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What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition Part 2 (Aberrant salience) B. Nelson , T.J. Whitford, S. Lavoie, L.A. Sass Orygen Youth Health Research Centre, 35 Poplar Rd (Locked Bag 10), Parkville, Victoria 3052, Australia abstract article info Article history: Received 8 April 2013 Received in revised form 17 June 2013 Accepted 18 June 2013 Available online xxxx Keywords: Schizophrenia Psychosis Phenomenology Self Neurocognition Phenomenological research indicates that disturbance of the basic sense of self may be a core phenotypic mark- er of schizophrenia spectrum disorders. Basic self-disturbance refers to disruption of the sense of ownership of experience and agency of action and is associated with a variety of anomalous subjective experiences. Little is known about the neurocognitive underpinnings of basic self-disturbance. In these two theoretical papers (of which this is Part 2), we review some recent phenomenological and neurocognitive research and point to a con- vergence of these approaches around the concept of self-disturbance. Specically, we propose that subjective anomalies associated with basic self-disturbance may be associated with: 1. source monitoring decits, which may contribute particularly to disturbances of ownershipand mineness(the phenomenological notion of presence or self-affection) and 2. aberrant salience, and associated disturbances of memory, prediction and atten- tion processes, which may contribute to hyper-reexivity, disturbed gripor holdon perceptual and concep- tual elds, and disturbances of intuitive social understanding (common sense). In this paper (Part 2) we focus on aberrant salience. Part 1 (this issue) addressed source monitoring decits. Empirical studies are required in a variety of populations in order to test these proposed associations between phenomenological and neurocognitive aspects of self-disturbance in schizophrenia. An integration of ndings across the phenomeno- logical and neurocognitive levelswould represent a signicant advance in the understanding of schizophrenia and possibly enhance early identication and intervention strategies. © 2013 Elsevier B.V. All rights reserved. 1. Introduction In Part 1 (Nelson et al., in press-b) we argued for the importance of integration across levelsof enquiry in schizophrenia research and proposed that there is a convergence in recent phenomenological and neurocognitive research around the concept of disturbance of the basic sense of self as a central feature of schizophrenia. We outlined the phenomenological basic self-disturbance model of schizophrenia and outlined how various aspects of this model, particularly dimin- ished ownership of experience, self-other boundary confusion, and hyper-reexivity, might correlate with neurocognitive disturbances of source monitoring. In this paper (Part 2) we focus on neurocognitive disturbances of aberrant salience and their possible phenomenological correlates and suggest avenues for empirical enquiry into these proposed associations. Our aim is not to introduce new elements to the existing phenomenological and neurocognitive models but rather to speculate about the possible connections between the two levelsof enquiry. 2. Aberrant salience: memoryattention disturbances A considerable amount of research indicates the presence of atten- tion and memory disturbances in schizophrenia. A major theme in this work is the failed suppression of attention to irrelevant or familiar information or stimuli in the environment, leading to aberrant salience of objects and associations (Kapur, 2003; Kapur et al., 2005) or, to reverse the terminology, excessive attention to information that is irrelevant or highly familiar. The term salienceis being used broadly in this context to describe the relative attention directed towards a stimulus compared to other stimuli (i.e., how prominent, noticeable, or important a stimulus appears to be) and the resultant affect on goal-directed behaviour (Gray et al., 1991; Hemsley, 1992; Berridge and Robinson, 1998; Kapur, 2003; Kapur et al., 2005). A number of neurocognitive models and experimental paradigms have yielded ndings consistent with this view. These include: Keefe and colleagues' memoryprediction model of cortical function (Keefe and Kraus, 2009; Kraus et al., 2009; Keefe et al., 2011); the salience dysregulation model based on dopamine system abnormalities (Gray et al., 1991; Hemsley, 1992; Kapur, 2003); mismatch negativity reduction (Todd et al., 2012); latent inhibition (Gray et al., 1992; Lubow and Gewirtz, 1995; Schizophrenia Research xxx (2013) xxxxxx Corresponding author. Tel.: +61 3 9342 2800; fax: +61 3 9387 3003. E-mail address: [email protected] (B. Nelson). SCHRES-05477; No of Pages 8 0920-9964/$ see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.schres.2013.06.033 Contents lists available at SciVerse ScienceDirect Schizophrenia Research journal homepage: www.elsevier.com/locate/schres Please cite this article as: Nelson, B., et al., What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition, Schizophr. Res. (2013), http://dx.doi.org/10.1016/j.schres.2013.06.033
Transcript

Schizophrenia Research xxx (2013) xxx–xxx

SCHRES-05477; No of Pages 8

Contents lists available at SciVerse ScienceDirect

Schizophrenia Research

j ourna l homepage: www.e lsev ie r .com/ locate /schres

What are the neurocognitive correlates of basic self-disturbance inschizophrenia?: Integrating phenomenology and neurocognitionPart 2 (Aberrant salience)

B. Nelson ⁎, T.J. Whitford, S. Lavoie, L.A. SassOrygen Youth Health Research Centre, 35 Poplar Rd (Locked Bag 10), Parkville, Victoria 3052, Australia

⁎ Corresponding author. Tel.: +61 3 9342 2800; fax:E-mail address: [email protected] (B. Nelson

0920-9964/$ – see front matter © 2013 Elsevier B.V. Allhttp://dx.doi.org/10.1016/j.schres.2013.06.033

Please cite this article as: Nelson, B., et al.,phenomenology and neurocognition, Schizo

a b s t r a c t

a r t i c l e i n f o

Article history:Received 8 April 2013Received in revised form 17 June 2013Accepted 18 June 2013Available online xxxx

