The neurophenomenology of early psychosis: An integrative empirical study

https://doi.org/10.1016/j.concog.2019.102845Get rights and content

Highlights

  • A core feature of schizophrenia may be disturbed self-experience.

  • The neural underpinnings of disturbed self-experience are not yet clear.

  • This study found a relationship between source monitoring deficits and disturbed self-experience in early psychosis patients.

  • Aberrant salience showed a relationship with general psychopathology.

  • A revised neurophenomenological model of schizophrenia spectrum disorders is proposed.

Abstract

Background

The integration of various domains or levels of analysis (clinical, neurobiological, genetic, etc.) has been a challenge in schizophrenia research. A promising approach is to use the core phenomenological features of the disorder as an organising principle for other levels of analysis. Minimal self-disturbance (fragility in implicit first-person perspective, presence and agency) is emerging as a strong candidate to play this role. This approach was adopted in a previously described theoretical neurophenomenological model that proposed that source monitoring deficits and aberrant salience may be neurocognitive/neurobiological processes that correlate with minimal self-disturbance on the phenomenological level, together playing an aetiological role in the onset of schizophrenia spectrum disorders. The current paper presents full cross-sectional data from the first empirical test of this model.

Methods

Fifty ultra-high risk for psychosis patients, 39 first episode psychosis patients and 34 healthy controls were assessed with a variety of clinical measures, including the Examination of Anomalous Self-Experience (EASE), and neurocognitive and neurophysiological (EEG) measures of source monitoring deficits and aberrant salience.

Results

Linear regression indicated that source monitoring (composite score across neurocognitive and neurophysiological measures), with study group as an interaction term, explained 39.8% of the variance in EASE scores (R2 = 0.41, F(3,85) = 14.78, p < 0.001), whereas aberrant salience (composite score) explained only 6% of the variance in EASE scores (R2 = 0.06, F(3,85) = 1.44, p = 0.93). Aberrant salience measures were more strongly related to general psychopathology measures, particularly to positive psychotic symptoms, than to EASE scores.

Discussion

A neurophenomenological model of minimal self-disturbance in schizophrenia spectrum disorders may need to be expanded from source monitoring deficits to encompass other relevant constructs such as temporal processing, intermodal/multisensory integration, and hierarchical predictive processing. The cross-sectional data reported here will be expanded with longitudinal analysis in subsequent reports. These data and other related recent research show an emerging picture of neuro-features of core phenomenological aspects of schizophrenia spectrum disorders beyond surface-level psychotic symptoms.

Introduction

In recent years there has been considerable interest in the construct of minimal self-disturbance as a phenotypic marker of the schizophrenia spectrum (Maj, 2012, Nelson et al., 2014, Nelson and Raballo, 2015, Parnas and Henriksen, 2014), particularly with regard to its utility in nosological, aetiological and prediction research. The ‘minimal self’, aka ‘basic’ or ‘core’ self, widely discussed in neuroscience, philosophy of mind, and phenomenology, refers to the pre-reflective and immediate consciousness of action, experience, and thought. Two nested concepts can be identified as constituting this aspect of selfhood: sense of ownership/mine-ness and sense of agency (Gallagher, 2011). While the former refers to perceiving my body, perceptions, and thoughts as my own, the latter refers to experiencing myself as the source of my actions and their consequences. These are generally implicit aspects of a normal sense of minimal self and facilitate interactions with others/the world (Zahavi, 2003). A fragile or unstable minimal self can manifest in a variety of anomalous subjective experiences including:

  • disturbed sense of ownership of moment-to-moment experience, e.g., the sense that my thoughts or body parts are not my own;

  • disturbed agency, e.g., the sense of not being the source or cause of my actions;

  • unstable ‘first-person’ perspective, associated with states of depersonalisation, e.g., feeling as though I am watching myself from a distance or somehow alienated from my own body;

  • difficulty forming a continuous and coherent identity, e.g., feeling anonymous or without a stable perspective and identity over time.

Such experiences frequently result in perplexity, disorientation, and difficulties with social functioning and understanding, also referred to as a lack of common sense (Blankenburg, 2001), and are profoundly distressing (Nelson et al., 2009). Minimal self-disturbance can intensify and crystallise over time into full-blown positive and negative psychotic symptoms (Davidsen, 2009, Møller and Husby, 2000, Nelson et al., 2012, Parnas, 1999, Parnas, 2000, Sass and Parnas, 2003).

