Post on 15-Dec-2015
transcript
THE ROLE OF THE VAGAL SYSTEM IN THE SENSORY PROCESSING PATTERNS OF CHILDREN WITH
AUTISTIC SPECTRUM DISORDERS
Catherine Cavaliere, PhD, OTR/LNew Jersey Occupational Therapy
Association Annual ConferenceOctober 1, 2011
The Beginning…
Clinical Hypothesis: “ Sensory integration intervention fosters
neural adaptations that thereby support behavioral adaptations within the environment in children with autistic spectrum disorders(ASD).”
Core assumption of SI theory: “The goal of sensory integration intervention
is to improve the efficiency of the nervous system in interpreting sensory information for functional use.” (Parham & Malliouz, 2000)
Treatment efficacy study – pre/post test - measure of neurophysiologic change
The Middle
Lack of research to support the theoretical assumption that SI intervention fosters neural change
Lack of information in literature as to how children, with and without autism, respond to sensation, neurophysiologically, PERIOD!
The End…The Beginning! “How do children with
ASD respond to sensation neurophysiologically? Is there a relationship between this and their behavioral responsivity to sensation?”
Measure and methods
Dr. Lucy Jane Miller and colleagues – Sensory Challenge Protocol (SCP)
Autistic Spectrum Disorder (ASD)
DSM IV Social Interaction
Marked impairment in nonverbal behavior Failure to develop age appropriate peer relationships Lack of spontaneous seeking to share interests with others Lack of social or emotional reciprocity
Communication Delay in or lack of spoken language Marked impairment in conversational skills Stereotyped use of language Lack of age appropriate pretend or social play
Stereotyped Patterns of Behavior At least one restricted pattern of interest Inflexible adherence to routines Stereotyped or repetitive motor mannerisms Preoccupation with parts of objects
(American Psychiatric Association, 1994)
Behavioral responses to sensation in children with ASD
70-97% of children with ASD – atypical patterns of sensory processing (Ornitz, 1989; Adrien et al., 1992, Eaves et al., 1994; Kientz and Dunn, 1996; Greenspan and Wieder, 1997; Tomcheck and Dunn, 2007)
Children with ASD – early signs of deficits in sensory processing – central to ASD diagnosis (Baraneck, 1999)
Children with ASD respond differently to sensation, behaviorally, than do children without ASD (Dunn and Kientz, 1996; Dietz and White, 2000)
ASD – most severe sensory processing disorders (Bagnato and Neilsworth, 1999)
Physiologic responses to sensation in children with ASD
Patterns of physiological responsivity (EDA) that are different than typically developing children and other groups of children with behavioral difficulties with sensation
Decreased magnitude of EDR – hypo-responsivity (Miller et. al., 2000)
2 groups – High arousal – higher magnitude EDR; Low arousal – lower magnitude EDR – heterogeneous group ( Schoen,S.A, Miller, L.J., Brett-Green, B., &Hepburn, S.L., 2008)
Lower vagal responses to auditory and tactile information (Schaaf and Benevides, 2006)
(McIntosh, D., Miller, L. J., Shyu, V., & Hagerman, R., 1999; Miller et al., 1999; Donelon,- Mangeot et al., 2001; Miller, L.J., McIntosh, D.N., Reisman, J.E., Simon, J., 2001; Schaaf , R.C.,& Benevides, T., 2006; Schoen, S.A, Miller, L.J., Brett-Green, B., &Hepburn, S.L., 2008)
“The objective of therapy for the autistic child is to improve sensory processing so that more sensations will be effectively “registered” and modulated, and to encourage the child to form simple adaptive responses as a means of helping him to learn and to organize his behavior… As we continue to treat autistic children, we shall find out more about their neurologic problems and develop ways of “reaching” their brains with sensory experience.”
