75
HBP
ConditionBaselineStressExercise
Tinnitus loudness
Figure 6 Correlation between the heart beat perception (HBP)score and tinnitus loudness The correlation is plotted separately forthe three conditions of the Schandry task Colored lines representthe linear regression lines for each condition
chronic tinnitus and healthy control subjects We found noclinically relevant differences between the groups neitherusing questionnaires (interoceptive sensibility) nor usingexperimental tasks (the Schandry task and a skin conduc-tance task interoceptive accuracy) However a trend in thebias measure C towards a more liberal perception of arousalthat is a higher preparedness to expect internal arousal in thetinnitus group was detected Furthermore tinnitus loudnessinfluenced performance on the Schandry task in the chronictinnitus group
In order to detect a clinically relevant influence of intero-ception on tinnitus we based our a priori power calculationson the averaged effect size from a review [32] for the Schandrytask which is the most field-tested and standardized taskfor interoception However our results show that changesin interoception in chronic tinnitus are not comparable toanxiety disorders
Our hypothesis that the tinnitus group might performbetter in interoceptive accuracy when stressed that is tryingto roughly simulate the cooccurrence of stress and tinnitusonset was not supported by the obtained experimentalresults Given the comparable heart frequency we assumedthat the origin of the heart beat differences stress or exercisemight have an influence on interoception Yet there was nodifference between performance in the two conditions noran interaction effect between group and condition Heartbeat elevation and the self-report of mental state after thestress induction reflect a successful manipulation Yet wedo not know how long the elevated stress level after theinduction lasted At least before the beginning of the exercisecondition the stress levels went back to normal It mightbe worth to enhance the stress level more persistently orldquorefreshrdquo the stress level between each trial in order to come
BioMed Research International 7
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
Figure 3Mean score for biasC in the control and the tinnitus groupError bars indicate the standard error
participants (counted heartbeat) during the experiment theheartbeat perception score was calculated (HBP HBP = 1 minus15 sum(|recorded heartbeats minus counted heartbeats|recordedheartbeats) (cf [11 52 53]))The better the performance thatis the accuracy of the given answers the higher the HBPThemaximal value is 1
3 Results
Twenty participants with chronic tinnitus (M= 428 years SD= 131 40 female) and twenty healthy control participantswithout tinnitus (M = 417 years SD = 129 40 female)were tested Groupswerematchedwith respect to age genderand level of education Unexpectedly the groups differ in theBody Mass Index (BMI) see Table 1
31 Questionnaires The 119905-test for independent samplesrevealed no significant differences between the two groupsregarding the self-report measures of interoception BAQ119905(38) =minus070119901 = 024 PBCS 119905(38) =minus008119901 = 047MAIA119905(38) =minus061119901 = 027The same is true for the SOMS 119905(38) =012 119901 = 091 PANAS-PA 119905(38) = minus046 119901 = 065 andPANAS-NA 119905(38) = 043 119901 = 067 (see Table 1)
32 Skin Conductance Task Due to too few spontaneous skinconductance fluctuations (less than 5) 12 participants hadto be excluded from the analysis yielding 15 participants inthe tinnitus group and 13 in the control group We found nodifference of the sensitivity index 1198891015840 between the groups in a119905-test for independent samples 119905(26) = 059 119901 = 028 and 119889= 022 (tinnitus groupM= minus014 SD = 130 and control groupM = 016 SD = 151) A trend was found for the bias C 119905(26)= 153 119901 = 007 119889 = 058 (see Figure 3 tinnitus group M =minus019 SD = 071 and control group M = 022 SD = 070)
ExerciseStressBaseline
700
600
500
400
MD
BF (s
um sc
ore)
Condition
Tinnitus groupControl group
Figure 4 Current mood throughout the Schandry task conditionsfor both groups Error bars indicate standard error MDBF Multidi-mensional Questionnaire of Mental State