The main measure of minimal self-disturbance is the Examination of Anomalous Self-Experience (EASE) (Parnas et al., 2005a, Parnas et al., 2005b). Empirical findings using the EASE and pre-EASE scales indicate that minimal self-disturbance:

  • characterises schizophrenia spectrum disorders independent of presence of frank psychotic symptoms, i.e., is present in schizotypal disorder as well as in psychotic schizophrenia-spectrum disorders (Handest and Parnas, 2005, Nordgaard and Parnas, 2014, Parnas et al., 2005a, Parnas et al., 2005b);

  • correlates moderately with clinical features of schizophrenia (Nordgaard & Parnas, 2014);

  • is more prominent in schizophrenia than in psychotic disorders outside the schizophrenia spectrum, such as bipolar disorder with psychosis (Haug et al., 2012, Nordgaard and Parnas, 2014, Parnas et al., 2003);

  • correlates moderately with prodromal symptoms in non-psychotic adolescents (Koren et al., 2016, Koren et al., 2013, Raballo et al., 2016) and predicts future onset of schizophrenia spectrum disorders in non-psychotic clinical populations (Parnas et al., 2011) and in clinical high risk for psychosis patients (Nelson et al., 2012);

  • increases in relation to schizophrenia symptom expression in a large genetic linkage sample (Raballo and Parnas, 2011, Raballo et al., 2011) and in relation to severity of psychotic diagnostic staging (Raballo et al., 2018);

  • is related to suicidality (Haug et al., 2012, Skodlar and Parnas, 2010, Skodlar et al., 2008), poor functioning (Haug et al., 2014, Raballo et al., 2016), and longer duration of untreated psychosis (Haug et al., 2015) in schizophrenia, and to failure to achieve symptomatic and functional recovery in patients with psychotic disorders (Svendsen, Merete, Møller, Nelson, Haug, & Melle, 2019).

Together, this body of research indicates that minimal self-disturbance is a trait vulnerability feature that has considerable specificity to schizophrenia spectrum disorders and is present in the prodromal phase of these disorders (Nelson et al., 2014, Nelson and Raballo, 2015, Parnas, 2011, Parnas, 2012, Parnas et al., 2002, Parnas and Henriksen, 2014, Sass and Parnas, 2003). Indeed, disturbed ‘self-experience’ is included in the schizophrenia criteria of the beta version of the International Classification of Diseases 11th revision (ICD-11) (Organisation, 2018).

In our view, schizophrenia research has suffered from a lack of integration across ‘levels’ of analysis, such as phenomenological, psychological, neurocognitive, neurobiological, genetic and social levels (Martin et al., 2014, Nelson et al., 2014a, Nelson et al., 2014b). We have argued that integrative models of vulnerability to schizophrenia spectrum disorders should be guided and constrained by the disorders’ core phenomenological features (Parnas & Zandersen, 2018), which can function as a central organising factor akin to Minkowski (1926) concept of le trouble générateur (generating disorder). Minimal self-disturbance is emerging as a strong candidate for this role. It is not clear at this stage how minimal self-disturbance relates to these different levels of analysis (see Sass, Borda, Madeira, Pienkos, and Nelson (2018) for a recent attempt at theoretical integration). Although there has been considerable recent empirical neuroscientific research into anomalies of bodily (e.g., Benson and Park, 2019, Sestito et al., 2017, Sestito et al., 2015), temporal (e.g., Giersch et al., 2016, Giersch and Mishara, 2017, Martin et al., 2018, Martin et al., 2014) or perceptual experience (e.g., Uhlhaas & Mishara, 2007) in the schizophrenia spectrum, this has tended not to extend to the broader construct of minimal self-disturbance which includes, but is not limited to, anomalous bodily, temporal or perceptual experience.