(Ayres, 1979)
Neuro-physiologic state
Behavioral state– attention, arousal
Adaptive Interactions
Occupational Performance
Theoretical PerspectiveNeuro-occupation (Padilla & Peyton, 1997)
Physiologic Measures
Autonomic Nervous System
Parasympathetic Nervous System
Restorative
functions
Cardiac Vagal
Tone
Respond to all environmental situatio
ns
Sympathetic Nervous System
Highly active stressful
situations
Electrodermal
Activity
Cardiac Vagal Tone (CVT)
Parasympathetic nervous system’s (PsNS) modulation of heart rate via the vagus nerve
Respiratory Sinus Arrhythmia(RSA) - rhythmic heart rate variability within spontaneous breathing
2 functional aspects of CVT: Baseline – rest – high CVT Vagal regulation – change from baseline to respond to
environment – drop in CVT
More variability indicating more efficient neural control physiologically able to meet the demands of
any situation – adaptive interactions
(Porges, 1992; 1995)
Physiologic Variability and Adaptive Interactions
Physiologic
Variability
Physiologic
Flexibility
Behavioral
Flexibility
Adaptive Interactio
ns
(Porges, 1992;1995)
Porges (1995)
Healthy Neonates High Risk - NICU
Baseline Vagal Tone
Higher baseline VT correlated with greater self-regulation and more positive developmental outcomes
( Porges et al, 1996; Fox, 1989; DeGangi et al, 1991; Fox and Porges, 1985; Huffman, L.C., Bryan, Y.E., delCarmen, R., Pedersen, F.A., Doussard-Roosevelt, J.A. & Porges, S.W., 1998; Gunnar, M.R., Porter, F.L., Wolf, C.M., Rigatuso, J. & Larson, M.C., 1995; Stifer and Fox, 1990; Richards, 1985)
Fragile x– lower baseline (less heart rate variability) VT than boys without (Boccia &Roberts ,2000)
SMD – lower baseline vagal tone than children without (Schaaf et al., 2003;
2010)
ASD – lower baseline vagal tone than typically developing children (Schaaf and Benevides, 2006)
Significant relationship between vagal tone and adaptive behaviors - ASD - lower vagal tone had less adaptive behaviors (vineland adaptive behavior scales) (Schaaf and Benevides, 2006)
Vagal Regulation
More consistency in suppressing vagal tone in response to environmental stimuli/task, the greater the social and attentional capacities and more even temperament
(Porges et al, 1996; Huffman et al, 1998; Fox, 1989; Calkins, 1997; Suess, P.E., Porges, S.W. & Plude, D.J, 1994; DeGangi et al., 1991;Gunnar et al., 1995; Stifter and Fox.,1990; Richards, 1987 )
Reliability of Baseline Vagal Tone
Author Subjects - age Testing period Results - VT
Fracasso et al., 1994
5,7,10,13 months
Every 3 months – 4 testing sessions
Moderate stability (r=.50-.55)
Stifter & Fox, 1990
Neonates, 5 months
5 months apart – 2 testing sessions
Not Stable (r=.07)
Fox & Field, 1989
3yrs 6 months apart - 2 testing sessions
Stable (r=.89)
Calkins & Keane, 1994
2 yrs, 4.5 yrs 2.5 years apart – 2 testing sessions
Moderate stability (r=.57)
Doussard-Roosevelt et al., 2003
5-6yrs 2 wks apart – 3 testing sessions
Moderate stability (r=.58)
Porges, 1992 NICU Neonates
first day off ventilator, every day for 5 days – 6 testing sessions
Stable (r=.90)
Reliability of Vagal Regulation
Author Subjects Task Results - VT
Calkins & Keane, 2004
2yrs, 4.5yrs Attention, empathy, frustration, problem solving
No stability (r=.05-.29)
Doussard-Roosevelt et al., 2003
5 yrs – once a wk – 4 wks
Negative affect elicitor task
Modest stability wks 1-2 (r=.40)No stability second 2 wks (r=.08-.25)
El-Sheik, 2005 9,11 yrs Cognitive taskEmotional task
Stability – cognitive task – (r=.60)No stability – emotional task – (r=.06)
Synthesis of Research on Vagal Tone
Infants/ young children with high baseline vagal tone demonstrate greater self-regulation
Children with ASD and SMD have lower baseline vagal tone than children without
Infants/ young children who consistently suppress vagal tone in response to a challenge demonstrate greater attentional and social interaction skills and more even temperament
Reliability– mixed results
Gaps in the Literature
Reliability of vagal tone has not been established
Limited information on vagal tone in older children (4+)
Limited information on vagal tone in various diagnostic groups including autism
Inconclusive information on the relationship between physiologic responsivity(CVT) and behavioral responses to sensation
Research Questions
Is cardiac vagal tone a reliable measure of physiologic responsivity to sensation in both typically developing children and children with ASD?