33 Schandry Task All participants were included in theanalysis In order to check if we successfully implemented thethree conditions we compared the three consecutive currentmental state scores A repeated measures ANOVA with thefactors Condition (baseline versus stress versus exercise)and Group (tinnitus versus control) showed a significantdifference between the three conditions 119865(276) = 5312 119901 lt0001 and 1205782 = 067 (see Figure 4)
Simple contrasts revealed that the current mental stateafter the stress induction was significantly reduced comparedto baseline 119865(138) = 6221 119901 lt 0001 and the exercisecondition119865(138) = 7426119901 lt 0001Therewas no significantinteraction between group and condition 119865(276) = 147 119901 =024 and 1205782 = 004
Besides the self-report measure of mood we also evalu-ated heart rate in the three different conditions The lowestheart rate was found in the baseline condition (M = 7304SD = 1401) followed by the stress (M = 8590 SD = 1753) andthe exercise condition (M = 8820 SD = 1594) An ANOVAfor repeated measure with the factors Condition and Groupshowed again a significant difference for the conditions forthe heart rate values 119865(276) = 6068 119901 lt 0001 and 1205782 =062 Simple contrasts showed a significant difference in heartrate between baseline condition and both stress condition119865(138) = 4559 119901 lt 0001 and exercise condition 119865(138) =10611 119901 lt 0001 and a significant difference between thestress condition and the exercise condition 119865(138) = 653119901 = 002There was no significant interaction of group 119909 con-dition 119865(276) = 005 119901 = 096 and 1205782 = 000
Using a repeated measures ANOVA on the HBP valueswith the factors Condition and Group no main effect for
6 BioMed Research International
SportStressBaseline
HBP
(mea
n)068
064
060
056
052
ConditionTinnitus groupControl group
Figure 5 Heartbeat perception score (HBP) of the tinnitus andcontrol group in the three conditions (baseline stress and exercise)of the Schandry task Error bars indicate the standard error
groups with regard to HBP 119865(276) = 190 119901 = 016 nor aninteraction effect 119865(276) = 030 119901 = 073 was found (seeFigure 5)
34 Post Hoc Analysis An analysis of covariance (ANCOVA)for the performance in the Schandry task in the three condi-tions within the tinnitus group was conducted using tinnitusloudness as a covariate Bonferroni correction for multipletesting was appliedThis analysis revealed a significant differ-ence between the three conditions when controlling tinnitusloudness 119865(236) = 516 119901 = 002 as well as the interactioncondition 119909 loudness 119865(236) = 439 119901 = 004 (see Figure 6)A simple linear regression analysis to predict the performancein the Schandry task for the stress condition compared to thebaseline condition revealed a significant influence of tinnitusloudness119865(118) = 855119901 lt 001 and1198772 = 028 Amarginallysignificant effect was found for the influence of loudness onthe performance in the exercise condition 119865(118) = 399119901 = 006 and 1198772 = 018 Quiet tinnitus went along with anenhanced performance in the Schandry task especially inthe stress and exercise condition whereas loud tinnitus isaccompanied with a decreased performance in the stress andexercise task
A second ANCOVA for repeated measures for the per-formance in the Schandry task with BMI as covariate didnot reach significance level 119865(274) = 037 119901 gt 099 (againBonferroni corrected for multiple comparisons)
4 Discussion
We evaluated whether interoceptive sensibility and accuracyas key factors of interoception differed in a sample with
000
025
050
075
100
25 50 75
HBP
ConditionBaselineStressExercise
Tinnitus loudness
Figure 6 Correlation between the heart beat perception (HBP)score and tinnitus loudness The correlation is plotted separately forthe three conditions of the Schandry task Colored lines representthe linear regression lines for each condition
chronic tinnitus and healthy control subjects We found noclinically relevant differences between the groups neitherusing questionnaires (interoceptive sensibility) nor usingexperimental tasks (the Schandry task and a skin conduc-tance task interoceptive accuracy) However a trend in thebias measure C towards a more liberal perception of arousalthat is a higher preparedness to expect internal arousal in thetinnitus group was detected Furthermore tinnitus loudnessinfluenced performance on the Schandry task in the chronictinnitus group