The theoretical models regarding neuro-correlates (neurocognitive, neurophysiological and neurobiological correlates) of minimal self-disturbance (Borda and Sass, 2015, Mishara et al., 2015, Nelson and Sass, 2017, Nelson et al., 2014a, Nelson et al., 2014b, Parnas et al., 1996, Sass and Borda, 2015) have not been sufficiently empirically examined to date. The four studies that have directly examined neurocognitive correlates of minimal self-disturbance have found no correlation or a weak correlation between the variables (Comparelli et al., 2016, Haug et al., 2012, Koren et al., 2017, Nordgaard et al., 2015). However, the neurocognitive variables examined in these studies were derived from traditional measures of general intelligence, psychomotor speed, working memory and executive function, which may lack specificity to the disturbances at play in minimal self-disturbance (Nelson and Sass, 2017, Nelson et al., 2014a, Nelson et al., 2014b). Indeed, two recent studies are consistent with the suggestion of more specific neuro-disturbances being of relevance to minimal disturbance. Sestito et al. (2015) found that facial reactions in response to negative emotional stimuli, recorded using electromyography, specifically and strongly correlated with minimal self-disturbance in schizophrenia spectrum patients. Martin et al. (2017) findings in schizophrenia indicated a relationship between compromised extraction of temporally predictive information assessed in experimental tasks and minimal self-disturbance. Given the complexity and foundational nature of the minimal self-disturbance construct it is likely that there are multiple rather than single neuro-mechanisms associated with this constellation of anomalous subjective phenomena (Martin et al., 2014).

Nelson et al. (Nelson and Sass, 2017, Nelson et al., 2014a, Nelson et al., 2014b) introduced a theoretical model proposing that the neuro-constructs of source monitoring deficits and aberrant salience may be of particular relevance to minimal self-disturbance in schizophrenia (see supplementary material video 1 for an animated diagram). Both of these constructs have been found to be prominent in schizophrenia spectrum disorders and related to psychosis risk (Gaweda et al., 2018, Gaweda et al., 2013, Waters et al., 2012). Source monitoring deficits refer to difficulties in making attributions about the origins of mental experiences, e.g., whether an experience was real or imagined, or whether its origin was internal (self-generated) or external (other-generated) (Crapse and Sommer, 2008, Stephan et al., 2009, Whitford et al., 2012). Aberrant salience refers to the reduced ability to suppress attention to irrelevant or familiar information or environmental stimuli (in other words, excessive attention to information that is irrelevant or highly familiar), leading to an unusual salience of stimuli (Kapur, 2003, Kapur et al., 2005).

There is strong face validity that the experiential disturbances that might arise from (and in turn consolidate (Sass et al., 2018)) these neuro-disturbances accord with many of the experiential alterations associated with minimal self-disturbance (Nelson and Sass, 2017, Nelson et al., 2014a, Nelson et al., 2014b, Sass et al., 2018). In brief, confusion regarding the origin of mental experiences associated with source monitoring deficits accord with a variety of aspects of minimal self-disturbance:

  • diminished ‘ownership’ of mental content;

  • confusion of self-other boundaries;

  • hyper-reflexivity, i.e., heightened awareness of aspects of one’s experience that are normally tacit and implicit) (Poletti, Gebhardt, & Raballo, 2017).

Aberrant salience, due to the reduction in the constraining and directing role of context, also accords with various aspects of minimal self-disturbance:

  • rigidity and perplexity in interaction with others/the world;

  • disturbance of ‘common sense’ (intuitive social understanding);

  • loosened ‘grip’ on the cognitive/perceptual world, i.e., the sharpness or stability with which meaning or perceptions emerge against a background context;

  • frequent shifts in perspective that undermine the possibility of blocking out alternative perspectives (referred to as ‘perspectival abridgement’);

  • weakened sense of the functional value (referred to as the ‘affordance value’) of objects;

  • hyper-reflexivity (see Nelson et al., 2014a, Nelson et al., 2014b for full explication of this integrated model).

We recently reported the first empirical support for the source monitoring aspect of this model, i.e., an association between minimal self-disturbance and source monitoring deficits in early psychosis patients (Nelson et al., 2019). However, these data, presented in letter format, were only partial data from the study. The purpose of the current report is to present the full data of this first empirical test of the proposed neurophenomenological model. The focus here is on cross-sectional association between variables.