Do children with ASD respond differently (behaviorally and physiologically) to sensation than typically developing children?
Is there a relationship between the behavioral and physiologic responses to sensation in children with and without ASD?
Short Sensory Profile (SSP)(Dunn, 1997)
Sensory Profile (Dunn, 1999)
Caregiver questionnaire Profiles a child’s behavioral responses to
sensation Construct validity – sensory processing (Dunn, 1997)
Discriminant validity - differentiate children with ASD from children without autism, ADHD, SMD (Kientz &Dunn, 1997; Ermer & Dunn, 1998)
Positively correlate with physiologic measures of sensory responsivity (EDR) using the SCP (Miller et al.,1999;2000)
Design
Test re-test/ Multifactorial repeated measures design
Independent variables Group Sensation (SCP) Testing session
Dependent variables Physiologic responsivity to sensation (CVT) Behavioral responsivity to sensation (SSP)
Inclusion Criteria
Experimental group Males with ASD - 4-11 yrs. No other developmental/neurological conditions No medications
Control group Typically developing males – 4-11 yrs. No developmental/neurological conditions No medications
Subjects
39 boys (16 typically developing; 23 with ASD) Excessive artifact (n=5) Technical Difficulties (n=3) Inability to tolerate testing (n=4)
15 typically developing boys; 11 boys with ASD Typically developing (TD)– 8.7 years ASD – 7.3 years
Instrumentation
Psylab stand alone monitor (SAM) acquisition and analysis system (Contact Precision Instruments) Heart rate and electrodermal responsivity Synced with the Sensory Challenge Protocol
MxEdit analysis program (S.Porges,1985)
heart rate converted to vagal tone index artifact identification and editing
Sensory Challenge Protocol (SCP) (Miller,
1999)
Five domains of sensation (vestibular, auditory, visual, olfactory, tactile)
10 trials of each sensation – 3 secs per trial 15-19 sec. between each trial – random intervals 20 secs between domains Baseline and Recovery 15 mins without stopping Testing can be paused Domains can be skipped
Procedures
Meet/greet parents; complete forms Acquaint child with testing environment Explain testing procedures in age appropriate
language Child signs assent Child seated - electrodes placed on child SCP started End of SCP child picks a small gift
Data Analysis
Question 1: Is cardiac vagal tone a reliable measure of responsivity to sensation in typically developing children and children with ASD?
Intraclass correlation Coefficient (ICC) Baseline measures of cardiac vagal tone Vagal changes in response to sensations
Data Analysis
Question 2: Do children with ASD respond to sensation (behaviorally and physiologically) differently than typically developing children?
Repeated Measures ANOVA – within group patterns of responsivity
Multivariate ANOVA – between group differences – SCP and SSP
Data Analysis
Question 3: Is there a relationship between physiologic and behavioral responses to sensation in children with ASD and typically developing children?
Pearson Correlation Coefficient –vagal scores SCP and SSP scores
Results
Question 1: Is cardiac vagal tone a reliable measure of responsivity to sensation in typically developing children and children with ASD?
Table 1. Test Re-test Reliability Measures.
