A hierarchical model of perceptual multistability involving interocular grouping

Ambiguous visual images can generate dynamic and stochastic switches in perceptual interpretation known as perceptual rivalry. Such dynamics have primarily been studied in the context of rivalry between two percepts, but there is growing interest in the neural mechanisms that drive rivalry between more than two percepts. In recent experiments, we showed that split images presented to each eye lead to subjects perceiving four stochastically alternating percepts (Jacot-Guillarmod et al., 2017): two single eye images and two interocularly grouped images. Here we propose a hierarchical neural network model that exhibits dynamics consistent with our experimental observations. The model consists of two levels, with the first representing monocular activity, and the second representing activity in higher visual areas. The model produces stochastically switching solutions, whose dependence on task parameters is consistent with four generalized Levelt Propositions. Our neuromechanistic model also allowed us to probe the roles of inter-actions between populations at the network levels. Stochastic switching at the lower level representing alternations between single eye percepts dominated, consistent with experiments.

[1]  G. Rees,et al.  Predicting the Stream of Consciousness from Activity in Human Visual Cortex , 2005, Current Biology.

[2]  Andreas Bartels,et al.  Binocular rivalry: a time dependence of eye and stimulus contributions. , 2010, Journal of vision.

[3]  K. Matsuoka The dynamic model of binocular rivalry , 2004, Biological Cybernetics.

[4]  M. Hollins,et al.  Adaptation of the binocular rivalry mechanism. , 1980, Investigative ophthalmology & visual science.

[5]  Carson C. Chow,et al.  Role of mutual inhibition in binocular rivalry. , 2011, Journal of neurophysiology.

[6]  Marcia Grabowecky,et al.  Evidence for Perceptual “Trapping” and Adaptation in Multistable Binocular Rivalry , 2002, Neuron.

[7]  Mathias Bode,et al.  Lateral Neural Model of Binocular Rivalry , 2003, Neural Computation.

[8]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[9]  Hugh R Wilson,et al.  Computational evidence for a rivalry hierarchy in vision , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Sheng He,et al.  Competing Global Representations Fail to Initiate Binocular Rivalry , 2004, Neuron.

[11]  O Braddick,et al.  Coherence dependence of high-density visual evoked potentials to global form and motion displays , 2010 .

[12]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[13]  K. Mullen,et al.  How long range is contour integration in human color vision? , 2003, Visual Neuroscience.

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

[15]  N. Logothetis,et al.  Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry , 1996, Nature.

[16]  Randolph Blake,et al.  The effects of transcranial magnetic stimulation on visual rivalry. , 2007, Journal of vision.

[17]  Karen R. Dobkins,et al.  Attention effects on motion processing are larger in the left vs. the right visual field , 2010 .

[18]  W. Levelt,et al.  The ‘laws’ of binocular rivalry: 50 years of Levelt’s propositions , 2015, Vision Research.

[19]  Jonathan A. Marshall,et al.  Neural model of temporal and stochastic properties of binocular rivalry , 2000, Neurocomputing.

[20]  S. Palmer,et al.  A century of Gestalt psychology in visual perception: I. Perceptual grouping and figure-ground organization. , 2012, Psychological bulletin.

[21]  N. Logothetis,et al.  Neuronal correlates of subjective visual perception. , 1989, Science.

[22]  André J. Noest,et al.  Attentional control over either of the two competing percepts of ambiguous stimuli revealed by a two-parameter analysis: Means do not make the difference , 2006, Vision Research.

[23]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[24]  E. Lumer A neural model of binocular integration and rivalry based on the coordination of action-potential timing in primary visual cortex. , 1998, Cerebral cortex.

[25]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[26]  Nava Rubin,et al.  Alternation rate in perceptual bistability is maximal at and symmetric around equi-dominance. , 2010, Journal of vision.

[27]  Jean Bennett,et al.  Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex , 2002, Neuron.

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

[29]  Nava Rubin,et al.  Dynamical characteristics common to neuronal competition models. , 2007, Journal of neurophysiology.

[30]  N. Logothetis,et al.  Visual competition , 2002, Nature Reviews Neuroscience.

[31]  W. Köhler The task of Gestalt psychology , 1969 .

[32]  I. Kovács,et al.  When the brain changes its mind: interocular grouping during binocular rivalry. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[33]  K. Nakayama,et al.  Binocular Rivalry and Visual Awareness in Human Extrastriate Cortex , 1998, Neuron.

[34]  K. Shapiro,et al.  The contingent negative variation (CNV) event-related potential (ERP) predicts the attentional blink , 2008 .

[35]  R. van Ee,et al.  Percept-choice sequences driven by interrupted ambiguous stimuli: a low-level neural model. , 2007, Journal of vision.

[36]  Tal Makovski,et al.  The visual attractor illusion. , 2010, Journal of vision.

[37]  Martin Golubitsky,et al.  Derived Patterns in Binocular Rivalry Networks , 2013, Journal of mathematical neuroscience.

[38]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[39]  C. Clifford Binocular rivalry , 2009, Current Biology.

[40]  Dario L. Ringach,et al.  Dynamics of orientation tuning in macaque primary visual cortex , 1997, Nature.