It is particularly valuable to research pathogenic models of psychotic disorders in the early stages of disorder because these stages may allow a clearer view of the mechanisms at play, before the effects of advanced illness stages cloud the clinical picture (Klosterkötter et al., 2001, Nelson et al., 2008, Parnas, 2000, Yung et al., 2004), as well as point towards possible preventative treatment targets. In this study, clinical measures, including the EASE, and neurocognitive and neurophysiological measures of source monitoring deficits and aberrant salience were administered in two patient groups (a first-episode psychosis [FEP] sample and an ultra-high risk [UHR] for psychosis sample), as well as a healthy control (HC) group. We hypothesised that:

  • 1.

    Minimal self-disturbance, source monitoring deficits and aberrant salience would show an increasing gradient of severity from HC to UHR to FEP individuals (HC < UHR < FEP). The expectation that minimal self-disturbance would show this differentiation between groups was based on the fact that schizophrenia spectrum cases are mostly highly represented in the FEP group.

  • 2.

    Minimal self-disturbance would be predicted by source monitoring deficits and aberrant salience in FEP and UHR individuals.

Section snippets

Setting

Patients were recruited from Orygen Youth Health Clinical Program (OYHCP), a tertiary public mental health service for young people aged between 15 and 25 years living in north-western Melbourne, Australia. UHR participants were recruited from the Personal Assessment and Crisis Evaluation (PACE) clinic, a specialist psychosis risk clinic within OYHCP, and FEP participants were recruited from the Early Psychosis Prevention and Intervention Centre (EPPIC), a specialist clinic for first-episode

Demographic and clinical characteristics

The samples consisted of 50 UHR, 39 FEP, and 34 HC participants. Demographic characteristics and clinical scale scores are presented in Table 1. The HC group was older (by a mean of 2 years) than the clinical groups. The UHR sample consisted of the following sub-groups: APS = 37 (74%), APS + Trait Vulnerability = 10 (20%), APS + BLIPS = 2 (4%), and Trait Vulnerability = 1 (2%). SCID diagnoses are presented in Table 2. At the time of assessment, 11 (22%) of the UHR group were taking

Discussion

Our first hypothesis was that minimal self-disturbance, source monitoring deficits and aberrant salience would show an increasing gradient of severity from HC participants to UHR patients to FEP patients (FEP < UHR < HC). There was partial support for this hypothesis. While minimal self-disturbance showed this pattern of severity, the neurocognitive and neurophysiological findings were less clear. One neurocognitive test of source monitoring deficits (the temporal binding task) showed the

Ethics statement

The study was approved by the Melbourne Health Human Research and Ethics Committee (HREC). Study participants provided full written and informed consent.

Acknowledgment

This study was supported by a Brain and Behavior Research Foundation (BBRF) Independent Investigator Award (23199) to BN.

References (134)

  • E. Haug et al.

    The association between self-disorders and neurocognitive dysfunction in schizophrenia

    Schizophrenia Research

    (2012)
  • J. Horvath

    Action-related auditory ERP attenuation: Paradigms and hypotheses

    Brain Research

    (2015)
  • B.N. Jack et al.

    Inner speech is accompanied by a temporally-precise and content-specific corollary discharge

    NeuroImage

    (2019)
  • S. Kapur et al.

    From dopamine to salience to psychosis–linking biology, pharmacology and phenomenology of psychosis

    Schizophrenia Research

    (2005)
  • R.S. Keefe et al.

    The brief assessment of cognition in schizophrenia: Reliability, sensitivity, and comparison with a standard neurocognitive battery

    Schizophrenia Research

    (2004)
  • M. Maj

    The self and schizophrenia: Some open issues

    World Psychiatry: Official Journal of the World Psychiatric Association

    (2012)
  • J. Moore et al.

    Awareness of action: Inference and prediction

    Consciousness and Cognition

    (2008)
  • S. Moritz et al.

    No deficits in nonverbal memory, metamemory and internal as well as external source memory in obsessive-compulsive disorder (OCD)

    Behaviour Research and Therapy

    (2009)
  • B. Nelson et al.

    What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition: Part 2 (Aberrant salience)

    Schizophrenia Research

    (2014)
  • B. Nelson et al.

    What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition. Part 1 (Source monitoring deficits)

    Schizophrenia Research

    (2014)
  • J. Parnas

    The core Gestalt of schizophrenia

    World Psychiatry: Official Journal of the World Psychiatric Association

    (2012)
  • D. Pearl et al.