SCP Domain _________________________________________________________
Total Typical ASD
M SD ICC M SD ICC M SD ICC
Baseline 6.36 1.20 .830 6.80 .981 .702 5.77 1.27 .889
Tones 6.57 1.16 .782 7.0 .933 .525 6.01 1.25 .905
Visual 6.59 1.05 .830 6.91 .847 .650 6.11 1.71 .911
Sirens 6.59 1.01 .828 7.01 .775 .724 6.03 1.07 .819
Olfactory 6.42 1.24 .920 6.91 .929 .923 5.74 1.33 .881
Tactile 6.55 1.17 .912 7.0 .779 .810 5.85 1.27 .916
Vestibular 6.76 1.11 .916 7.31 .711 .837 6.01 1.13 .896
Recovery 6.42 1.17 .851 6.90 .899 .710 5.77 1.21 .899
Av. Response 6.57 1.11 .894 7.04 .865 .801 5.94 1.18 .901
______________________________________________________________________________
Results
Question 2: Do children with ASD respond to sensation (behaviorally and physiologically) differently than typically developing children?
Baseline Vagal Tone
Baseline - t(20)=2.58, p=.018 ASD – lower baseline vagal tone – less
heart rate variability at rest Covariate
TYP (M=6.80, SD=.981) ASD group (M= 5.77, SD=1.27)
Figure 1. Within group vagal response patterns.
F=3.04, p=0.13
Figure 2. Between group differences in vagal responses.
P=.008
Table 2. Between group differences on SSP.
SSP Sig._(a)__TYP ASD M SD M SD
SSP total 175.0 15.4 128.0 16.4 .000Tactile 32.3 2.5 28.4 5.1 .013Taste/Smell 18.5 5.5 11.6 6.2 .011Movementsensitivity 13.8 2.4 14.6 .81 .298Under resp./ 32.3 3.0 18.3 4.2 .000seeks sensationAuditory Filter 26.9 2.9 17.0 5.7 .000Low energy 28.6 4.1 21.6 7.7 .012Visual Auditory 24.2 1.7 16.4 4.5 .000
___________________________________________________________________a Adjustment for multiple comparisons: Bonferroni
Results
Question 3: Is there a relationship between physiologic and behavioral responses to sensation in children with ASD and typically developing children?
Table 3. Correlations between SSP sections and vagal responses on SCP domains.
SSP SCP domain r_______________TYP/ASD sessions combinedSSP total vestibular .510Auditory vestibular .526Visual/auditory vestibular .668Visual/auditory olfaction .509Visual/auditory tactile .558Visual/auditory av. response .542 Visual/auditory vestibular .569
ASD sessions combinedVisual/auditory tones .627
ASD session 2Visual/auditory sirens .555Visual/auditory olfaction .606Visual/auditory tactile .551Visual/auditory vestibular .708 Visual/auditory av. response .613________________________________________________________________________
Correlations
ASD - 99.9% of the vagal responses to sensations across sessions were correlated (<.75) – Ex: visual 1 to olfaction 2
Little physiologic variability across time and across sensations
TYP- 77.5% - more variability across time and across sensation
Discussion: Reliability of CVT
Overall high stability
ASD - high stability – little variability across time (.819-.916)
TYP- mixed stability – more variability across time (.525-.923)
Discussion: Group differences in baseline vagal tone
ASD – sig. lower baseline vagal tone than TYP – less heart rate variability at rest
Supports previous findings (Schaaf et al., 2003; 2010)
Supports reliability findings- pattern of less physiologic variability - ASD
Physiologic Variability and Adaptive Interactions in ASD
Less Physiolo
gic Variabilit
y
Less Physiolo
gic Flexibilit
y
Less Behavior
al Flexibilit
y
Rigid/ inflexibl
e behavio
rs
Decreased
Adaptive
Interactions
(Porges, 1992;1995)
Discussion: Group differences in vagal responsivity.
F=3.04, p=0.13
Why Vestibular???
Vestibular system – central integrator (Cool, 1987) -
Spatial map – body, head, position and orientation - understand our environment in relation to self
“reference base “against which all sensory input and motor output must be evaluated ( Cool, 1987)
CN VIII - posterior parietal lobe (cerebellum and brainstem)
“bridge” between sensory inputs and motor outputs (Ayres, 1979)
Only sensory system that also has direct motor innervations (CN VIII) at spinal level – muscle tone and arousal – low in ASD (Miller et. al, 2001)
Why Vestibular???
Stereotyped behaviors – body sense driven (vestibular, proprioceptive and tactile)
Vestibular - critical role as central integrator
Examples: body rocking, head banging, darting, rigid inflexible
Stereotyped behaviors - seeking out vestibular stimulation (Bender, 1947, 1956).
