Feature-specific prediction errors for visual mismatch

Predictive coding (PC) theory posits that our brain employs a predictive model of the environment to infer the causes of its sensory inputs. A fundamental but untested prediction of this theory is that the same stimulus should elicit distinct precision weighted prediction errors (pwPEs) when different (feature-specific) predictions are violated, even in the absence of attention. Here, we tested this hypothesis using functional magnetic resonance imaging (fMRI) and a multi-feature roving visual mismatch paradigm where rare changes in either color (red, green), or emotional expression (happy, fearful) of faces elicited pwPE responses in human participants. Using a computational model of learning and inference, we simulated pwPE and prediction trajectories of a Bayes-optimal observer and used these to analyze changes in blood oxygen level dependent (BOLD) responses to changes in color and emotional expression of faces while participants engaged in a distractor task. Controlling for visual attention by eye-tracking, we found pwPE responses to unexpected color changes in the fusiform gyrus. Conversely, unexpected changes of facial emotions elicited pwPE responses in cortico-thalamo-cerebellar structures associated with emotion and theory of mind processing. Predictions pertaining to emotions activated fusiform, occipital and temporal areas. Our results are consistent with a general role of PC across perception, from low-level to complex and socially relevant object features, and suggest that monitoring of the social environment occurs continuously and automatically, even in the absence of attention.

[1]  Jakob Heinzle,et al.  Timing of repetition suppression of event‐related potentials to unattended objects , 2018, The European journal of neuroscience.

[2]  Tomaso Poggio,et al.  Models of object recognition , 2000, Nature Neuroscience.

[3]  Ana Susac,et al.  Neurodynamic Studies on Emotional and Inverted Faces in an Oddball Paradigm , 2003, Brain Topography.

[4]  G. Stefanics,et al.  Visual Mismatch Negativity Reveals Automatic Detection of Sequential Regularity Violation , 2011, Front. Hum. Neurosci..

[5]  John L. Barbur,et al.  Colour constancy and conscious perception of changes of illuminant , 2008, Neuropsychologia.

[6]  Jakob Heinzle,et al.  Visual Mismatch and Predictive Coding: A Computational Single-Trial ERP Study , 2018, The Journal of Neuroscience.

[7]  C. Frith Role of facial expressions in social interactions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  Naotsugu Tsuchiya,et al.  Neural markers of predictive coding under perceptual uncertainty revealed with Hierarchical Frequency Tagging , 2017, eLife.

[9]  Karl J. Friston,et al.  Attention, Uncertainty, and Free-Energy , 2010, Front. Hum. Neurosci..

[10]  Karl J. Friston,et al.  Not All Predictions Are Equal: “What” and “When” Predictions Modulate Activity in Auditory Cortex through Different Mechanisms , 2018, The Journal of Neuroscience.

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

[12]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[13]  Andrea Bergmann,et al.  Statistical Parametric Mapping The Analysis Of Functional Brain Images , 2016 .

[14]  Risto Näätänen,et al.  vMMN for schematic faces: automatic detection of change in emotional expression , 2013, Front. Hum. Neurosci..

[15]  D H HUBEL,et al.  RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT. , 1965, Journal of neurophysiology.

[16]  Jordi Costa-Faidella,et al.  Interactions between “What” and “When” in the Auditory System: Temporal Predictability Enhances Repetition Suppression , 2011, The Journal of Neuroscience.

[17]  C. Keysers,et al.  Evidence for mirror systems in emotions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  G. Stefanics,et al.  Visual mismatch negativity: a predictive coding view , 2014, Front. Hum. Neurosci..

[19]  Caspar M. Schwiedrzik,et al.  High-Level Prediction Signals in a Low-Level Area of the Macaque Face-Processing Hierarchy , 2017, Neuron.

[20]  A. J. Fridlund Human Facial Expression: An Evolutionary View , 1994 .

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

[22]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[23]  Norbert Kathmann,et al.  Modeling subjective relevance in schizophrenia and its relation to aberrant salience , 2018, PLoS Comput. Biol..

[24]  Gábor Csukly,et al.  Elementary sensory deficits in schizophrenia indexed by impaired visual mismatch negativity , 2015, Schizophrenia Research.

[25]  Karl J. Friston,et al.  Task relevance modulates the behavioural and neural effects of sensory predictions , 2017, PLoS biology.

[26]  Karl J. Friston,et al.  The Anatomy of Inference: Generative Models and Brain Structure , 2018, Front. Comput. Neurosci..

