A predictive coding account of bistable perception - a model-based fMRI study

In bistable vision, subjective perception wavers between two interpretations of a constant ambiguous stimulus. This dissociation between conscious perception and sensory stimulation has motivated various empirical studies on the neural correlates of bistable perception, but the neurocomputational mechanism behind endogenous perceptual transitions has remained elusive. Here, we recurred to a generic Bayesian framework of predictive coding and devised a model that casts endogenous perceptual transitions as a consequence of prediction errors emerging from residual evidence for the suppressed percept. Data simulations revealed close similarities between the model’s predictions and key temporal characteristics of perceptual bistability, indicating that the model was able to reproduce bistable perception. Fitting the predictive coding model to behavioural data from an fMRI-experiment on bistable perception, we found a correlation across participants between the model parameter encoding perceptual stabilization and the behaviourally measured frequency of perceptual transitions, corroborating that the model successfully accounted for participants’ perception. Formal model comparison with established models of bistable perception based on mutual inhibition and adaptation, noise or a combination of adaptation and noise was used for the validation of the predictive coding model against the established models. Most importantly, model-based analyses of the fMRI data revealed that prediction error time-courses derived from the predictive coding model correlated with neural signal time-courses in bilateral inferior frontal gyri and anterior insulae. Voxel-wise model selection indicated a superiority of the predictive coding model over conventional analysis approaches in explaining neural activity in these frontal areas, suggesting that frontal cortex encodes prediction errors that mediate endogenous perceptual transitions in bistable perception. Taken together, our current work provides a theoretical framework that allows for the analysis of behavioural and neural data using a predictive coding perspective on bistable perception. In this, our approach posits a crucial role of prediction error signalling for the resolution of perceptual ambiguities.

[1]  Alexander Pastukhov,et al.  Believable change: bistable reversals are governed by physical plausibility. , 2012, Journal of vision.

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

[3]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[4]  N. Logothetis,et al.  A Common Neurodynamical Mechanism Could Mediate Externally Induced and Intrinsically Generated Transitions in Visual Awareness , 2013, PloS one.

[5]  David A. Leopold,et al.  What is rivalling during binocular rivalry? , 1996, Nature.

[6]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[7]  Aaron Schurger A very inexpensive MRI-compatible method for dichoptic visual stimulation , 2009, Journal of Neuroscience Methods.

[8]  G. Hesselmann,et al.  Revisiting the Lissajous figure as a tool to study bistable perception , 2014, Vision Research.

[9]  R. van Ee,et al.  Early interactions between neuronal adaptation and voluntary control determine perceptual choices in bistable vision. , 2008, Journal of vision.

[10]  J. Hohwy Attention and Conscious Perception in the Hypothesis Testing Brain , 2012, Front. Psychology.

[11]  G. Rees,et al.  The Neural Bases of Multistable Perception , 2022 .

[12]  Hugh R. Wilson,et al.  Minimal physiological conditions for binocular rivalry , 2010 .

[13]  Philipp Sterzer,et al.  Frontoparietal Cortex Mediates Perceptual Transitions in Bistable Perception , 2013, The Journal of Neuroscience.

[14]  R. Blake,et al.  Neural bases of binocular rivalry , 2006, Trends in Cognitive Sciences.

[15]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[16]  S. R. Lehky An Astable Multivibrator Model of Binocular Rivalry , 1988, Perception.

[17]  W J Levelt,et al.  Note on the distribution of dominance times in binocular rivalry. , 1967, British journal of psychology.

[18]  D. Knill,et al.  The Bayesian brain: the role of uncertainty in neural coding and computation , 2004, Trends in Neurosciences.

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

[20]  William D. Penny,et al.  Bayesian model selection maps for group studies , 2009, NeuroImage.

[21]  R. Blake,et al.  Negligible fronto-parietal BOLD activity accompanying unreportable switches in bistable perception , 2015, Nature Neuroscience.

[22]  N. Logothetis,et al.  Multistable phenomena: changing views in perception , 1999, Trends in Cognitive Sciences.

[23]  Joel Pearson,et al.  Sensory memory for ambiguous vision , 2008, Trends in Cognitive Sciences.

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

[25]  W. Einhäuser,et al.  Binocular Rivalry: Frontal Activity Relates to Introspection and Action But Not to Perception , 2014, The Journal of Neuroscience.

[26]  Richard H. A. H. Jacobs,et al.  The time course of binocular rivalry reveals a fundamental role of noise. , 2006, Journal of vision.

[27]  Karl J. Friston,et al.  Bayesian model selection for group studies (vol 46, pg 1005, 2009) , 2009 .

[28]  Philipp Sterzer,et al.  Perceptual Stability of the Lissajous Figure Is Modulated by the Speed of Illusory Rotation , 2016, PloS one.

[29]  J. Rinzel,et al.  Noise-induced alternations in an attractor network model of perceptual bistability. , 2007, Journal of neurophysiology.

[30]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[31]  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.

[32]  R. Sundareswara,et al.  Perceptual multistability predicted by search model for Bayesian decisions. , 2008, Journal of vision.

[33]  Philipp Sterzer,et al.  A neural basis for inference in perceptual ambiguity , 2007, Proceedings of the National Academy of Sciences.

[34]  Floris P de Lange,et al.  Serial Dependence in Perceptual Decisions Is Reflected in Activity Patterns in Primary Visual Cortex , 2016, The Journal of Neuroscience.

[35]  Geraint Rees,et al.  Brain activity dynamics in human parietal regions during spontaneous switches in bistable perception , 2015, NeuroImage.

[36]  D. Whitney,et al.  Serial dependence in visual perception , 2011 .

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

[38]  Geraint Rees,et al.  Structural and functional fractionation of right superior parietal cortex in bistable perception , 2011, Current Biology.

[39]  G. Rees,et al.  Neural correlates of perceptual rivalry in the human brain. , 1998, Science.

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

[41]  Karl J. Friston,et al.  Predictive coding explains binocular rivalry: An epistemological review , 2008, Cognition.

[42]  Hugh R Wilson,et al.  Minimal physiological conditions for binocular rivalry and rivalry memory , 2007, Vision Research.

[43]  Randolph Blake,et al.  The Role of Frontal and Parietal Brain Areas in Bistable Perception , 2011, The Journal of Neuroscience.

[44]  Karl J. Friston,et al.  Free-energy and the brain , 2007, Synthese.

[45]  J. O'Doherty,et al.  Model‐Based fMRI and Its Application to Reward Learning and Decision Making , 2007, Annals of the New York Academy of Sciences.