Keywords:SchizophreniaPsychosisPhenomenologySelfNeurocognition

Phenomenological research indicates that disturbance of the basic sense of self may be a core phenotypic mark-er of schizophrenia spectrum disorders. Basic self-disturbance refers to disruption of the sense of ownership ofexperience and agency of action and is associated with a variety of anomalous subjective experiences. Little isknown about the neurocognitive underpinnings of basic self-disturbance. In these two theoretical papers (ofwhich this is Part 2), we review some recent phenomenological and neurocognitive research and point to a con-vergence of these approaches around the concept of self-disturbance. Specifically, we propose that subjectiveanomalies associated with basic self-disturbance may be associated with: 1. source monitoring deficits, whichmay contribute particularly to disturbances of “ownership” and “mineness” (the phenomenological notion ofpresence or self-affection) and 2. aberrant salience, and associated disturbances of memory, prediction and atten-tion processes, which may contribute to hyper-reflexivity, disturbed “grip” or “hold” on perceptual and concep-tual fields, and disturbances of intuitive social understanding (“common sense”). In this paper (Part 2) we focuson aberrant salience. Part 1 (this issue) addressed source monitoring deficits. Empirical studies are required in avariety of populations in order to test these proposed associations between phenomenological andneurocognitive aspects of self-disturbance in schizophrenia. An integration of findings across the phenomeno-logical and neurocognitive “levels”would represent a significant advance in the understanding of schizophreniaand possibly enhance early identification and intervention strategies.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

In Part 1 (Nelson et al., in press-b) we argued for the importance ofintegration across “levels” of enquiry in schizophrenia research andproposed that there is a convergence in recent phenomenological andneurocognitive research around the concept of disturbance of thebasic sense of self as a central feature of schizophrenia. We outlinedthe phenomenological basic self-disturbance model of schizophreniaand outlined how various aspects of this model, particularly dimin-ished ownership of experience, self-other boundary confusion, andhyper-reflexivity, might correlate with neurocognitive disturbances ofsource monitoring. In this paper (Part 2) we focus on neurocognitivedisturbances of aberrant salience and their possible phenomenologicalcorrelates and suggest avenues for empirical enquiry into theseproposed associations. Our aim is not to introduce new elements tothe existing phenomenological and neurocognitive models but ratherto speculate about the possible connections between the two “levels”of enquiry.

+61 3 9387 3003.).

rights reserved.

What are the neurocognitivphr. Res. (2013), http://dx.do

2. Aberrant salience: memory–attention disturbances

A considerable amount of research indicates the presence of atten-tion and memory disturbances in schizophrenia. A major theme in thiswork is the failed suppression of attention to irrelevant or familiarinformation or stimuli in the environment, leading to aberrant salienceof objects and associations (Kapur, 2003; Kapur et al., 2005) — or, toreverse the terminology, excessive attention to information that isirrelevant or highly familiar. The term “salience” is being used broadlyin this context to describe the relative attention directed towards astimulus compared to other stimuli (i.e., how prominent, noticeable,or important a stimulus appears to be) and the resultant affect ongoal-directed behaviour (Gray et al., 1991; Hemsley, 1992; Berridgeand Robinson, 1998; Kapur, 2003; Kapur et al., 2005). A number ofneurocognitive models and experimental paradigms have yieldedfindings consistent with this view. These include: Keefe and colleagues'memory–prediction model of cortical function (Keefe and Kraus, 2009;Kraus et al., 2009; Keefe et al., 2011); the salience dysregulation modelbased on dopamine system abnormalities (Gray et al., 1991; Hemsley,1992; Kapur, 2003); mismatch negativity reduction (Todd et al.,2012); latent inhibition (Gray et al., 1992; Lubow and Gewirtz, 1995;

e correlates of basic self-disturbance in schizophrenia?: Integratingi.org/10.1016/j.schres.2013.06.033

2 B. Nelson et al. / Schizophrenia Research xxx (2013) xxx–xxx

Gray, 1998); and Corlett's model of ketamine as a pharmacological modelof psychosis (Corlett et al., 2006; Corlett et al., 2007).1 Both Hemsley(Hemsley, 1987, 1998, 2005a) and Sass (Sass, 1992) have drawn on thenotion of malfunction in the hippocampus-based, “comparator” systemin schizophrenia, proposing that such dysfunction results in an automatic,hyperreflexive awareness that disrupts the tacit/focal structure essen-tial to normal experience and, in particular, to the normal experienceof basic selfhood. In brief, a “comparator” system refers to a compari-son between predicted stimuli (“the next expected state of the percep-tual world” (Hemsley, 2005a, p.980)) and stimuli actually received.Although space limitations prohibit a full review of these models andrelevant findings, below we review what we consider to be themajor common themes of these models and how they accord withthe phenomenological model of basic self-disturbance.

Keefe and colleagues (Keefe and Kraus, 2009; Kraus et al., 2009;Keefe et al., 2011) have recently attempted to introduce an organisingprinciple in studies of cognition in schizophrenia in the form of a“memory–prediction”model of cortical function, which has substantialaffinities with the prediction error models described in Part 1 (thisissue), as well as the earlier models of Hemsley (Hemsley, 1987,1992, 1998) and Gray (Gray et al., 1991). This model will be briefly de-scribed and then we will address how it may contribute to aspects ofbasic self-disturbance. The model is founded on the understandingthat perceptual processes do not simply involve the reproduction ofstimuli, but that they involve matching fragmented sensory inputwith “working models” of the world. The brain encodes memoriesbased on the consistent, repeated aspects of our environment, whichthen constitute a working model of the world. The working model isused to continuously make automatic predictions about what willappear or happen in the flow of experience. This so-called “top-down”process (implying a domination of sensory input by cognitive/sensoryschemas) allows us to “fill the gaps” in sensory input and to facilitateefficient interaction with a complex, constantly shifting externalworld. Keefe and Kraus (2009) provide the example of encounteringa partially obscured “STOP” road sign: “…Because of our past experi-ences with stop signs, we are not confused by deviations from thearchetypal stop sign; even if the lower left corner of the sign is bentand the “OP” is obscured by a tree branch, we immediately recognisethe symbol and step on the brake” (p.415). In this way, memory–prediction processes infuse familiar forms of meaning into the world,endowing perception and interaction with our environment with asignificant amount of ease and automaticity.