In order to detect a clinically relevant influence of intero-ception on tinnitus we based our a priori power calculationson the averaged effect size from a review [32] for the Schandrytask which is the most field-tested and standardized taskfor interoception However our results show that changesin interoception in chronic tinnitus are not comparable toanxiety disorders
Our hypothesis that the tinnitus group might performbetter in interoceptive accuracy when stressed that is tryingto roughly simulate the cooccurrence of stress and tinnitusonset was not supported by the obtained experimentalresults Given the comparable heart frequency we assumedthat the origin of the heart beat differences stress or exercisemight have an influence on interoception Yet there was nodifference between performance in the two conditions noran interaction effect between group and condition Heartbeat elevation and the self-report of mental state after thestress induction reflect a successful manipulation Yet wedo not know how long the elevated stress level after theinduction lasted At least before the beginning of the exercisecondition the stress levels went back to normal It mightbe worth to enhance the stress level more persistently orldquorefreshrdquo the stress level between each trial in order to come
BioMed Research International 7
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
Figure 5 Heartbeat perception score (HBP) of the tinnitus andcontrol group in the three conditions (baseline stress and exercise)of the Schandry task Error bars indicate the standard error
groups with regard to HBP 119865(276) = 190 119901 = 016 nor aninteraction effect 119865(276) = 030 119901 = 073 was found (seeFigure 5)
34 Post Hoc Analysis An analysis of covariance (ANCOVA)for the performance in the Schandry task in the three condi-tions within the tinnitus group was conducted using tinnitusloudness as a covariate Bonferroni correction for multipletesting was appliedThis analysis revealed a significant differ-ence between the three conditions when controlling tinnitusloudness 119865(236) = 516 119901 = 002 as well as the interactioncondition 119909 loudness 119865(236) = 439 119901 = 004 (see Figure 6)A simple linear regression analysis to predict the performancein the Schandry task for the stress condition compared to thebaseline condition revealed a significant influence of tinnitusloudness119865(118) = 855119901 lt 001 and1198772 = 028 Amarginallysignificant effect was found for the influence of loudness onthe performance in the exercise condition 119865(118) = 399119901 = 006 and 1198772 = 018 Quiet tinnitus went along with anenhanced performance in the Schandry task especially inthe stress and exercise condition whereas loud tinnitus isaccompanied with a decreased performance in the stress andexercise task
A second ANCOVA for repeated measures for the per-formance in the Schandry task with BMI as covariate didnot reach significance level 119865(274) = 037 119901 gt 099 (againBonferroni corrected for multiple comparisons)
4 Discussion
We evaluated whether interoceptive sensibility and accuracyas key factors of interoception differed in a sample with
000
025
050
075
100
25 50 75
HBP
ConditionBaselineStressExercise
Tinnitus loudness
Figure 6 Correlation between the heart beat perception (HBP)score and tinnitus loudness The correlation is plotted separately forthe three conditions of the Schandry task Colored lines representthe linear regression lines for each condition
chronic tinnitus and healthy control subjects We found noclinically relevant differences between the groups neitherusing questionnaires (interoceptive sensibility) nor usingexperimental tasks (the Schandry task and a skin conduc-tance task interoceptive accuracy) However a trend in thebias measure C towards a more liberal perception of arousalthat is a higher preparedness to expect internal arousal in thetinnitus group was detected Furthermore tinnitus loudnessinfluenced performance on the Schandry task in the chronictinnitus group
In order to detect a clinically relevant influence of intero-ception on tinnitus we based our a priori power calculationson the averaged effect size from a review [32] for the Schandrytask which is the most field-tested and standardized taskfor interoception However our results show that changesin interoception in chronic tinnitus are not comparable toanxiety disorders
