Perceptual Gains and Losses in Synesthesia and Schizophrenia

Abstract Individual differences in perception are widespread. Considering inter-individual variability, synesthetes experience stable additional sensations; schizophrenia patients suffer perceptual deficits in, eg, perceptual organization (alongside hallucinations and delusions). Is there a unifying principle explaining inter-individual variability in perception? There is good reason to believe perceptual experience results from inferential processes whereby sensory evidence is weighted by prior knowledge about the world. Perceptual variability may result from different precision weighting of sensory evidence and prior knowledge. We tested this hypothesis by comparing visibility thresholds in a perceptual hysteresis task across medicated schizophrenia patients (N = 20), synesthetes (N = 20), and controls (N = 26). Participants rated the subjective visibility of stimuli embedded in noise while we parametrically manipulated the availability of sensory evidence. Additionally, precise long-term priors in synesthetes were leveraged by presenting either synesthesia-inducing or neutral stimuli. Schizophrenia patients showed increased visibility thresholds, consistent with overreliance on sensory evidence. In contrast, synesthetes exhibited lowered thresholds exclusively for synesthesia-inducing stimuli suggesting high-precision long-term priors. Additionally, in both synesthetes and schizophrenia patients explicit, short-term priors—introduced during the hysteresis experiment—lowered thresholds but did not normalize perception. Our results imply that perceptual variability might result from differences in the precision afforded to prior beliefs and sensory evidence, respectively.

[1]  Caspar M. Schwiedrzik,et al.  Expectations Change the Signatures and Timing of Electrophysiological Correlates of Perceptual Awareness , 2011, The Journal of Neuroscience.

[2]  W. A. Phillips,et al.  Evidence for impaired visual context processing in schizotypy with thought disorder , 2004, Schizophrenia Research.

[3]  Johannes Jacobus Fahrenfort,et al.  NMDA Receptor Antagonist Ketamine Distorts Object Recognition by Reducing Feedback to Early Visual Cortex. , 2016, Cerebral cortex.

[4]  Vincent Walsh,et al.  Enhanced sensory perception in synaesthesia , 2009, Experimental Brain Research.

[5]  S. Silverstein,et al.  Measures of Retinal Structure and Function as Biomarkers in Neurology and Psychiatry , 2020, Biomarkers in Neuropsychiatry.

[6]  P. Uhlhaas,et al.  Perceptual organization in schizophrenia spectrum disorders: empirical research and theoretical implications. , 2005, Psychological bulletin.

[7]  P. Hagoort,et al.  Behavioral/systems/cognitive Effective Connectivity Determines the Nature of Subjective Experience in Grapheme-color Synesthesia , 2022 .

[8]  Julian E. Asher,et al.  Is synaesthesia more common in autism? , 2013, Molecular Autism.

[9]  Victor A. F. Lamme,et al.  Confuse Your Illusion , 2013, Psychological science.

[10]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[11]  Thomas V Papathomas,et al.  Reduced depth inversion illusions in schizophrenia are state-specific and occur for multiple object types and viewing conditions. , 2013, Journal of abnormal psychology.

[12]  T. M. van Leeuwen Constructing priors in synesthesia , 2014, Cognitive neuroscience.

[13]  J. Wagemans,et al.  Perceptual Organization in Individuals With Autism Spectrum Disorder , 2018 .

[14]  Christoph Teufel,et al.  Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals , 2015, Proceedings of the National Academy of Sciences.

[15]  John H Krystal,et al.  Functional hierarchy underlies preferential connectivity disturbances in schizophrenia , 2015, Proceedings of the National Academy of Sciences.

[16]  W. PEDDIE,et al.  Helmholtz's Treatise on Physiological Optics , 1926, Nature.

[17]  P. Fletcher,et al.  Glutamatergic Model Psychoses: Prediction Error, Learning, and Inference , 2011, Neuropsychopharmacology.

[18]  J. Ward,et al.  Investigating genetic links between grapheme–colour synaesthesia and neuropsychiatric traits , 2019, Philosophical Transactions of the Royal Society B.

[19]  Increased positive and disorganised schizotypy in synaesthetes who experience colour from letters and tones , 2012, Cortex.

[20]  Karl J. Friston,et al.  The Neural Structures Expressing Perceptual Hysteresis in Visual Letter Recognition , 2002, Neuron.

[21]  M. Overgaard,et al.  Is conscious perception gradual or dichotomous? A comparison of report methodologies during a visual task , 2006, Consciousness and Cognition.

[22]  S. Silverstein,et al.  Computational Modeling of Contrast Sensitivity and Orientation Tuning in First-Episode and Chronic Schizophrenia , 2017, Computational Psychiatry.

[23]  Karl J. Friston,et al.  Computational Phenotyping in Psychiatry: A Worked Example , 2016, eNeuro.

[24]  Melloni Lucia Being a Grapheme-Color-Synesthete Makes a Difference – Perceiving Synesthetic Color Alters the Processing of Visual Stimuli. , 2010 .

[25]  T. Palomo,et al.  Cognition and the five-factor model of the Positive and Negative Syndrome Scale in schizophrenia , 2013, Schizophrenia Research.

[26]  J G Snodgrass,et al.  Impaired sensory processing as a basis for object-recognition deficits in schizophrenia. , 2001, The American journal of psychiatry.

[27]  Wenjun Gao,et al.  NMDA hypofunction as a convergence point for progression and symptoms of schizophrenia , 2013, Front. Cell. Neurosci..