It has been argued that the hierarchical structure and column-likearchitecture of the cortex gives rise to these memory or learning-based predictions (Keefe and Kraus, 2009). If we encounter stimulithat do not neatly fit our predictions based on previous experience(the memory component of the model), as in the ‘STOP’ signal exam-ple, an area of cortex will relay details of these stimuli or patterns ofstimuli to higher cortical areas. The signal will keep being passed onto the next higher cortical layer until a match is achieved. If a matchis not achieved, a new mental representation of this stimulus willbe introduced. When stimuli become more familiar through repeti-tion, their mental representations are shifted to lower cortical areas,allowing higher areas to detect high-level or superordinate patterns.According to this model, familiar stimuli (i.e., input that conforms toexpectations/predictions based on previous experience) will beprocessed at lower cortical levels, allowing for efficient use of cortical

1 However, we note that measures of the constructs that we have proposed are con-sistent with the notion of aberrant salience, as defined in the current paper, do not con-sistently display high correlations with each other (e.g., see Gjini et al., 2010; Todd etal., 2012). It could be that measures of these constructs pick up on different processesthat all contribute to aberrant salience as an end result. For instance, some measuresmay pick up on “gating out” processes (habituation to repeated redundant stimuli)and others on “gating in” processes (responding when the incoming stimuli take onnew or added significance) (Gjini et al., 2010), both of which may ultimately contrib-ute to aberrant salience. This issue is need of further investigation.

Please cite this article as: Nelson, B., et al., What are the neurocognitivphenomenology and neurocognition, Schizophr. Res. (2013), http://dx.do

resources. As Keefe and Kraus (2009) write, “Thus these memory–prediction processes constitute an elegant and automatic system bywhich familiar stimuli are efficiently processed by lower level brainregions, unexpected stimuli are flagged for more deliberate analysisby higher cortical areas and the essential elements of experience areencoded into memory” (p. 416).

In schizophrenia, according to this model, the memory–predictionprocess is compromised. There is disturbance of both “bottom-up”and “top-down” cortical processing, probably due to widespreadand early disruption of neuronal circuitry (Keefe and Kraus, 2009).Lower cortical levels do not provide adequate perceptual details forhigher levels to establish invariant representations, and higher levelsdo not provide enough context for lower cortical levels to interpretincoming stimuli. This proposal is consistent with Hemsley's (1998,2005a, 2005b) earlier suggestion that schizophrenia is characterisedby a loosening of expectations based on previous experience, an ideaanticipated by the Russian psychologist Polyakov who spoke ofdisturbances of “probability prognosis” (1969, see Sass, 1992, p.127).The consequences of this are 1) slowed, more effortful processing of in-coming information and 2) increased probability of arbitrary, internallygenerated interpretations of stimuli.

One significant feature of the memory-based “context” provided byhigher cortical levels is that it will often have or take on an inherentlysocial nature. A given event or situation is likely to be interpreted in aparticular way based on its social or public significance (e.g., think ofhow shaking your head from side to side might be interpreted in onecultural context compared to another). In other words, socioculturalgroups “share” representations that are stored in each individualmember's memory. When this “shared” context is weakened or dis-turbed in an individual, as in the case of schizophrenia, then interpre-tation of events and situations is more likely to be unconventional,arbitrary and idiosyncratic. A brain-based disturbance of memory andattention processes (and associated aberrant salience) could obviouslycontribute, then, to forms of idiosyncrasy and social disarticulation. Theaccumulation of inaccurate (but internally meaningful) perceptionsmay build upon one another into idiosyncratic and incorrect beliefs,distancing the person from common sense and consensual reality(Blankenburg, 2001; Sass, 2001), and even leading, in some instances,to a solipsistic orientation (Sass, 1992, chp 9) and development ofdelusions and hallucinations.

There is an accumulating body of evidence consistent with thismodel. Post-mortem studies indicate that brain tissue of peoplewith schizophrenia is characterised by abnormal cerebral cortexarchitecture, marked by decreased neuropil, decreased synapticdensity and disarray of neuronal location, particularly in layers thatsit between bottom-up signalling and top-down contextual predic-tions (layers II and III) (Harrison, 1999). Cortical thinning has alsobeen observed in UHR patients who later develop psychotic disorder(Pantelis et al., 2003). Keefe and Kraus (2009) argue that while suchcortical disruption may have a wide-ranging impact on cognition,memory–prediction processes may be particularly affected due to theparticular cortical layers most disrupted. Behavioural observations areconsistent with this interpretation. Deficits in smooth pursuit eyetracking observed in schizophrenia are largely due to impairments inpredictive mechanisms (Thaker et al., 1998, 1999; Hong et al., 2005,2008). The improved performance of schizophrenia patients comparedto controls when tracking a target that changes direction unpredictablyalso suggests a weakening of prediction processes, i.e. that the person isless constrained or directed by automatic predictions. Similarly,reduced mismatch negativity (MMN, see below) and P300 amplitudeindicate deficits in physiological responses to unexpected stimuli, con-sistent with the notion of impairments in memory-based predictionprocesses. A recent study by Morris et al. (2012) found that attentionto irrelevant (i.e., non-predictive) cues, assessed using a causal learningtest, was characteristic of schizophrenia and that learning about thesecues correlated with intensity of positive symptoms. The authors

e correlates of basic self-disturbance in schizophrenia?: Integratingi.org/10.1016/j.schres.2013.06.033

3B. Nelson et al. / Schizophrenia Research xxx (2013) xxx–xxx

argued that excessive attention to irrelevant cues results in learninginaccurate and irrelevant causal associations and that this may be thebasis of positive symptoms in schizophrenia. Corlett's studies withketamine as a pharmacological model of psychotic symptoms haveyielded similar findings (Corlett et al., 2007). Interestingly, the tenden-cy to ascribe meaning where none is present, assessed using awhite-noise task, has been found to be a strong predictor of onset ofpsychotic disorder in an at-risk population (Hoffman et al., 2007). Inthis experiment, irrelevant, meaningless stimuli were endowed withpotential significance, consistent with the memory–prediction model'snotion of an increase in arbitrary, internally generated interpretationsof stimuli (aberrant salience).