Our hypothesis that the tinnitus group might performbetter in interoceptive accuracy when stressed that is tryingto roughly simulate the cooccurrence of stress and tinnitusonset was not supported by the obtained experimentalresults Given the comparable heart frequency we assumedthat the origin of the heart beat differences stress or exercisemight have an influence on interoception Yet there was nodifference between performance in the two conditions noran interaction effect between group and condition Heartbeat elevation and the self-report of mental state after thestress induction reflect a successful manipulation Yet wedo not know how long the elevated stress level after theinduction lasted At least before the beginning of the exercisecondition the stress levels went back to normal It mightbe worth to enhance the stress level more persistently orldquorefreshrdquo the stress level between each trial in order to come
BioMed Research International 7
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
to a final conclusion about the connection of stress level andinteroceptive accuracy
If we evaluate loudness of the tinnitus as a covariate forthe Schandry task performance we find a significant differ-ence for the conditions in the Schandry task The louder thetinnitus the worse the heart beat perception performance inthe stress and exercise condition In the baseline conditionthe cognitive load is lower and the cognitive resources are notyet depleted Thus it can be hypothesized that with a quiettinnitus perception attention shifts are still possible as theparticipants were able to take away their attention from thetinnitus and focus on the task If the tinnitus is especially loudthis might reduce the capacity to direct the attention awayfrom the tinnitus towards perception of the heartbeat Thisis in line with previous findings of difficulties of especiallysevere tinnitus sufferers on selective and divided attention[54 55]
As the BMI negatively correlates with interoceptive accu-racy for the heartbeat [56] the significant difference betweenthe groups regarding this factor may have influenced theresults as well However using BMI as covariate did notchange our results
The skin conductance task especially suffered from a lowpower due to its novelty effect sizes were difficult to estimateand in addition we encountered an unexpectedly significantnumber of dropouts Furthermore both groups had a low 1198891015840score representing guessing probability in this task Whereasthis finding is not completely surprising given that in thetwo previous studies 1198891015840 scores in healthy control groups werealso low in our study the 1198891015840 scores were lower than whatwas previously found [28 30] Obviously the task was toodifficult for both groups and the especially low 1198891015840 scoresrender it unlikely that chronic tinnitus sufferers are especiallyadept at perceiving phasic sympathetic arousal as indexed bynonspecific skin conductance fluctuations
Notwithstanding the bias C calculation is interestingThisfinding adumbrates that the tinnitus group tends to perceive abodily sensation regardless of its actual physical occurrenceThis perception biasmight also apply to internal acoustic sen-sations and might be a starting point for a tinnitus sensationAnother possible explanation for the current results might bethat people suffering from tinnitus may only have specificallyincreased interoception for internal acoustic processes whichwould not be detected through themeasures used in the studyat hand Albeit we try to cover the concept of interoceptionas broad as possible those measures might have been toocoarse to detect this idea about specific and solely auditoryinteroception
In contrast to these findings of interoceptive accuracyanother study found a reduced discrimination of externalelectromagnetically evoked stimuli [57] In the future itmight be interesting to investigate the relationship betweenextro- and interoception in tinnitus
Overall our populationwas lowly distressed through theirtinnitus According to severity grading [58] 45 of oursubjects had negligible tinnitus which is only audible in quietsurroundings 40 a light tinnitus which can easily beignored and the rest mild tinnitus where daily functioningis not impaired The two more severe categories were not
represented within our study Through our screening formental disorders we might have likewise excluded highlydistressed tinnitus sufferers as high distress in tinnitus is oftenaccompanied by a mental disorder [59] We would assumethat in a high distressed group interoceptive processes mightbe more pronounced This is also a key distinctive charac-teristic which varies between our study and the studies oninteroception in mental disorders In order to be diagnosedwith a mental disorder high distress and impairment arenecessary in the study at hand we explicitly excluded partic-ipants based on this aspect