Clinically – stereotyped behaviors - child’s attempt to seek out vestibular input
Treatment – large vestibular component
Goals of treatment - modulate arousal; increase body awareness; improve sensory modulation; attention and interaction
Why Vestibular???
ASD - demonstrated hypo-responsivity to sensation (Miller et. al., 2000)
Our findings support this – physiologic hypo- reactivity to vestibular information as compared to TYP
Results - provide preliminary evidence to support this clinical assumption : Stereotyped behaviors - fulfill a need for additional vestibular input in order to make sense of their environment
Discussion: Group differences in behavioral responses to sensation
ASD – sig. lower scores on all sections of SSP except movement sensitivity - TYP scoring lower
Vestibular Based – body position, orientation Questions related to safety awareness:
“ Becomes anxious/distressed when feet leave ground”“Fears falling or heights”“Dislikes activities where head is upside down”
TYP –more behaviorally sensitive to movement because they more efficiently react to vestibular information thereby providing them with a greater safety awareness and better body awareness
ASD patterns of response to vestibular information
Stereotyped
Behaviors
Less physiolog
ic reactivity
to vestibula
r
Less behavior
al reactivity
to vestibula
r
Seek out vestibular input
Discussion: Relationship between physiologic and behavioral responses to sensation
SSP SCP domain r_______________TYP/ASD sessions combinedSSP total vestibular .510Auditory vestibular .526Visual/auditory vestibular .668Visual/auditory olfaction .509Visual/auditory tactile .558Visual/auditory av. response .542 Visual/auditory vestibular .569
ASD sessions combinedVisual/auditory tones .627
ASD session 2Visual/auditory sirens .555Visual/auditory olfaction .606Visual/auditory tactile .551Visual/auditory vestibular .708 Visual/auditory av. response .613________________________________________________________________________
Why Visual/Auditory???
Visual/auditory section- single sensory system “holds hands over ears to protect from loud sounds” “is bothered by bright lights” “covers or squints eyes to protect from light”.
Other sections – multimodal “has a weak grasp” “has difficulty paying attention” “has difficulty standing in line close to other people”
SCP domains – single system based
Multimodal sensory experiences to SCP
Discussion: Relationship between physiologic and behavioral responses to sensation
Children with autism demonstrated less reactivity to vestibular information both physiologically (vagal responses )and behaviorally (score on movement sensitivity section)
Support this clinical assumption that the stereotyped behaviors - fulfill a need for additional vestibular input in order to make sense of their environment
relationship between physiology and behavior
Limitations
Small sample size Not age matched Initial testing anxiety
Conclusions
Preliminary info on reliability of vagal tone
Differences in physiologic responsivity between groups – ASD less physiologic variability
Relationship between physiology and behavior
Conclusion
Combined these findings provides preliminary evidence to support the theoretical and clinical assumptions that neurophysiologic state affects behavior
Directions for Future Research
Replicated - larger sample size Compare these results to SNS measures Modify the SCP to include some
multimodal sensory experiences *Intervention studies
“The objective of therapy for the autistic child is to improve sensory processing so that more sensations will be effectively “registered” and modulated, and to encourage the child to form simple adaptive responses as a means of helping him to learn and to organize his behavior… As we continue to treat autistic children, we shall find out more about their neurologic problems and develop ways of “reaching” their brains with sensory experience.”
