Sensory learning and inference is impaired in the non-clinical continuum of psychosis: a replication study

Our perceptions result from the brains ability to make inferences, or predictive models, of sensory information. Recently, it has been proposed that psychotic traits may be linked to impaired predictive processes. Here, we examine the brain dynamics underlying sensory learning and inference in stable and volatile environments, in a population of healthy individuals (N=75) with a range of psychotic-like experiences. We measured prediction error responses to sound sequences with electroencephalography, gauged sensory inference explicitly by behaviourally recording sensory regularity learning errors, and used dynamic causal modelling to tap into the underlying neural circuitry. We discuss the findings that were robust to replication across the two experiments (N=31 and N=44 for the discovery and the validation datasets, respectively). First, we found that during stable conditions, participants demonstrated a stronger predictive model, reflected in a larger prediction error response to unexpected sounds, and decreased regularity learning errors. Moreover, individuals with attenuated prediction errors in stable conditions were found to make greater incorrect predictions about sensory information. Critically, we show that greater errors in sensory learning and inference are related to increased psychotic-like experiences. These findings link neurophysiology to behaviour during sensory learning and prediction formation, as well as providing further evidence for the idea of a continuum of psychosis in the healthy, non-clinical population.

[1]  Michael Wagner,et al.  Prediction of Psychosis by Mismatch Negativity , 2011, Biological Psychiatry.

[2]  Karl J. Friston,et al.  The Computational Anatomy of Psychosis , 2013, Front. Psychiatry.

[3]  E. Schröger,et al.  Temporal regularity facilitates higher‐order sensory predictions in fast auditory sequences , 2014, The European journal of neuroscience.

[4]  Raymond J. Dolan,et al.  Outlier Responses Reflect Sensitivity to Statistical Structure in the Human Brain , 2013, PLoS Comput. Biol..

[5]  Rick A Adams,et al.  Computational Psychiatry: towards a mathematically informed understanding of mental illness , 2015, Journal of Neurology, Neurosurgery & Psychiatry.

[6]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[7]  M. Garrido,et al.  Sensory prediction errors in the continuum of psychosis , 2018, Schizophrenia Research.

[8]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[9]  Maxine T. Sherman,et al.  Prior expectations facilitate metacognition for perceptual decision , 2015, Consciousness and Cognition.

[10]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[11]  Karl J. Friston,et al.  The mismatch negativity: A review of underlying mechanisms , 2009, Clinical Neurophysiology.

[12]  A. Üçok,et al.  Mismatch negativity at acute and post-acute phases of first-episode schizophrenia , 2008, European Archives of Psychiatry and Clinical Neuroscience.

[13]  D. A. Kenny,et al.  The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. , 1986, Journal of personality and social psychology.

[14]  R. Näätänen,et al.  Mismatch negativity (MMN) deficiency: a break-through biomarker in predicting psychosis onset. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  Raymond J. Dolan,et al.  Exploration, novelty, surprise, and free energy minimization , 2013, Front. Psychol..

[16]  Karl J. Friston,et al.  The functional anatomy of the MMN: A DCM study of the roving paradigm , 2008, NeuroImage.

[17]  M. Chait,et al.  Enhanced deviant responses in patterned relative to random sound sequences , 2017, Cortex.

[18]  M. Garrido,et al.  Auditory prediction errors and auditory white matter microstructure associated with psychotic-like experiences in healthy individuals , 2019, Brain Structure and Function.

[19]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[20]  Karl J. Friston,et al.  Spatial Attention, Precision, and Bayesian Inference: A Study of Saccadic Response Speed , 2013, Cerebral cortex.

[21]  Tyrone D. Cannon,et al.  The prodromal questionnaire (PQ): Preliminary validation of a self-report screening measure for prodromal and psychotic syndromes , 2005, Schizophrenia Research.

[22]  Karl J. Friston,et al.  A Bayesian Foundation for Individual Learning Under Uncertainty , 2011, Front. Hum. Neurosci..