Concluding as first study in this field we tried to trackdown interoception in tinnitusWe took recent developmentsinto consideration and systematically analyzed differentaspects of interoception In order to exclude confounders ofinteroception we matched the two groups and profoundlyscreened for mental disorders Despite our reasoning we didnot detect any main differences between a tinnitus group anda group of healthy controls regarding interoceptive accuracyand sensibility If there are differences in the interoceptionbetween the two groups the impact is not comparable toother disorders for example panic disorder and eating dis-orders Yet we found that tinnitus sufferers might have a biasto perceive bodily symptoms irrespective of a physiologicalbasis Finally we found that the loudness of tinnitus goesalongwith a decrease in performance in cognitive demandingtasks We think it might be worth to further investigatethe bias effect on the tinnitus population and to continueto complete the analysis of clinically relevant psychologicalvariables influencing tinnitus and its distress
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The authors are grateful to Gerhard Mutz Karin Berningand Louisa Hegermann for support in the measurementsThis research was supported by DFG (PA 39214-1) andInterdisziplinares Zentrum fur klinische Forschung (IZKFCRA05)
References
[1] R R Coles ldquoEpidemiology of tinnitus (1) prevalencerdquoThe Jour-nal of Laryngology amp Otology vol 98 supplement 9 pp 7ndash151984
[2] R A Dobie ldquoDepression and tinnitusrdquo Otolaryngologic Clinicsof North America vol 36 no 2 pp 383ndash388 2003
[3] C Pantev H Okamoto and H Teismann ldquoTinnitus the darkside of the auditory cortex plasticityrdquo Annals of the New YorkAcademy of Sciences vol 1252 no 1 pp 253ndash258 2012
[4] W Schlee N Mueller T Hartmann J Keil I Lorenz and NWeisz ldquoMapping cortical hubs in tinnitusrdquo BMC Biology vol 7article 80 2009
8 BioMed Research International
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
[5] G Andersson and L McKenna ldquoThe role of cognition in tinn-itusrdquoActa Oto-LlaryngologicamdashSupplementum no 556 pp 39ndash43 2006
[6] D De Ridder S Vanneste NWeisz et al ldquoAn integrativemodelof auditory phantom perception tinnitus as a unified percept ofinteracting separable subnetworksrdquo Neuroscience amp Biobehav-ioral Reviews vol 44 pp 16ndash32 2014
[7] L McKenna L Handscomb D J Hoare and D A Hall ldquoA sci-entific cognitive-behavioral model of tinnitus novel concep-tualizations of tinnitus distressrdquo Frontiers in Neurology vol 5article 196 15 pages 2014
[8] D M Clark ldquoA cognitive approach to panicrdquo BehaviourResearch andTherapy vol 24 no 4 pp 461ndash470 1986
[9] S Reiss and R J McNally ldquoThe expectancy model of fearrdquo inTheoretical Issues in Behavior Therapy pp 107ndash122 AcademicPress 1985
[10] S N Garfinkel and H D Critchley ldquoInteroception emotionand brain new insights link internal physiology to social behav-iour Commentary on lsquoanterior insular cortex mediates bodilysensibility and social anxietyrsquo by Terasawa et al (2012)rdquo SocialCognitive and Affective Neuroscience vol 8 no 3 pp 231ndash2342013
[11] M Klabunde D T Acheson KN Boutelle S CMatthews andW H Kaye ldquoInteroceptive sensitivity deficits in women recov-ered from bulimia nervosardquo Eating Behaviors vol 14 no 4 pp488ndash492 2013
[12] O Pollatos A-L Kurz J Albrecht et al ldquoReduced perceptionof bodily signals in anorexia nervosardquo Eating Behaviors vol 9no 4 pp 381ndash388 2008
[13] M Schaefer B Egloff andMWitthoft ldquoIs interoceptive aware-ness really altered in somatoform disorders Testing competingtheories with two paradigms of heartbeat perceptionrdquo Journalof Abnormal Psychology vol 121 no 3 pp 719ndash724 2012
[14] L F Barrett K S Quigley E Bliss-Moreau and K R AronsonldquoInteroceptive sensitivity and self-reports of emotional experi-encerdquo Journal of Personality and Social Psychology vol 87 no 5pp 684ndash697 2004
[15] O Pollatos and R Schandry ldquoEmotional processing and emo-tional memory are modulated by interoceptive awarenessrdquoCognition and Emotion vol 22 no 2 pp 272ndash287 2008