The findings that schizophrenia patients have difficulty identifyingincomplete images of common objects are also consistent with thememory–prediction dysfunction model (Doniger et al., 2001;Cavezian et al., 2007). As Keefe and Kraus (2009) note, these deficitssuggest “a failure of top-down hypotheses to guide perceptual comple-tion” (p. 416). Similarly, schizophrenia patients have been found to beimpaired in their ability to fill in missing gaps in speech (Newby, 1998)and exhibit less of a decrease than healthy controls in electrophysiolog-ical response (N400 peaks) in response to semantically primed com-pared to unprimed words (Kiang et al., 2008). Schizophrenia patientsare more hindered in identifying faces by superficial differences inthe face images (e.g., lighting conditions and visual angle) comparedto controls (Benton and Van Allen, 1972; Whittaker et al., 2001). Inthe same vein, schizophrenia patients are more likely to perceive theimage of a concave face when presented using the Binocular Depth In-version Test (BDIT), rather than automatically invert the image into astandard convex face, as healthy controls typically do (Emrich, 1989).Interestingly, scores on the BDIT correlate with the severity of psychot-ic symptoms (Schneider et al., 2002), which is often not the case withmore standard tests of cognition. These findings are consistent withthe notion of a failure to make accurate “top-down” predictionsbased on contextual information (drawing on memory-based process-es) and an over-reliance on lower level perceptual processing. It isinteresting, then, that schizophrenia patients show a pattern of superiorperformance on several kinds of tasks in which standard expectanciesnormally cause a decline in performance: 1, recognition of unlikelyscenes shown tachistoscopically (Polyakov, 1969); 2, a tendency to bemore “logical” when logic requires the ignoring of practical context(Owen et al., 2007); 3, greater accuracy in discerning a concave mask,as described above, or in which attention to larger Gestalt factorsmight be misleading (Uhlhaas and Silverstein, 2005; Uhlhaas et al.,2005, 2006); and 4, more accurate perception of speech when pairedwith video footage of incongruous facial movements (the McGurkeffect) (Pearl et al., 2009).

Findings from a range of neurocognitive experimental paradigmsare consistent with the memory–prediction model. An example ofthis is mismatch negativity (MMN), which refers to a change in brainactivity in response to the occurrence of novel, unexpected stimuli,leading to an attentional shift (Naatanen and Kahkonen, 2009;Naatanen et al., 2011). The most widely used experimental paradigmto elicit MMN is the oddball paradigm, which involves presentingunexpected, deviant (i.e., “oddball”) stimuli amidst an otherwise con-tinuous stream of stimuli and measuring the resulting electrical brainactivity using electroencephalography (EEG). The stimuli may bedeviant due to presenting a difference in any of its physical properties(e.g., pitch, duration, location, intensity) compared to previouslypresented stimuli. Studies have indicated a consistent decrease in theamplitude of the MMN in response to oddball stimuli in schizophrenia(Umbricht and Krljes, 2005), although there is evidence that thisdecrease is not always present at the first episode (Salisbury et al.,2002; Umbricht et al., 2003a) and that deficits in MMN correlate withillness duration (Umbricht and Krljes, 2005). These latter findings aresomewhat at odds with a study indicating that MMN impairmentwas a significant predictor of transition to psychotic disorder in a

Please cite this article as: Nelson, B., et al., What are the neurocognitivphenomenology and neurocognition, Schizophr. Res. (2013), http://dx.do

sample clinically at high risk, i.e. prior to illness onset (Bodatsch etal., 2011). Overall, these data relating to brain electrical activity indicatea reduced ability to discriminate between relevant and irrelevant stim-uli in schizophrenia. Interestingly, the MMN abnormality has beenfound to correlate with compromised global functioning (Light andBraff, 2005; Rasser et al., 2011; Henriksen and Parnas, 2012) and socialcognition (Wynn et al., 2010) in schizophrenia patients, possibly indi-cating that this basic information processing disturbance may have adownstream effect on a person's ability to function in everyday life. Itis of note that the MMN deficits are not observed (or, if present, areless pronounced (Jahshan et al., 2012)) in other major mental illnessessuch as bipolar disorder or major depression (Catts et al., 1995;Umbricht et al., 2003b). The generation of MMN is thought to reflectthe functioning of N-methyl-D-aspartate receptors (NMDA-R) (Javittet al., 1996), which are essential for memory encoding. Therefore, theNMDA-R hypofunction observed in schizophrenia is likely to beresponsible for some of the memory and cognitive deficits observedin the illness (for a review see Javitt (2010)).