[23]  D. Linden,et al.  Evidence of absence: no relationship between behaviourally measured prediction error response and schizotypy , 2017, Cognitive neuropsychiatry.

[24]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses: The role of intrinsic connections , 2007, NeuroImage.

[25]  B. Rockstroh,et al.  Topography of the auditory P300 in schizotypal personality , 1999, Biological Psychiatry.

[26]  O. Bertrand,et al.  Implicit learning of predictable sound sequences modulates human brain responses at different levels of the auditory hierarchy , 2015, Front. Hum. Neurosci..

[27]  J. van os,et al.  Psychosis as a transdiagnostic and extended phenotype in the general population , 2016, World psychiatry : official journal of the World Psychiatric Association.

[28]  J. Os,et al.  Psychotic symptoms in non-clinical populations and the continuum of psychosis , 2002, Schizophrenia Research.

[29]  Karl J. Friston,et al.  Dynamic Causal Modeling of the Response to Frequency Deviants , 2009, Journal of neurophysiology.

[30]  M. Grube,et al.  Weighting of neural prediction error by rhythmic complexity: A predictive coding account using mismatch negativity , 2019, The European journal of neuroscience.

[31]  E. Bramon,et al.  P300 waveform and dopamine transporter availability: a controlled EEG and SPECT study in medication-naive patients with schizophrenia and a meta-analysis , 2013, Psychological Medicine.

[32]  Kristopher J Preacher,et al.  SPSS and SAS procedures for estimating indirect effects in simple mediation models , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[33]  Karl J. Friston,et al.  Dynamic causal modelling of evoked potentials: A reproducibility study , 2007, NeuroImage.

[34]  Peter Dayan,et al.  Expected and Unexpected Uncertainty: ACh and NE in the Neocortex , 2002, NIPS.

[35]  J. Changeux,et al.  A Neuronal Model of Predictive Coding Accounting for the Mismatch Negativity , 2012, The Journal of Neuroscience.

[36]  Danai Dima,et al.  Impaired top-down processes in schizophrenia: A DCM study of ERPs , 2010, NeuroImage.

[37]  R. Croft,et al.  Schizotypy and auditory mismatch negativity in a non-clinical sample of young adults , 2016, Psychiatry Research: Neuroimaging.

[38]  L. Elliot Hong,et al.  Refining the Predictive Pursuit Endophenotype in Schizophrenia , 2008, Biological Psychiatry.

[39]  Erich Schröger,et al.  Regularity Extraction and Application in Dynamic Auditory Stimulus Sequences , 2007, Journal of Cognitive Neuroscience.

[40]  I. Winkler,et al.  Mismatch negativity (MMN) to pitch change is susceptible to order-dependent bias , 2014, Front. Neurosci..

[41]  Klaas E. Stephan,et al.  Ketamine Affects Prediction Errors about Statistical Regularities: A Computational Single-Trial Analysis of the Mismatch Negativity , 2019, The Journal of Neuroscience.

[42]  Karl J. Friston,et al.  Bayesian inferences about the self (and others): A review , 2014, Consciousness and Cognition.

[43]  P. Paavilainen,et al.  Predictive coding of phonological rules in auditory cortex: A mismatch negativity study , 2016, Brain and Language.

[44]  E. Schröger,et al.  Differential Contribution of Frontal and Temporal Cortices to Auditory Change Detection: fMRI and ERP Results , 2002, NeuroImage.

[45]  A. Provost,et al.  Lasting first impressions: A conservative bias in automatic filters of the acoustic environment , 2011, Neuropsychologia.

[46]  Klaas E. Stephan,et al.  Inferring on the Intentions of Others by Hierarchical Bayesian Learning , 2014, PLoS Comput. Biol..

[47]  Albert R. Powers,et al.  Pavlovian conditioning–induced hallucinations result from overweighting of perceptual priors , 2017, Science.

[48]  P. DeRosse,et al.  Examining the Psychosis Continuum , 2015, Current Behavioral Neuroscience Reports.