[16] B M Herbert C Herbert and O Pollatos ldquoOn the relationshipbetween interoceptive awareness and alexithymia is intero-ceptive awareness related to emotional awarenessrdquo Journal ofPersonality vol 79 no 5 pp 1149ndash1175 2011
[17] J Salonen R Johansson and M Joukamaa ldquoAlexithymiadepression and tinnitus in elderly peoplerdquo General HospitalPsychiatry vol 29 no 5 pp 431ndash435 2007
[18] M R Laureano E T Onishi R A Bressan et al ldquoMemory net-works in tinnitus a functional brain image studyrdquo PLoS ONEvol 9 no 2 Article ID e87839 2014
[19] H-U W T Lang S Helbig-Lang D Westphal and A TGloster Expositionsbasierte Therapie der Panikstorung mit Ago-raphobie Ein Behandlungsmanual Broschiert 22nd edition2011
[20] G G Birgit Kroner-Herwig and B Jager Tinnitus Kognitiv-ver-haltenstherapeutisches Behandlungsmanual Mit Online-Materi-alien 2010
[21] B Kroner-Herwig A Frenzel G Fritsche G Schilkowsky andG Esser ldquoThe management of chronic tinnitus comparison ofan outpatient cognitive-behavioral group training to minimal-contact interventionsrdquo Journal of Psychosomatic Research vol54 no 4 pp 381ndash389 2003
[22] A D Craig ldquoInteroception the sense of the physiological con-dition of the bodyrdquoCurrent Opinion in Neurobiology vol 13 no4 pp 500ndash505 2003
[23] H D Critchley S Wiens P Rotshtein A Ohman and R JDolan ldquoNeural systems supporting interoceptive awarenessrdquoNature Neuroscience vol 7 no 2 pp 189ndash195 2004
[24] A H Lockwood R J Salvi M L Coad M L Towsley D SWack and B W Murphy ldquoThe functional neuroanatomy oftinnitus evidence for limbic system links and neural plasticityrdquoNeurology vol 50 no 1 pp 114ndash120 1998
[25] S Vanneste M Plazier E Van der Loo M Congedo and D DeRidder ldquoThe neural correlates of tinnitus-related distressrdquoNeu-roImage vol 52 no 2 pp 470ndash480 2010
[26] E van der Loo M Congedo S Vanneste P Van De Heyningand D De Ridder ldquoInsular lateralization in tinnitus distressrdquoAutonomic Neuroscience Basic and Clinical vol 165 no 2 pp191ndash194 2011
[27] S N Garfinkel A K Seth A B Barrett K Suzuki and H DCritchley ldquoKnowing your own heart distinguishing interocep-tive accuracy from interoceptive awarenessrdquo Biological Psychol-ogy vol 104 pp 65ndash74 2015
[28] S Krautwurst A L Gerlach L Gomille W Hiller and MWitthoft ldquoHealth anxietymdashan indicator of higher interoceptivesensitivityrdquo Journal of Behavior Therapy and ExperimentalPsychiatry vol 45 no 2 pp 303ndash309 2014
[29] R Schandry ldquoHeart beat perception and emotional experiencerdquoPsychophysiology vol 18 no 4 pp 483ndash488 1981
[30] T Andor A L Gerlach and F Rist ldquoSuperior perception ofphasic physiological arousal and the detrimental consequencesof the conviction to be aroused onworrying andmetacognitionsin GADrdquo Journal of Abnormal Psychology vol 117 no 1 pp 193ndash205 2008
[31] AKatzerDOberfeldWHiller A LGerlach andMWitthoftldquoTactile perceptual processes and their relationship to somato-form disordersrdquo Journal of Abnormal Psychology vol 121 no 2pp 530ndash543 2012
[32] KDomschke S Stevens B Pfleiderer andA LGerlach ldquoInter-oceptive sensitivity in anxiety and anxiety disorders anoverview and integration of neurobiological findingsrdquo ClinicalPsychology Review vol 30 no 1 pp 1ndash11 2010
[33] BMazurek T Stover HHaupt et al ldquoThe significance of stressits role in the auditory system and the pathogenesis of tinnitusrdquoHNO vol 58 no 2 pp 162ndash172 2010
[34] A Baigi A Oden V Almlid-LarsenM-L Barrenas and K-MHolgers ldquoTinnitus in the general population with a focus onnoise and stress a public health studyrdquo Ear and Hearing vol 32no 6 pp 787ndash789 2011
[35] S Hebert and S J Lupien ldquoThe sound of stress blunted cortisolreactivity to psychosocial stress in tinnitus sufferersrdquo Neuro-science Letters vol 411 no 2 pp 138ndash142 2007
[36] M Wittchen H-U Wunderlich U Gruschwitz and S ZaudigSKID ImdashStrukturiertes Klinisches Interview fur DSM-IVmdashAchsemdashI Psychische Storungen Hogrefe Gottingen Germany1997
[37] W E Mehling V Gopisetty J Daubenmier C J Price F MHecht and A Stewart ldquoBody awareness construct and self-report measuresrdquo PLoS ONE vol 4 no 5 Article ID e56142009
[38] S A ShieldsM EMallory andA Simon ldquoThe body awarenessquestionnaire reliability and validityrdquo Journal of PersonalityAssessment vol 53 no 4 pp 802ndash815 1989
BioMed Research International 9
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