[41]  R. Shapley,et al.  Dynamics of orientation tuning in macaque V1: the role of global and tuned suppression. , 2003, Journal of neurophysiology.

[42]  Scott L. Brincat,et al.  Dynamic Shape Synthesis in Posterior Inferotemporal Cortex , 2006, Neuron.

[43]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

[44]  Jeroen J. A. van Boxtel,et al.  Retinotopic and non-retinotopic stimulus encoding in binocular rivalry and the involvement of feedback. , 2008, Journal of vision.

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

[46]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[47]  Randolph Blake,et al.  What causes alternations in dominance during binocular rivalry? , 2010, Attention, perception & psychophysics.

[48]  Alan W Freeman,et al.  Multistage model for binocular rivalry. , 2005, Journal of neurophysiology.

[49]  Carson C. Chow,et al.  A Spiking Neuron Model for Binocular Rivalry , 2000 .

[50]  Yunjiao Wang,et al.  Reduction and Dynamics of a Generalized Rivalry Network with Two Learned Patterns , 2012, SIAM J. Appl. Dyn. Syst..

[51]  Haluk Ogmen,et al.  Extending Levelt’s Propositions to perceptual multistability involving interocular grouping , 2016 .

[52]  Timothy J Andrews,et al.  Fusion and Rivalry Are Dependent on the Perceptual Meaning of Visual Stimuli , 2004, Current Biology.

[53]  Jochen Braun,et al.  Attractors and noise: Twin drivers of decisions and multistability , 2010, NeuroImage.

[54]  R. Blake,et al.  V1 activity is reduced during binocular rivalry. , 2002, Journal of vision.

[55]  Gislin Dagnelie Visual performance under simulated conditions of prosthetic vision , 2002 .

[56]  M. Häusser,et al.  Estimating the Time Course of the Excitatory Synaptic Conductance in Neocortical Pyramidal Cells Using a Novel Voltage Jump Method , 1997, The Journal of Neuroscience.

[57]  R. Blake A neural theory of binocular rivalry. , 1989, Psychological review.

[58]  J. R. Pomerantz,et al.  A century of Gestalt psychology in visual perception: II. Conceptual and theoretical foundations. , 2012, Psychological bulletin.

[59]  Martin Golubitsky,et al.  The Symmetry of Generalized Rivalry Network Models Determines Patterns of Interocular Grouping in Four-Location Binocular Rivalry. , 2019, Journal of neurophysiology.

[60]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[61]  L. Abbott,et al.  A model of multiplicative neural responses in parietal cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Konstantinos Moutoussis,et al.  Binocular rivalry alternations and their relation to visual adaptation , 2012, Front. Hum. Neurosci..

[63]  Peter Dayan,et al.  A Hierarchical Model of Binocular Rivalry , 1998, Neural Computation.

[64]  David L. Sheinberg,et al.  The role of temporal cortical areas in perceptual organization. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[66]  A. V. van den Berg,et al.  Intermittent ambiguous stimuli: implicit memory causes periodic perceptual alternations. , 2009, Journal of vision.

[67]  Randolph Blake,et al.  Report Experience-Driven Plasticity in Binocular Vision , 2010 .

[68]  Andreas V. M. Herz,et al.  A Universal Model for Spike-Frequency Adaptation , 2003, Neural Computation.

[69]  Gustavo Deco,et al.  A model of binocular rivalry based on competition in IT , 2002, Neurocomputing.

[70]  R. Blake,et al.  Temporal perturbations of binocular rivalry , 1990, Perception & psychophysics.

[71]  Nava Rubin,et al.  The oblique plaid effect , 2004, Vision Research.

[72]  John Rinzel,et al.  Noise and adaptation in multistable perception: noise drives when to switch, adaptation determines percept choice. , 2014, Journal of vision.

[73]  D. Heeger,et al.  Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry , 2000, Nature Neuroscience.

[74]  Nava Rubin,et al.  Mechanisms for Frequency Control in Neuronal Competition Models , 2008, SIAM J. Appl. Dyn. Syst..

[75]  R. Blake © 2001 Kluwer Academic Publishers. Printed in the Netherlands. 5 A Primer on Binocular Rivalry, Including Current Controversies , 2000 .

[76]  Zachary P. Kilpatrick Short term synaptic depression improves information transfer in perceptual multistability , 2013, Front. Comput. Neurosci..

[77]  M. Lankheet,et al.  Unraveling adaptation and mutual inhibition in perceptual rivalry. , 2006, Journal of vision.

[78]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

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

[80]  K. Josić,et al.  Extending Levelt’s Propositions to perceptual multistability involving interocular grouping , 2016, Vision Research.

[81]  David J. Heeger,et al.  A Model of Binocular Rivalry and Cross-orientation Suppression , 2013, PLoS Comput. Biol..

[82]  M. Landy,et al.  The effect of viewpoint on perceived visual roughness. , 2007, Journal of vision.

[83]  R Blake,et al.  The Site of Binocular Rivalry Suppression , 1979, Perception.

[84]  P. Roelfsema Cortical algorithms for perceptual grouping. , 2006, Annual review of neuroscience.

[85]  N J Wade,et al.  Aftereffects in Binocular Rivalry , 1986, Perception.

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

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

[88]  David C. Burr,et al.  Space-time in the brain , 2010 .