[28]  J. Wagemans,et al.  Precise minds in uncertain worlds: predictive coding in autism. , 2014, Psychological review.

[29]  John J. Foxe,et al.  Differences in early sensory-perceptual processing in synesthesia: A visual evoked potential study , 2008, NeuroImage.

[30]  T. Bachmann,et al.  Individual differences in the effects of priors on perception: A multi-paradigm approach , 2019, Cognition.

[31]  Anil K. Seth,et al.  Diagnosing synaesthesia with online colour pickers: Maximising sensitivity and specificity , 2013, Journal of Neuroscience Methods.

[32]  Victor A F Lamme,et al.  Two critical periods in early visual cortex during figure–ground segregation , 2012, Brain and behavior.

[33]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[34]  D. Eagleman,et al.  A standardized test battery for the study of synesthesia , 2007, Journal of Neuroscience Methods.

[35]  Caspar M. Schwiedrzik,et al.  Expecting to See a Letter: Alpha Oscillations as Carriers of Top-Down Sensory Predictions. , 2016, Cerebral cortex.

[36]  T. M. van Leeuwen,et al.  Autistic traits in synaesthesia: atypical sensory sensitivity and enhanced perception of details , 2019, Philosophical Transactions of the Royal Society B.

[37]  S. Dakin,et al.  Visual Perception and Its Impairment in Schizophrenia , 2008, Biological Psychiatry.

[38]  D. Burr,et al.  When the world becomes ‘too real’: a Bayesian explanation of autistic perception , 2012, Trends in Cognitive Sciences.

[39]  Johan Kwisthout,et al.  Perception is in the Details: A Predictive Coding Account of the Psychedelic Phenomenon , 2017, CogSci.

[40]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  Caspar M. Schwiedrzik,et al.  Subjective and objective learning effects dissociate in space and in time , 2011, Proceedings of the National Academy of Sciences.

[42]  Karl J. Friston,et al.  Predictive Coding or Evidence Accumulation? False Inference and Neuronal Fluctuations , 2010, PloS one.

[43]  Daniel Smilek,et al.  Not all synaesthetes are created equal: Projector versus associator synaesthetes , 2004, Cognitive, affective & behavioral neuroscience.

[44]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

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

[46]  Karl J. Friston Precision Psychiatry. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[47]  J. P. Southall Helmholtz's Treatise on Physiological Optics, Translated from the Third German Edition. Vol. I , 1925 .

[48]  Heinrich Lanfermann,et al.  Understanding why patients with schizophrenia do not perceive the hollow-mask illusion using dynamic causal modelling , 2009, NeuroImage.

[49]  Romke Rouw,et al.  Brain areas involved in synaesthesia: a review. , 2011, Journal of neuropsychology.

[50]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[51]  F. Ferri,et al.  A Neural “Tuning Curve” for Multisensory Experience and Cognitive-Perceptual Schizotypy , 2017, Schizophrenia bulletin.

[52]  Albert R. Powers,et al.  Hallucinations and Strong Priors , 2019, Trends in Cognitive Sciences.

[53]  A. Seth A predictive processing theory of sensorimotor contingencies: Explaining the puzzle of perceptual presence and its absence in synesthesia , 2014, Cognitive neuroscience.

[54]  W. Dillo,et al.  Is synesthesia more common in patients with Asperger syndrome? , 2013, Front. Hum. Neurosci..

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

[56]  F. D. Lange,et al.  How Do Expectations Shape Perception? , 2018, Trends in Cognitive Sciences.

[57]  Peter Hagoort,et al.  Synaesthetic Colour in the Brain: Beyond Colour Areas. A Functional Magnetic Resonance Imaging Study of Synaesthetes and Matched Controls , 2010, PloS one.

[58]  P. Stoerig,et al.  Modality and variability of synesthetic experience. , 2012, The American journal of psychology.

[59]  Karl J. Friston,et al.  Human Neuroscience Hypothesis and Theory Article an Aberrant Precision Account of Autism , 2022 .

[60]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[61]  V. van de Ven,et al.  Reduced intrinsic visual cortical connectivity is associated with impaired perceptual closure in schizophrenia , 2017, NeuroImage: Clinical.

[62]  Raymond J. Dolan,et al.  Dopamine, Affordance and Active Inference , 2012, PLoS Comput. Biol..

[63]  J. Simner Defining synaesthesia. , 2012, British journal of psychology.

[64]  Philip D. Harvey,et al.  The Brief Assessment of Cognition in Schizophrenia: reliability, sensitivity, and comparison with a standard neurocognitive battery , 2004, Schizophrenia Research.

[65]  Casimir J. H. Ludwig,et al.  A novel, illustrated questionnaire to distinguish projector and associator synaesthetes , 2009, Cortex.

[66]  G. Kanizsa Subjective contours. , 1976, Scientific American.

[67]  Lars Muckli,et al.  The Predictive Coding Account of Psychosis , 2018, Biological Psychiatry.

[68]  J. Ward,et al.  An autistic-like profile of attention and perception in synaesthesia , 2017, Cortex.

[69]  C. Alvarado,et al.  A Survey Exploring Synesthetic Experiences: Exceptional Experiences, Schizotypy, and Psychological Well-Being , 2019, Psychology of Consciousness: Theory, Research, and Practice.

[70]  H. Scholte,et al.  Increased structural connectivity in grapheme-color synesthesia , 2007, Nature Neuroscience.

[71]  D. Dima,et al.  Understanding why patients with schizophrenia do not perceive the hollow mask illusion using dynamic causal modelling. , 2009, NeuroImage.