    Differences in audiovisual integration, as measured by McGurk phenomenon, among adult and adolescent patients with schizophrenia and age-matched healthy control groups

    Comprehensive Psychiatry

    (2009)
  • L. Postmes et al.

    Schizophrenia as a self-disorder due to perceptual incoherence

    Schizophrenia Research

    (2014)
  • P.L. Ackerman et al.

    Cognitive, perceptual-speed, and psychomotor determinants of individual differences during skill acquisition

    Journal of Experimental Psychology: Applied

    (2000)
  • N.C. Andreasen

    The scale for the assessment of negative symptoms (SANS)

    (1983)
  • Y. Benjamini et al.

    Controlling the false discovery rate: A practical and powerful approach to multiple testing

    Journal of the Royal Statistical Society

    (1995)
  • W. Blankenburg

    First steps toward a psychopathology of “common sense”

    Philosophy, Psychiatry, & Psychology

    (2001)
  • A. Bubic et al.

    Prediction, cognition and the brain

    Frontiers in Human Neuroscience

    (2010)
  • A. Clark

    Surfing uncertainty: Prediction, action, and the embodied mind

    (2015)
  • R. Clowes

    Rethinking the ipseity disturbance theory of schizophrenia through predictive processing

  • T.B. Crapse et al.

    Corollary discharge across the animal kingdom

    Nature Reviews. Neuroscience

    (2008)
  • K.A. Davidsen

    Anomalous self-experience in adolescents at risk of psychosis. Clinical and conceptual elucidation

    Psychopathology

    (2009)
  • M.B. First et al.

    Structured clinical interview for DSM-IV axis I disorders – Patient edition (SCID-I/P, Version 2.0)

    (1996)
  • M.B. First et al.

    Structured clinical interview for DSM-IV personality disorders (SCID-II)

    (1997)
  • P.C. Fletcher et al.

    Perceiving is believing: A Bayesian approach to explaining the positive symptoms of schizophrenia

    Nature Reviews. Neuroscience

    (2009)
  • M. Galdos et al.

    Affectively salient meaning in random noise: A task sensitive to psychosis liability

    Schizophrenia Bulletin

    (2011)
  • S. Gallagher

    Mutual enlightenment: Recent phenomenology in cognitive science

    Journal of Consciousness Studies

    (1997)
  • A. Giersch et al.

    Implicit timing as the missing link between neurobiological and self disorders in schizophrenia?

    Frontiers in Human Neuroscience

    (2016)
  • A. Giersch et al.

    Is schizophrenia a disorder of consciousness? Experimental and phenomenological support for anomalous unconscious processing

    Frontiers in Psychology

    (2017)
  • S.L. Giráldez et al.

    Assessment of essential components of schizotypy using neurocognitive measures

    Psychology in Spain

    (2000)
  • S. Gupta et al.

    The early identification of psychosis: Can lessons be learnt from cardiac stress testing?

    Psychopharmacology (Berl)

    (2016)
  • P. Haggard et al.

    Voluntary action and conscious awareness

    Nature Neuroscience

    (2002)
  • S.M. Haigh et al.

    Mismatch negativity in first-episode schizophrenia: A meta-analysis

    Clinical EEG and Neuroscience: Official Journal of the EEG and Clinical Neuroscience Society

    (2017)
  • P. Handest et al.

    Clinical characteristics of first-admitted patients with ICD-10 schizotypal disorder

    British Journal of Psychiatry – Supplementum

    (2005)
  • E. Haug et al.

    Selective aggregation of self-disorders in first-treatment DSM-IV schizophrenia spectrum disorders

    The Journal of Nervous and Mental Disease

    (2012)
  • E. Haug et al.

    High levels of anomalous self-experience are associated with longer duration of untreated psychosis

    Early Intervention in Psychiatry

    (2015)
  • R.E. Hoffman et al.

    Extracting spurious messages from noise and risk of schizophrenia-spectrum disorders in a prodromal population

    The British Journal of Psychiatry: The Journal of Mental Science

    (2007)
  • J. Hohwy

    The sense of self in the phenomenology of agency and perception

    Psyche

    (2007)
  • O.D. Howes et al.

    The dopamine hypothesis of schizophrenia: Version III–the final common pathway

    Schizophrenia Bulletin

    (2009)
  • Cited by (0)

    View full text