[27]  C. Summerfield,et al.  Visual Prediction Error Spreads Across Object Features in Human Visual Cortex , 2016, The Journal of Neuroscience.

[28]  C. Mathys,et al.  Hierarchical Prediction Errors in Midbrain and Basal Forebrain during Sensory Learning , 2013, Neuron.

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

[30]  C. Summerfield,et al.  Expectation in perceptual decision making: neural and computational mechanisms , 2014, Nature Reviews Neuroscience.

[31]  Rafal Bogacz,et al.  A tutorial on the free-energy framework for modelling perception and learning , 2017, Journal of mathematical psychology.

[32]  Wenbo Luo,et al.  Automatic Processing of Changes in Facial Emotions in Dysphoria: A Magnetoencephalography Study , 2018, Frontiers in Human Neuroscience.

[33]  Christopher Summerfield,et al.  Dissociable prior influences of signal probability and relevance on visual contrast sensitivity , 2011 .

[34]  Piia Astikainen,et al.  This Reprint May Differ from the Original in Pagination and Typographic Detail. Event-related Potentials to Task-irrelevant Changes in Facial Expressions Behavioral and Brain Functions Event-related Potentials to Task-irrelevant Changes in Facial Expressions , 2022 .

[35]  Karl J. Friston,et al.  Cortical Coupling Reflects Bayesian Belief Updating in the Deployment of Spatial Attention , 2015, The Journal of Neuroscience.

[36]  Tobias U. Hauser,et al.  The PhysIO Toolbox for Modeling Physiological Noise in fMRI Data , 2017, Journal of Neuroscience Methods.

[37]  Karl J. Friston,et al.  Analysis of family‐wise error rates in statistical parametric mapping using random field theory , 2016, Human brain mapping.

[38]  Christopher K. Kovach,et al.  Neural signatures of perceptual inference , 2016, eLife.

[39]  Byron Nakos,et al.  EyeMMV toolbox: An eye movement post-analysis tool based on a two-step spatial dispersion threshold for fixation identification , 2014 .

[40]  U. Ernst,et al.  Perceptual Inference Predicts Contextual Modulations of Sensory Responses , 2012, The Journal of Neuroscience.

[41]  Geraint Rees,et al.  Corrigendum : Adults with autism overestimate the volatility of the sensory environment , .

[42]  J. Desmond,et al.  A meta‐analysis of cerebellar contributions to higher cognition from PET and fMRI studies , 2014, Human brain mapping.

[43]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[44]  Jim M. Monti,et al.  Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream , 2010, The Journal of Neuroscience.

[45]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[46]  Karl J. Friston,et al.  Uncertainty in perception and the Hierarchical Gaussian Filter , 2014, Front. Hum. Neurosci..

[47]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[48]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[49]  Tapani Ristaniemi,et al.  Event-related potentials to unattended changes in facial expressions : detection of regularity violations or encoding of emotions ? , 2013 .

[50]  S. Dehaene,et al.  Evidence for a hierarchy of predictions and prediction errors in human cortex , 2011, Proceedings of the National Academy of Sciences.

[51]  Risto Näätänen,et al.  Unattended and attended visual change detection of motion as indexed by event-related potentials and its behavioral correlates , 2013, Front. Hum. Neurosci..

[52]  G. Stefanics,et al.  Visual mismatch negativity (vMMN): A review and meta-analysis of studies in psychiatric and neurological disorders , 2016, Cortex.

[53]  P. Lennie,et al.  The machinery of colour vision , 2007, Nature Reviews Neuroscience.

[54]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[55]  Karl J. Friston,et al.  Repetition suppression and its contextual determinants in predictive coding , 2016, Cortex.

[56]  Anjali Krishnan,et al.  Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations , 2014, NeuroImage.

[57]  D. Heeger,et al.  Decoding and Reconstructing Color from Responses in Human Visual Cortex , 2009, The Journal of Neuroscience.

[58]  Skyler T. Hawk,et al.  Presentation and validation of the Radboud Faces Database , 2010 .

[59]  Karl J. Friston The free-energy principle: a rough guide to the brain? , 2009, Trends in Cognitive Sciences.

[60]  Bevil R. Conway,et al.  Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques , 2016, The Journal of Neuroscience.

[61]  R. Rescorla A theory of pavlovian conditioning: The effectiveness of reinforcement and non-reinforcement , 1972 .

[62]  Karl J. Friston,et al.  Modelling Trial-by-Trial Changes in the Mismatch Negativity , 2013, PLoS Comput. Biol..