(Ayres, 1979)
Acknowledgements
Dr. Genevieve Pinto-Zipp, EdD, PT Dr. Susan Simpkins, EdD, PT Dr. Valerie Olsen, EdD, PT Dr. Raju Parasher, EdD, PT Barbara Schupak, OTR/L, MPH Michele Parkins, MS/OTR/L
Acknowledgements
Dr. Lucy Miller, PhD, OTR/L Dr. Roseann Schaaf, PhD, OTR/L Teal Benevides, MS/ OTR/L
Celebrate the Children School - Michele Parkins, MS/OTR/L
Pediatric Therapeutics – Missy Briody, MS/OTR/L
Bergen Pediatric Therapy – Lisa Koo, MS/OTR/L
References Adrien, L.J., Ornitz, E., Barthelemy, C., Sauvage, D. & Lelord, G. (1987). The presence
or absensce of certain behaviors associated with infantile autism in severely retarded autistic and non-autistic children and very young normal children. Journal of Autism and Developmental Disorders, 17(3), 407-416. 27
American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author. 6
Bagnato, S.J., & Neilsworth, J.T. (1999). Normative detection of early regulatory disorders and autism: Empiracle confirmation of DC:0-3. Infants and Young Children, 12, 98-106. 27
Baraneck, G.T. (1999). Autism during infancy: A retrospective video analysis of sensory motor and social behaviors at 9-12 months of age. Journal of Autism and Developmental Disorders, 29(3), 213-224. 27
Calkins, S. (1997). Cardiac vagal tone indices of tempermental reactivity and behavioral regulation in young children. Developmental Psychobiology, 31(2), 125-135. 27
DiGangi, G.A., Greenspan, S.I., & Porges, S.W. (1991). Psychophysiologic characteristics of the regulatory disordered infant. Behavior and Development, 14, 37-50. 27
Donelan-Mangeot, S., Miller, L.J., McIntosh, D., McGrath-Clarke. J., Simon, J., Hagerman, R., & Goldson, E. (2001). Sensory modulation dysfunction in children with attention deficit hyperactivity disorder. Developmental Medicine and Child Neurology, 43, 399-406. 27
References Doussard-Roosevelt, J.A., Montgomery, L.A., & Porges, S. (2003). Short term stability of
physiologic measures in kindergarten children: Respiratoty sinus arrythmia,heart period and cortisol. Wiley Interscience, . 27
Doussard-Roosevelt, J.A., Porges, S.W., Scanlon, J.W., Alemi, B., & Scanlon, K.B. (1997). Vagal regulation of heart rate in the prediction of developmental outcome for very low birth weight pre-term infants. Child Development, 68(2). 27
Dunn, W. (1999). Sensory Profile User's Manual. The Psychological Corporation. 6 Dunn, W., & Brown, C. (1997). Factor analysis on the sensory profile from a national
sample of children without disabilities. American Journal of Occupational Therapy, 51(7), 490-495. 27
Dunn, W., & Westman, K. (1997). The Sensory Profile: The performance of a national sample of children without disabilities. American Journal of Occupational Therapy, 51(1), 25-34. 27
Eaves, L.C., Ho, H. H. & Eaves, D.M. (1994). Sub-types of autism by cluster analysis. Journal of Autism and Developmental Disorders, 24, 3-22. 27
El-Sheikh, M. (2005). Stability of respiratory sinus arrythmia in children and young adolescents: A longitudinal examination. Developmental Psychobiology, 46, 66-74. 27
Fox, N., & Porges, S.W. (1985). The relation beteween neonate heart period patterns and developmental outcomes. Child Development, 56, 28-37. 27
Gunnar, M.R., Porter, F.L., Wolf, C.M., Rigatuso, J., & Larson, M.C. (1995). Neonatal stress reactivity: Predictions to later temperment. Child Development, 66, 1-13
References Heubner, R.A. (2001). Autism: A sensorimotor approach to management.