Another relevant construct from neurocognitive research is latentinhibition (Gray et al., 1992; Lubow and Gewirtz, 1995; Gray, 1998).Latent inhibition is a neurologically-based concept that describes thephenomenon of attenuated attention to stimuli upon repeated expo-sure. It is based on the notion of a gatingmechanism that allows organ-isms with complex nervous systems to cease responding to stimuliwith no apparent motivational or emotional value (Peterson et al.,2002). Reduced latent inhibition (i.e., non-reduction of attention tostimuli upon repeated exposure) has been found to be characteristicof the schizophrenia spectrum, including both schizotypy (Baruch etal., 1988b; Lubow et al., 1992; Allan et al., 1995; Braunstein-Bercovitzet al., 2002) and schizophrenia, particularly in its acute rather thanchronic manifestations (Baruch et al., 1988a; Gray et al., 1992). Thereis some inconsistency in the literature with regard to the associationbetween latent inhibition abnormalities and positive and negativesymptom domains (Cohen et al., 2004; Yogev et al., 2004; Kumariand Ettinger, 2010). The integrity of sensory gating processes can bemeasured with EEG during an auditory dual-click paradigm. The ampli-tude of the positive potential occurring approximately 50 mspost-stimulus (i.e., the P50) is normally decreased when the secondclick is presented. This decrease in amplitude is thought to reflect asensory gating mechanism that functions to protect against informa-tion overload. An abnormal auditory gating (i.e., a decreased attenua-tion in the amplitude of the second P50) has been observed inschizophrenia (Bramon et al., 2004; Patterson et al., 2008). This indi-cates that these patients cannot inhibit, or “gate”, irrelevant sensoryinput, leading to an overload of information reaching the brain andcontributing to perception and attention deficits in schizophrenia. In-terestingly, P50 suppression impairment has been observed in patientswith bipolar disorder with a history of psychosis, but not in bipolarpatients without a history of psychosis, indicating that this neurophys-iological abnormality may be specific to psychotic symptoms (for areview see Thaker (2008)).

The disturbances of attention and memory described in theseneurocognitive models may lead to distorted interpretations of events,e.g. cognitive associations between irrelevant stimuli, which may con-tribute to delusional thinking. In other words, the neurocognitive dis-turbances may have a bottom-up influence on cognitive processes of“meaning-making” in schizophrenia. The neurocognitive disturbancesmay also be associated with various disturbances of subjective experi-ence, such as hyper-reflexivity, disturbed perception of affordances,perspectival abridgement, disturbed “grip” or “hold” on the perceptualand cognitive world, sense of perplexity, and lack of common sense, allof which are aspects of the basic self-disturbance model (Sass, 1992;Sass and Parnas, 2007). These connections between aberrant salience(neurocognitive disturbance) and anomalous subjective experiences(phenomenological disturbances) will now be addressed (see Table 1for summary).

e correlates of basic self-disturbance in schizophrenia?: Integratingi.org/10.1016/j.schres.2013.06.033

Table 1Proposed neurocognitive and phenomenological correlates indicative of basic self-disturbance in schizophrenia.

Basic self disturbance: levels of enquiry

Neurocognitive Phenomenological

Neural/electrophysiological Behavioural/cognitive

Source

monitoring

deficits

− Efference copy

(Crapse and Sommer,

2008; Stephen et al,

2009)

− Corollary discharge

(Poulet and Hedwig,

2007; Taylor, 2011;

Whitford et al, 2011)

− Reduced functional

connectivity

(Breakspear et al, 2003;

Fletcher et al, 1996,

1998; Ford et al, 2002,

2005, 2008, 2012;

Lawrie et al, 2002)

− Elevated “resting state”

brain activity

(Whitfield-Gabrieli et

− Endogenous−exogenous

confusion

(Blakemore et al, 2000;

Keefe, 1998; Wilquin and

Delevoye, 2012)

− Prediction errors

(Feinberg, 1978; Fletcher

and Frith, 2009; Frith 1992,

2012; Gray, 1998; Hemsley,

1992, 2005a,b)

− Diminished ownership of mental

content (Parnas, 2003; Parnas et al,

2005b)

− “Transitivistic” phenomena: self-other

boundary confusion (Parnas et al, 2005b;

Sass, 1992)

− Hyper-reflexivity (Sass, 1992; Sass and

Parnas, 2003, 2007)

al, 2009; Northoff and

Qin, 2011)

Aberrant

salience

− Latent inhibition (Gray,

1998; Gray et al, 1992;

Lubow and Gewirtz,

1995)

− Mismatch negativity

(Bodatsch et al, 2011;

Naatanen and

Kahkonen, 2009;

Naatanen et al, 2011;

Todd et al, 2012;

Umbricht and Krljes,

2005)

− Attention and memory

disturbances (Hemsley,

1998, 2005a, b; Keefe and

Kraus, 2009; Keefe et al,

2011; Kraus et al 2009)

− Failed suppression of

attention to irrelevant

stimuli (Morris et al, 2012)

− Weakening of contextual

constraint (Benton and Van

Allen, 1972; Cavezian et al,

2007; Doniger et al, 2007;

Emrich, 1989; Hemsley,

2005a, b; Newby, 1998;

Owen et al, 2007; Pearl et al,

2009; Polyakov, 1969;

Uhlhaas et al, 2006; Uhlhaas

and Silverstein, 2005;

Whitaker et al, 2001)

− Prediction errors (Feinberg,

1978; Fletcher and Frith,

2009; Frith 1992; Gray,

1998; Hemsley, 1992,

2005a,b)

− Hyper-reflexivity (Sass, 1992; Sass and

Parnas, 2003, 2007)

− Rigidity and perplexity in interaction with

world (Parnas, 2011; Parnas et al, 2005;

Sass, 1992)

− Disturbance of “common sense”

(Blankenburg, 1969, 2001; Stanghellini,

2004)

− Disturbed “grip” or “hold” on conceptual

and perceptual field (Sass and Parnas,

2003, 2007)

− Diminished perspectival abridgement

(Sass, 1992; Sass and Parnas, 2003)

− Diminished “affordance value” of objects

(Sass, 1992)

4 B. Nelson et al. / Schizophrenia Research xxx (2013) xxx–xxx

3. Phenomenological correlates

The tacit process of “matching” stimuli to predictions and “fillingin the gaps” in stimuli described above endows perception with a

