Report Experience-Driven Plasticity in Binocular Vision

Experience-driven neuronal plasticity allows the brain to adapt its functional connectivity to recent sensory input. Here we use binocular rivalry, an experimental paradigm in which conflicting images are presented to the individual eyes, to demonstrate plasticity in the neuronal mechanisms that convert visual information from two separated retinas into single perceptual experiences. Perception during binocular rivalry tended to initially consist of alternations between exclusive representations of monocularly defined images, but upon prolonged exposure, mixture percepts became more prevalent. The completeness of suppression, reflected in the incidence of mixture percepts, plausibly reflects the strength of inhibition that likely plays a role in binocular rivalry. Recovery of exclusivity was possible but required highly specific binocular stimulation. Documenting the prerequisites for these observed changes in perceptual exclusivity, our experiments suggest experience-driven plasticity at interocular inhibitory synapses, driven by the correlated activity (and also the lack thereof) of neurons representing the conflicting stimuli. This form of plasticity is consistent with a previously proposed but largely untested anti-Hebbian learning mechanism for inhibitory synapses in vision. Our results implicate experience-driven plasticity as one governing principle in the neuronal organization of binocular vision.

[1]  George Sperling,et al.  A gain-control theory of binocular combination. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Siu Kang,et al.  Bidirectional plasticity in fast-spiking GABA circuits by visual experience , 2009, Nature.

[3]  Frans A. J. Verstraten,et al.  Storage for free: a surprising property of a simple gain-control model of motion aftereffects , 2004, Vision Research.

[4]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[5]  H. Barlow Vision: A theory about the functional role and synaptic mechanism of visual after-effects , 1991 .

[6]  C. Clifford,et al.  When your brain decides what you see: grouping across monocular, binocular, and stimulus rivalry. , 2005, Psychological science.

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

[8]  Frans A. J. Verstraten,et al.  Recovery from motion adaptation is delayed by successively presented orthogonal motion , 1994, Vision Research.

[9]  M. Livingstone,et al.  Differences between stereopsis, interocular correlation and binocularity , 1996, Vision Research.

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

[11]  Stephen Grossberg,et al.  How does binocular rivalry emerge from cortical mechanisms of 3-D vision? , 2008, Vision Research.

[12]  Peter Földiák,et al.  Adaptation and decorrelation in the cortex , 1989 .

[13]  R. Blake,et al.  Spatial zones of binocular rivalry in central and peripheral vision , 1992, Visual Neuroscience.

[14]  D. Badcock,et al.  Implicit exploitation of regularities: Novel correlations in images quickly alter visual perception , 2006, Vision Research.

[15]  L. P. O'Keefe,et al.  Adaptation to contingencies in macaque primary visual cortex. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  J A Movshon,et al.  Storage of Spatially Specific Threshold Elevation , 1978, Perception.

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

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

[19]  W. Levelt On binocular rivalry , 1965 .

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

[21]  Richard Durbin,et al.  The computing neuron , 1989 .

[22]  Raymond van Ee,et al.  Distributions of alternation rates in various forms of bistable perception. , 2005, Journal of vision.

[23]  E. Reece,et al.  The Once and Future , 2009 .

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

[25]  Robert P. O'Shea,et al.  The effect of spatial frequency and field size on the spread of exclusive visibility in binocular rivalry , 1997, Vision Research.

[26]  Y Yang,et al.  On the Variety of Percepts Associated with Dichoptic Viewing of Dissimilar Monocular Stimuli , 1992, Perception.

[27]  S. Nelson Hebb and anti-Hebb meet in the brainstem , 2004, Nature Neuroscience.

[28]  Colin Blakemore,et al.  Vision: Coding and Efficiency , 1991 .

[29]  L. Trussell,et al.  Cell-specific, spike timing–dependent plasticities in the dorsal cochlear nucleus , 2004, Nature Neuroscience.

[30]  P. Földiák,et al.  Forming sparse representations by local anti-Hebbian learning , 1990, Biological Cybernetics.

[31]  Raymond van Ee,et al.  Dynamics of perceptual bi-stability for stereoscopic slant rivalry and a comparison with grating, house-face, and Necker cube rivalry , 2005, Vision Research.

[32]  E. Vul,et al.  The McCollough effect reflects permanent and transient adaptation in early visual cortex. , 2008, Journal of vision.

[33]  L. C. Katz,et al.  Development of cortical circuits: Lessons from ocular dominance columns , 2002, Nature Reviews Neuroscience.

[34]  E. Debski,et al.  Fixing my gaze: A scientist’s journey into seeing in three dimensions , 2009 .

[35]  D. Purves,et al.  Similarities in normal and binocularly rivalrous viewing. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[36]  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.

[37]  Terrence J. Sejnowski,et al.  The Once and Future Hebb Synapse , 2003 .

[38]  Randolph Blake,et al.  On the coexistence of stereopsis and binocular rivalry , 1991, Vision Research.

[39]  M. Grabowecky,et al.  Long-Term Speeding in Perceptual Switches Mediated by Attention-Dependent Plasticity in Cortical Visual Processing , 2007, Neuron.

[40]  David Alais,et al.  Strength and coherence of binocular rivalry depends on shared stimulus complexity , 2007, Vision Research.

[41]  M. Hollins,et al.  The effect of contrast on the completeness of binocular rivalry suppression , 1980, Perception & psychophysics.

[42]  H. Wilson,et al.  Dynamics of travelling waves in visual perception , 2001, Nature.

[43]  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.

[44]  P. Christiaan Klink,et al.  General Validity of Levelt's Propositions Reveals Common Computational Mechanisms for Visual Rivalry , 2008, PloS one.

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

[46]  Gustavo Deco,et al.  Decorrelated Hebbian Learning for Clustering and Function Approximation , 1995, Neural Computation.

[47]  Leonard J. Press Fixing My Gaze: A Scientist’s Journey into Seeing in Three Dimensions , 2009 .

[48]  Peter Somogyi,et al.  Anti-Hebbian Long-Term Potentiation in the Hippocampal Feedback Inhibitory Circuit , 2007, Science.