Austin, TX: Pro-ed. 6 Huffman, L.C., Bryan, Y.E., delCarmen, R., Pederson, F.A, Doussard-Roosevelt,
J.A., & Porges, S.W. (1998). Infant temperment and cardiac vagal tone: Assesment at twelve weeks of age. Child Development, 69, 624-635. 27
Interdiscplinary council on developmental and learning disorders. (2005). Diagnostic manual for infancy and early childhood. Bethesda, MD: Author. 12
Kientz, M.A., & Dunn, W. (1996). A comparison of the performance of children with and without autism on the Sensory Profile. American Journal of Occupational Therapy, 51(7), 530-537. 27
McIntosh, D., Miller, L.J., Shyu, V., & Hagerman, R. (1999). Sensory modulation disruption, electrodermal responses and functional behaviors. Developmental Medicine and Child Neurology, 41, 608-615. 27
Miller, L.J., Lane, S. (2000). Toward a consensus in terminology in sensory integration theory and practice: Part 1: Taxonomy of neurophysiologic processes. Senaory Integration Special Interest Section Quarterly, 23(1), 1-4. 43
Miller, L.J., McIntosh, D., McGrath, J., Shyu, V., Lampe, M.,& Taylor, A.K. (1999). Electrodermal responses to sensory stimuli in individuals with fragile x syndrome. American Jouranl of Medical Genetics, 83, 268-279. 27
References Miller, L.J., McIntosh, D.N., Reisman, J.E., & Simon, J. (2001). An ecological model of
sensory modulation: Performance of children with fragile x syndrome, autistic disorder, attention deficit hyperactivity disorder, and sensory modulation dysfunction. In Smith Roley, S., Imperatore Blanch, E., Schaaf, R.C. (Ed.), Understanding the nature of sensory integration with diverse populations (pp. 57-88). Bethesda, MD: Therapy Skill Builders. 15
Padilla, R.P, Peyton, C.G. (1997). Neuro-occupation: Historical review and examples. In C. Royeen (Ed.), Neuroscience and occupation: Links to practice. (pp. 1-31). Bethesda, MD: The Occupational Therapy Association. 15
Porges, S. (1992). Vagal tone: A physiologic marker of stress vulnerability. Pediatrics, 90(3), 498-504. 27
Porges, S. (1995). Cardiac vagal tone: A physiogic index of stress. Neuroscience and Behavioral Reviews, 19(2), 225-233. 27
Porges, S.W. (2007). The polyvagal perspective. Biological Psychology, 74, 116-143. 27
Porges, S.W., Doussard-Roosevelt, J.A., Portales, A.L., & Greenspan, S.I. (1996). Infant regulation of the vagal brake predicts child behavior problems: A psychobiological model of social behavior. Developmental Psychobiology, 29(8), 697-712. 27
Reeves, G.D. (2001). From neuron to behavior: Regulation, arousal and attention as important substrates for the process of sensory integration. In S. Smith Roley, E., Imperatore Blanche, R.C. Schaaf (Ed.), Understanding the nature of sensory integration with diverse populations (pp. 89-108). Therapy Skill Builders. 15
References Richards, J.E. (1987). Infant visual sustained attention and respiratory sinus arrythmia.
Child Development, 58, 488-496. 27 Schaaf, R.C., Benevides, T., Imperatore Blanch, E., Brett-Greem, B., Burke, J.P., Cohn,
E.S., Koomar, J., Miller, L.J., May-Benson, T.A., Parham, D., Reynolds, S., & Schoen, S. (2010). Parasympathetic functions in children with sensory processing disorder. Fronteirs in Integrative Neuroscience, 4(4), 1-11. 27
Schaaf, R.C., Miller, L.J., Seawell, D., & O'Keefe, S. (2003). Children with disturbances in sensory processing: A pilot study examining the role of the parasympathetic nervous system. American Journal of Occupational Therapy, 57(4), 442-449. 27
Stifter, C.A., & Fox, N.A. (1990). Infant reactivity: Physiological correlates of newborn and five month temperment. Developmental Psychology, 26(4), 582-588. 27
Suess, P.E., & Bornstein, M.H. (2001). Task to task vagal regulation: Relations with language and playing 20 month old children. Infancy, 1(3), 303-322. 27
Suess, P.E., Porges, S.W., & Plude, D.J. (1994). Cardiac vagal tone and sustained attention in school aged children. Psychophysiology, 31, 17-22. 27
Watling, R., Dietz, J., & White, O. (2000). Sensory profile scores of young children with and without autism spectrum disorders. American Journal of Occupational Therapy, 55(4), 416-423. 27
Willemsen-Swinkles, S.H., Buitelaar, J.K., Dekker, M., & vanEngland, H. (1998). Sub-typing stereotypic behavior in children: The association between stereotypic behavior, mood and heart rate. Journal of Autism and Developmental Disorders, 28, 547-557. 27