Please cite this article as: Nelson, B., et al., What are the neurocognitivphenomenology and neurocognition, Schizophr. Res. (2013), http://dx.do

fluidity and automaticity and facilitates ease of interaction with theenvironment. However, if there is a breakdown in this system, asseems to be the case in schizophrenia, a person is likely to find him-self directing attention to relatively fragmentary stimuli that

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5B. Nelson et al. / Schizophrenia Research xxx (2013) xxx–xxx

normally go unnoticed (aspects of the environment, but also of self-experience, such as cenesthetic sensations), to the exclusion of larger,more meaningful Gestalts; and this in turn will elicit ever moreintense and ever more fragmenting forms of focal attention. If anew context does not easily “match” what I predict to occur in thatsituation then I must pay more attention to the constituent aspectsof that context/situation. To return to the (rather simplistic butnevertheless useful) “STOP” example, if I do not automatically men-tally complete the “ST” with “OP” (to form the word “STOP”) then Imust pay more attention to the stimulus “ST” and put extraeffort into determining its meaning. It is possible that this may havea cascading effect on my attentional and reflective processes. Thatis, my initial difficulty comprehending the meaning of “ST” and theextra attention I therefore give to this stimulus might lead to me be-coming excessively aware of my own attentional processes (“Why amI paying this so much attention?”, “Why aren't others paying thismore attention?” etc.). This process is captured in the phenomenolog-ical concept of hyper-reflexivity — that is, excessive attention beingpaid to aspects of experience that are normally tacit and remain inthe “background” of awareness. Hyper-reflexivity is one of the centralfeatures of disturbed basic selfhood (see Part 1, this issue).

In the rather prototypical case study of “Adam” presented in Nelsonand Sass (2009), the patient complained of all aspects of his functioningand action requiring a lot more thought and effort than normal,prompting him to “give up” and remain immobile and unresponsive:“I lost my automatic things — they became conscious. Everything I didwas a conscious effort — for example, picking up a glass.” (p. 493). Histhoughts were slowed down and disconnected, as though they lackedameaningful flow.2While this is a form of hyper-reflectivity the processof attention being drawn to irrelevant or background stimuli is also like-ly to be associated with operative hyper-reflexivity (see distinctionmade in Part 1, this issue)— that is, acts of awareness that are not intel-lectual, effortful or voluntary but are automatic in nature, such as sensa-tions suddenly “popping” into awareness, as represented by someof thecenesthetic “basic symptoms” of schizophrenia (McGhie and Chapman,1961; Gross et al., 1987).

Herewe see that the excessive attention to tacit, background aspectsof experience and stimuli (the tacit becoming focal), possibly driven bythe compromised memory–prediction processes described above, candisrupt one's ability to act or behave in theworld. Rather than automat-ically “knowing” how to respond to a particular situation or what sensetomake out of stimuli, the personmay be “caught up” or “stuck” on cog-nitive or perceptual stimuli that would normally be incorporatedsmoothly into the stream of experience. These extra “processing”requirements may have the effect of introducing an awkward rigidity,slowness and sense of perplexity into the person's interactions withtheworld,which have all been described in the phenomenological liter-ature (Sass, 1992; Parnas et al., 2005; Parnas, 2011).

The (temporal or visual) context in which a stimulus appears or anevent occurs tends to anchor its significance and directs how to inter-pret it. The neurocognitive disturbances described above show howan individual stimulus (internal or external) might “come loose”from its context. For example, consider hearing a siren from a localfire station most evenings at about the same time. The temporalcontext (the regularity of the noise), and perhaps also the contextof having been informed by a neighbour that the fire station tests itssiren at that time, will guide how this noise is interpreted. However,a reduced influence of such contextual factors is likely to lead tomore arbitrary and idiosyncratic interpretations of such an event.These neurocognitive disturbances may lead a person to pay attentionto “irrelevant” stimuli (i.e., stimuli that do not seem to be providingany “new” information) as if they were “new” and of potential signifi-cance — and possibly less attention to “relevant” stimuli. That is, the

2 Also see the EASE instrument (Parnas et al., 2005), items 2.2 (Distorted first personperspective) and 2.6 (Hyperreflectivity).

Please cite this article as: Nelson, B., et al., What are the neurocognitivphenomenology and neurocognition, Schizophr. Res. (2013), http://dx.do

appropriate salience of events and objects is disrupted (Kapur, 2003;Hemsley, 2005a, 2005b; Kapur et al., 2005). This accords well withmany of the subjective disturbances in schizophrenia described in thephenomenological literature. The basic self-disturbance model involvesa disturbed “grip” or “hold” on the conceptual or perceptual field (seePart 1, this issue). There is an alteration in the objects or field of aware-ness, a disruption of the focus or saliencewith which objects andmean-ings emerge from a background context (Sass and Parnas, 2007). Todraw on terminology from perception research, the normal figure–ground relationship is disrupted. Individual thoughts or perceptionscan seem to be atomistic, disconnected from other thoughts or percep-tions, and may take on a thing- or object-like quality (see EASE, items1.7 and 1.8). Phenomenological literature (Sass, 1992; Sass andParnas, 2003) also describes various types of perspectival shift or driftthat undermine the possibility of blocking out alternative perspectives(referred to as “perspectival abridgement”), which can feed into statesof perplexity or ambivalence: “He is ‘snowed under with options’; e.g.he thinks that he probably ought to become a vegetarian even thoughhe loves meat. Such considerations lead him into ‘doubleness’ and‘silly, blind alleys’” (Parnas et al., 2005, p.242; see EASE item 1.9). Thisis preciselywhat onewould expectwith a disruption of the “grounding”influence of background context (in itsmost inclusive sense) on how anindividual stimulus (internal or external) is experienced.