[39] L C Miller R Murphy and A H Buss ldquoConsciousness ofbody private and publicrdquo Journal of Personality and Social Psy-chology vol 41 no 2 pp 397ndash406 1981
[40] W EMehling C Price J J DaubenmierMAcree E Bartmessand A Stewart ldquoThe multidimensional assessment of intero-ceptive awareness (MAIA)rdquo PLoS ONE vol 7 no 11 Article IDe48230 2012
[41] A J Christensen J S Wiebe D L Edwards J D Michels andW J Lawton ldquoBody consciousness illness-related impairmentand patient adherence in hemodialysisrdquo Journal of Consultingand Clinical Psychology vol 64 no 1 pp 147ndash152 1996
[42] B Bornemann B M Herbert W E Mehling and T SingerldquoDifferential changes in self-reported aspects of interoceptiveawareness through 3 months of contemplative trainingrdquo Fron-tiers in Psychology vol 5 article 1504 13 pages 2015
[43] DWatson L A Clark and A Tellegen ldquoDevelopment and val-idation of brief measures of positive and negative affect thePANAS scalesrdquo Journal of Personality and Social Psychology vol54 no 6 pp 1063ndash1070 1988
[44] J Rief W Hiller and W Heuser SOMS das Screening fursomatoforme Storungen Manual zum Fragebogen [SOMSScreening for Somatoform Disorders The Questionnaire Man-ual] Hubors Bern Switzerland 1997
[45] F K Kuk R S Tyler D Russell and H Jordan ldquoThe psycho-metric properties of a tinnitus handicap questionnairerdquo Ear andHearing vol 11 no 6 pp 434ndash445 1990
[46] C W Newman G P Jacobson and J B Spitzer ldquoDevelopmentof the tinnitus handicap inventoryrdquo Archives of Otolaryngol-ogymdashHead and Neck Surgery vol 122 no 2 pp 143ndash148 1996
[47] D C Fowles M J Christie R Edelberg W W Grings D TLykken and P H Venables ldquoCommittee report Publicationrecommendations for electrodermal measurementsrdquo Psycho-physiology vol 18 pp 232ndash239 1981
[48] W Boucsein Elektrodermale Aktivitat Grundlagen Methodenund Anwendungen Springer Berlin Germany 1988
[49] R Steyer P Schwenkmezger and P Notz Der Mehrdimension-ale Befindlichkeitsfragebogen (MDBF) vol 31 Hogrefe 1997
[50] L Elling H Schupp J Bayer et al ldquoThe impact of acute psycho-social stress on magnetoencephalographic correlates of emo-tional attention and exogenous visual attentionrdquoPLoSONE vol7 no 6 Article ID e35767 2012
[51] C Kirschbaum K-M Pirke and D H Hellhammer ldquoThelsquotrier social stress testrsquomdasha tool for investigating psychobiologicalstress responses in a laboratory settingrdquo Neuropsychobiologyvol 28 no 1-2 pp 76ndash81 1993
[52] O Pollatos W Kirsch and R Schandry ldquoOn the relationshipbetween interoceptive awareness emotional experience andbrain processesrdquo Cognitive Brain Research vol 25 no 3 pp948ndash962 2005
[53] C Ring and J Brener ldquoInfluence of beliefs about heart rate andactual heart rate on heartbeat countingrdquo Psychophysiology vol33 no 5 pp 541ndash546 1996
[54] C Stevens G Walker M Boyer and M Gallagher ldquoSeveretinnitus and its effect on selective and divided attentionrdquo Inter-national Journal of Audiology vol 46 no 5 pp 208ndash216 2007
[55] S Rossiter C Stevens andGWalker ldquoTinnitus and its effect onworking memory and attentionrdquo Journal of Speech Languageand Hearing Research vol 49 no 1 pp 150ndash160 2006
[56] B M Herbert J Blechert M Hautzinger E Matthias and CHerbert ldquoIntuitive eating is associated with interoceptive sensi-tivity Effects on body mass indexrdquo Appetite vol 70 pp 22ndash302013
[57] M Landgrebe U Frick S Hauser G Hajak and B LangguthldquoAssociation of tinnitus and electromagnetic hypersensitivityhints for a shared pathophysiologyrdquo PLoS ONE vol 4 no 3Article ID e5026 2009
[58] A McCombe D Baguley R Coles L McKenna C McKinneyand P Windle-Taylor ldquoGuidelines for the grading of tinnitusseverity the results of a working group commissioned by theBritish Association of Otolaryngologists Head and Neck Sur-geons 1999rdquoClinical Otolaryngology andAllied Sciences vol 26no 5 pp 388ndash393 2001
[59] N Zirke G Goebel and B Mazurek ldquoTinnitus and psycholog-ical comorbiditiesrdquo HNO vol 58 no 7 pp 726ndash732 2010
![Tumorigenic Factor CRIPTO-1 Is Immunolocalized in ......2 BioMedResearchInternational serouslayertoreachadjacentstructuressuchasthebladder andureters[6,13,14,19].Thesedescriptionscharacterizethe](https://static.documents.pub/doc/80x56/611f6e1ec798c173264571a4/tumorigenic-factor-cripto-1-is-immunolocalized-in-2-biomedresearchinternational.jpg)
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