[63]  Erich Schröger,et al.  Object-related regularities are processed automatically: evidence from the visual mismatch negativity , 2013, Front. Hum. Neurosci..

[64]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[65]  J. Perner,et al.  Neuroscience and Biobehavioral Reviews Fractionating Theory of Mind: a Meta-analysis of Functional Brain Imaging Studies , 2022 .

[66]  F. D’Agata,et al.  Consensus Paper: Cerebellum and Emotion , 2016, The Cerebellum.

[67]  Lun Zhao,et al.  Visual mismatch negativity elicited by facial expressions: new evidence from the equiprobable paradigm , 2012, Behavioral and Brain Functions.

[68]  G Stefanics,et al.  Automatic Detection of Trustworthiness of the Face: A Visual Mismatch Negativity Study , 2014, Acta biologica Hungarica.

[69]  R. Knight,et al.  Hierarchy of prediction errors for auditory events in human temporal and frontal cortex , 2016, Proceedings of the National Academy of Sciences.

[70]  Floris P. de Lange,et al.  How Prediction Errors Shape Perception, Attention, and Motivation , 2012, Front. Psychology.

[71]  Tai Sing Lee,et al.  Hierarchical Bayesian inference in the visual cortex. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[72]  Erich Schröger,et al.  Unintentional temporal context-based prediction of emotional faces: an electrophysiological study. , 2012, Cerebral cortex.

[73]  A. Clark Surfing Uncertainty: Prediction, Action, and the Embodied Mind , 2015 .

[74]  S. Solomon,et al.  Moving Sensory Adaptation beyond Suppressive Effects in Single Neurons , 2014, Current Biology.

[75]  Karl J. Friston,et al.  Attentional Enhancement of Auditory Mismatch Responses: a DCM/MEG Study , 2015, Cerebral cortex.

[76]  István Czigler,et al.  Mismatch negativity and neural adaptation: Two sides of the same coin. Response: Commentary: Visual mismatch negativity: a predictive coding view , 2016, Front. Hum. Neurosci..

[77]  P. Czobor,et al.  Emotion-Related Visual Mismatch Responses in Schizophrenia: Impairments and Correlations with Emotion Recognition , 2013, PloS one.

[78]  Karl J. Friston,et al.  The Dopaminergic Midbrain Encodes the Expected Certainty about Desired Outcomes , 2014, Cerebral cortex.

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

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

[81]  Mareike Grotheer,et al.  The relationship between stimulus repetitions and fulfilled expectations , 2015, Neuropsychologia.

[82]  Fraser W. Smith,et al.  Nonstimulated early visual areas carry information about surrounding context , 2010, Proceedings of the National Academy of Sciences.

[83]  Janneke F. M. Jehee,et al.  Attention Reverses the Effect of Prediction in Silencing Sensory Signals , 2011, Cerebral cortex.

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

[85]  C. Summerfield,et al.  Attention Sharpens the Distinction between Expected and Unexpected Percepts in the Visual Brain , 2013, The Journal of Neuroscience.

[86]  Lilian A. E. Weber,et al.  Hierarchical prediction errors in midbrain and septum during social learning , 2017, Social cognitive and affective neuroscience.

[87]  Kazuo Okanoya,et al.  Event-Related Potentials Elicited by Pre-Attentive Emotional Changes in Temporal Context , 2013, PloS one.

[88]  Erich Schröger,et al.  Visual Object Representations Can Be Formed outside the Focus of Voluntary Attention: Evidence from Event-related Brain Potentials , 2010, Journal of Cognitive Neuroscience.

[89]  D. Vernon,et al.  Event-Related Brain Potential Correlates of Human Auditory Sensory Memory-Trace Formation , 2005, The Journal of Neuroscience.

[90]  Benedikt V Ehinger,et al.  Humans treat unreliable filled-in percepts as more real than veridical ones , 2017, bioRxiv.

[91]  Karl J. Friston,et al.  Free Energy, Precision and Learning: The Role of Cholinergic Neuromodulation , 2013, The Journal of Neuroscience.

[92]  István Czigler,et al.  Processing of unattended facial emotions: A visual mismatch negativity study , 2012, NeuroImage.

[93]  Alex R. Wade,et al.  Visual field maps and stimulus selectivity in human ventral occipital cortex , 2005, Nature Neuroscience.

[94]  Greg O. Horne,et al.  Controlling low-level image properties: The SHINE toolbox , 2010, Behavior research methods.

[95]  Gary Napier,et al.  Attractor-like Dynamics in Belief Updating in Schizophrenia , 2018, The Journal of Neuroscience.