Similarly, the disturbances of “common sense” in schizophrenia de-scribed in the phenomenological literature may be seen as arising froma weakening of the “grounding” effect of context. Blankenburg (1969,2001) described an essential feature of schizophrenia as a loss or lackof “common sense”. Common sense, as Blankenburg used the term, re-fers to the ability “to see things in the proper perspective, to distinguishbetween what is relevant and irrelevant, likely and improbable, which is amore elementary ability than to distinguish between what is true andwhat is false” (Bovet and Parnas, 1993, p.583, italics added). To see things“in the proper perspective” implies being able to automatically grasp thesignificance of an event, act or utterance given its social context. The dis-ruption of contextual understanding, as described in the neurocognitivemodels above,will undermine the ability to distinguish the relevant fromthe irrelevant, with possibly increased significance being assigned to ir-relevant stimuli. This will disrupt an individual's attunement to othersand the world (the disturbances of “common sense”), a characteristicfeature of schizophrenia (Stanghellini, 2004; Stanghellini and Lysaker,2007) that has been formulated in the cognitive psychology literatureas disturbances of social cognition (Green et al., 2005; Penn et al.,2008). The notion of an erosion in the “grounding” and “orienting” influ-ence of context has substantial affinities with Rhodes and Gipps' (2008)thesis that a disruption in the foundational, non-representational,non-rule-governed, dispositional structure of everyday understanding(drawing on philosophical concepts of the “Bedrock” and “Background”)underlies the formation and maintenance of delusions.

These neurocognitive models also have relevance to the loss of 2ob-jects' “affordance” value that has been described in phenomenologicalliterature (Sass, 1992), and which contributes to a disturbed self–world relationship (Parnas et al., 2002; Henriksen et al., 2010). Asdescribed above, these models emphasise the breakdown in contextualperception/understanding of stimuli. An important feature of the self–world relationship is the functional value of objects in the world, howthey might be used by us, which is referred to as the affordance valueof objects (Gibson, 1977, 2001). Our motivations, needs and desiresstructure and direct how we view or approach objects, e.g. if I am lostin a forest at night and feel vulnerable I am likely to see a metal poleI am carrying as a potential weapon. This is the pole's affordancevalue for me in this context. In many ways, this “directed” relationshipto the world (the phenomenological concept of intentionality (Spinelli,1989)) provides context and organises our multifarious experience ofthe world. The attenuation or loss of affordance value and its replace-ment with a sense of an object's crude physical presence (or “merebeing” (Nelson and Sass, 2008; Sass, 1992)) has been observed in

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psychotic states. A hammer, for example, is no longer a tool but isperceived as a pure object. (See Nelson and Sass (2008) for how thismight also occur during drug intoxicated states, e.g. Huxley's (1954/2004) description of the “thing-ness” or “Is-ness” of his surroundings.)In this state, conceptual frameworks recede in favour of “mere being”.This experience can be characterised by a sense of nausea and horrorat the arbitrariness of things (along with a sense of wonder) (Sass,1992) (also see Sartre's (1964) classic description in his novel Nausea).

While the above discussion focuses on aspects of self-disturbancethat involve disruptions in the experience of and ability to interactwith others/the environment, it is important to note that the neuro-cognitive concept of aberrant salience, broadly conceived (as de-scribed above), accords with more “private”, “non-interactive” (andarguably more fundamental) aspects of self-disturbance as well. Ab-errant salience involves focal attention being directed to the familiaror “irrelevant” and making the “background” or the implicit notewor-thy, a process captured in the concept of hyper-reflexivity (see Nelsonet al., in press-b). This disrupts the naturalness and automaticity ofvarious aspects of self-experience (Sass, 1992; Sass and Parnas,2003). If aspects of self-experience (e.g., bodily experience such askinaesthetic sensations in my elbow or cognitive processes such as“inner speech” underlying thinking) come to be noticed (i.e., enterthe focus of awareness) then this can have the effect of distancingor alienating oneself from these components of selfhood and the nor-mally unified nature of basic self-experience can become fragmented.This can result in these aspects of consciousness no longer being livedor “inhabited” aspects of selfhood (i.e. no longer constituting self-hood) but becoming alienated processes, acts or experiences (Sass,1992; Sass and Parnas, 2003). Hemsley (1998) argues that this dis-ruption in the automatic ability to appropriately “integrate” sensoryinput/information with stored material (aberrant salience) can dis-rupt the sense of continuity and consistency in sense of self, contrib-uting to a gradually developing instability in personal identity (alsosee EASE, domain 2 items relating to identity confusion and instability(Parnas et al., 2005)).3

The freeing of stimuli from the usual significance bestowed on themby context (or the “openness” to stimuli irrespective of their past sig-nificance) might confer some benefits as well as interfere with aperson's functioning (Hemsley, 1998; Nelson and Rawlings, 2008). Asmentioned above, Owen et al. (2007) found that patients with schizo-phrenia in fact displayed greater logical ability than healthy controls.That is, the patient group displayed greater “theoretical rationality”(formal logical rationality) than “practical rationality” (socially sharedbackground assumptions about the world or “common sense”), asassessed using syllogisms. These findings suggest that schizophreniapatients are less constrained or directed by contextual information(in this case, social understanding or “common sense”), which facili-tates formal logical cognitive processes. The link between the schizo-phrenia spectrum and enhanced creative ability is also of relevancehere, since creativity, and especially certain of its forms, may benefitfrom freedom from conventional expectations, assumptions, andmodes of attention (Schuldberg, 1997, 2000–2001; Nettle, 2006;Nettle and Clegg, 2006; Nelson and Rawlings, 2008).

4. Conclusions and future directions

Although progress has been made in understanding phenomeno-logical and neurocognitive disturbances in schizophrenia, these“levels” or domains of enquiry have tended to remain separate fromeach other. In these papers, we have argued that there is a

3 The issue of the relationship between basic or minimal selfhood and more elabo-rated aspects of selfhood, such as the particularities of personal identity (sometimesreferred to as “narrative selfhood”), remains unclear, but here we see how the formermay disrupt the development and maintenance of the latter (also see Nelson et al. (inpress)).

Please cite this article as: Nelson, B., et al., What are the neurocognitivphenomenology and neurocognition, Schizophr. Res. (2013), http://dx.do

convergence of models and empirical findings from these levels of en-quiry around the concept of disturbance of the basic sense of self. Wehave described how the neurocognitive disturbances of source moni-toring and aberrant salience accord with many of the anomalies ofsubjective experience described in the phenomenological literature(see Table 1 for a summary). These neurocognitive disturbancesmay constitute the neural correlates or cause of an abnormal senseof basic selfhood or ipseity (and by implication, of experience ofothers and the world), which may, in turn, evolve into frank psychoticsymptoms. However, the distortions in the basic sense of self arearguably more primary (and often more disturbing to the person(Saks, 2007; Kean, 2009, 2011)) than the resultant psychotic symp-toms themselves. The neurocognitive models discussed above maypick up more directly on the specific disturbances at play in schizo-phrenia than more standard neurocognitive models of schizophreniabased on measures of cognitive functioning devised for measuringgeneral intelligence or brain injury in patients with no previousrelevant illness. The point of these papers has not been to “reduce”phenomenological disturbances to neurocognitive or neurologicaldisturbances, but rather to point towards convergences in theseareas of research and how they might be integrated in “cross-level”models of schizophrenia and in future empirical research.

A number of hypotheses and directions for future research emergefrom this discussion. They include the following:

1. Based on the above argument we would expect neurocognitivemeasures of source monitoring deficits and aberrant salience andphenomenological measures of basic self-disturbances to be posi-tively correlated. We suggest the inclusion of measures of theseconstructs (such as neurocognitive measures of corollary dis-charge, mismatch negativity and latent inhibition and clinical mea-sures of basic self-disturbance, such as the EASE instrument) inpsychotic samples to assess this hypothesis.

2. These neurocognitive and phenomenological disturbances may as-sist in the identification of people at highest risk of developingschizophrenia and other psychotic disorders. There are indicationsof this in several recent studies in UHR samples (Hoffman et al.,2007; Nelson et al., 2012). Measures of these neurocognitive dis-turbances (such as binocular depth inversion, perceptual closure,learned irrelevance, spurious messages from noise, mismatch neg-ativity, salience attribution, reversal learning tasks, and temporalbinding tasks) and phenomenological disturbances (such as theEASE instrument) may prove to enhance identification of “truepositives” within high-risk cohorts.

3. What is the relationship between source monitoring deficits andaberrant salience? Are they different aspects of a single underlyingdisturbance or distinct neurocognitive processes that are both dis-turbed in schizophrenia? It would seem, based on the above re-view, that prediction errors could account for both sourcemonitoring deficits and aberrant salience (McClure et al., 2003;Corlett et al., 2007), i.e., self-generated stimuli are more predict-able than externally-generated stimuli and that prediction errorsmight thereby lead to confusion of internal–external boundaries(source monitoring deficits) and that prediction errors based onbreakdown of context-dependent processing/interpretation of in-formation result in aberrant salience. Alternatively, it may be pos-sible that source monitoring deficits might cause downstreamabnormalities in salience, or vice versa (Whitford et al., 2012). Itis also possible that all these variables are but sequelae or manifes-tations of a distorted core self experience that has still other keyneurobiological correlates (see Sass, in press).

4. Are the neurocognitive and phenomenological disturbances of atrait or state nature? It would be of interest to investigate whetherthey vary in relation to intensity of psychotic symptoms or aremore enduring, symptom-independent disturbances. Longitudinalstudies of psychotic samples, as well as genetic linkage studies and

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studies with non-psychotic schizophrenia spectrum samples,would shed light on this issue. One might consider as well (andtest experimentally) how much these disturbances (of self-experience and also of neurocognitive functioning on variousmeasures) might vary in accordance with changes of orientation,attentional attitude, action-orientation, or motivational state, asmight well be expected (see Sass, in press).

5. What are the treatment options for these forms of disturbances?Some suggestions have been made regarding possible avenuesfor psychosocial interventions for basic self-disturbance (Nelsonand Sass, 2009; Nelson et al., 2009). Promising results have beenfound for body oriented psychological therapy (BPT), which aimsto foster a coherent sense of embodied self, self-directed and vital-ized social interaction and emotional expressiveness, in improvingself-disturbances and negative symptoms (Röhricht et al., 2009).With regard to the neurocognitive disturbances, aberrant salienceis thought to be due to excessive dopamine transmission (Kapur,2003; Kapur et al., 2005), which is targeted by the current genera-tion of antipsychotic medications. Of course, these medications arenot unproblematic. They may in fact dampen the tonic dopaminer-gic signal to such an extent that relevant internal and external stim-uli fail to generate attentional and motivational responses, whichmay contribute to negative symptoms (Gardner et al., 2005).Whitford et al. (2012) suggest that abnormal myelination of frontal-ly projecting fasciculi may be responsible for corollary dischargedeficits (due to conduction delays) and that remyelination medica-tions, such as those currently used in the treatment of multiplesclerosis, may be of value. On the other hand, in view of their centralrole in long-term potentiation (LTP) and memory formation pro-cesses, NMDA receptors also represent a promising target. Neuro-cognitive remediation therapies that focus on attention deficitsand prediction errors may also be of value. These are importantavenues for further research.

Role of funding sourceNo funding source.

ContributorsAll authors contributed to the content of the manuscript.

Conflict of interestThe authors report no conflicts of interest.

AcknowledgmentsBN is supported by an NHMRC Career Development Fellowship (#1027532). TJW is

supported by a Young Investigator Award (Barbara and John Streicker Investigator)from the National Alliance for Research on Schizophrenia and Depression (NARSAD)Brain and Behavior Research Foundation (#17537).

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