Long-term effects of monocular deprivation revealed with binocular rivalry gratings modulated in luminance and in color.

During development, within a specific temporal window called the critical period, the mammalian visual cortex is highly plastic and literally shaped by visual experience; to what extent this extraordinary plasticity is retained in the adult brain is still a debated issue. We tested the residual plastic potential of the adult visual cortex for both achromatic and chromatic vision by measuring binocular rivalry in adult humans following 150 minutes of monocular patching. Paradoxically, monocular deprivation resulted in lengthening of the mean phase duration of both luminance-modulated and equiluminant stimuli for the deprived eye and complementary shortening of nondeprived phase durations, suggesting an initial homeostatic compensation for the lack of information following monocular deprivation. When equiluminant gratings were tested, the effect was measurable for at least 180 minutes after reexposure to binocular vision, compared with 90 minutes for achromatic gratings. Our results suggest that chromatic vision shows a high degree of plasticity, retaining the effect for a duration (180 minutes) longer than that of the deprivation period (150 minutes) and twice as long as that found with achromatic gratings. The results are in line with evidence showing a higher vulnerability of the P pathway to the effects of visual deprivation during development and a slower development of chromatic vision in humans.

[1]  Fang Fang,et al.  Adaptive changes in visual cortex following prolonged contrast reduction. , 2009, Journal of vision.

[2]  Pascal Mamassian,et al.  Temporal dynamics in bistable perception. , 2005, Journal of vision.

[3]  Alexander Pastukhov,et al.  A short-term memory of multi-stable perception. , 2008, Journal of vision.

[4]  S. Engel,et al.  Distinct mechanism for long-term contrast adaptation , 2012, Proceedings of the National Academy of Sciences.

[5]  R. Shapley,et al.  Color and luminance contrast as tools for probing the primate retina. , 1988, Neuroscience research. Supplement : the official journal of the Japan Neuroscience Society.

[6]  M. Concetta Morrone,et al.  Development of contrast sensitivity and acuity of the infant colour system , 1990, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  D. Maurer,et al.  Better perception of global motion after monocular than after binocular deprivation , 2002, Vision Research.

[8]  P. Lennie,et al.  Profound Contrast Adaptation Early in the Visual Pathway , 2004, Neuron.

[9]  DH Hubel,et al.  Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[11]  L. Merabet,et al.  The plastic human brain cortex. , 2005, Annual review of neuroscience.

[12]  O. Carter,et al.  Color and Luminance Influence, but Can Not Explain, Binocular Rivalry Onset Bias , 2011, PloS one.

[13]  S. McKee,et al.  Visual deficits in anisometropia , 2003, Vision Research.

[14]  Leo Maurice Hurvich,et al.  Color vision , 1981 .

[15]  D. Maurer,et al.  Development of grating acuity in children treated for unilateral or bilateral congenital cataract. , 1995, Investigative ophthalmology & visual science.

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

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

[18]  J. Horton,et al.  Timing of the Critical Period for Plasticity of Ocular Dominance Columns in Macaque Striate Cortex , 1997, The Journal of Neuroscience.

[19]  M. Meister,et al.  Fast and Slow Contrast Adaptation in Retinal Circuitry , 2002, Neuron.

[20]  Nicoletta Berardi,et al.  Critical periods during sensory development , 2000, Current Opinion in Neurobiology.

[21]  Naomi B. Pitskel,et al.  Rapid and Reversible Recruitment of Early Visual Cortex for Touch , 2008, PloS one.

[22]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[23]  Tomas Knapen,et al.  Opposite Influence of Perceptual Memory on Initial and Prolonged Perception of Sensory Ambiguity , 2012, PloS one.

[24]  W. Levelt.  The alternation process in binocular rivalry , 1966 .

[25]  Ethan M. Meyers,et al.  Visual Parsing After Recovery From Blindness , 2009, Psychological science.

[26]  Nicoletta Berardi,et al.  Reducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity , 2010, The Journal of Neuroscience.

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

[28]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[29]  L. Cohen,et al.  Mechanisms underlying rapid experience-dependent plasticity in the human visual cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P. Lennie,et al.  Chromatic Gain Controls in Visual Cortical Neurons , 2005, The Journal of Neuroscience.

[31]  A. Fairhall,et al.  Timescales of Inference in Visual Adaptation , 2009, Neuron.

[32]  Rachel N. Denison,et al.  Distinct Contributions of the Magnocellular and Parvocellular Visual Streams to Perceptual Selection , 2012, Journal of Cognitive Neuroscience.

[33]  Zijiang J. He,et al.  Effectively Reducing Sensory Eye Dominance with a Push-Pull Perceptual Learning Protocol , 2010, Current Biology.

[34]  C. McCollough.  Color Adaptation of Edge-Detectors in the Human Visual System , 1965, Science.

[35]  J. Pokorny,et al.  Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm , 1975, Vision Research.

[36]  L. Maffei,et al.  The Antidepressant Fluoxetine Restores Plasticity in the Adult Visual Cortex , 2008, Science.

[37]  J. Mollon.  Color vision. , 1982, Annual review of psychology.

[38]  F. Rösler,et al.  Speech processing activates visual cortex in congenitally blind humans , 2002, The European journal of neuroscience.

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

[40]  A. V. van den Berg,et al.  Multi-Timescale Perceptual History Resolves Visual Ambiguity , 2008, PloS one.

[41]  R. Shapley,et al.  Background light and the contrast gain of primate P and M retinal ganglion cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Hensch.  Critical period regulation. , 2004, Annual review of neuroscience.

[43]  R. Reid,et al.  Homeostatic Regulation of Eye-Specific Responses in Visual Cortex during Ocular Dominance Plasticity , 2007, Neuron.

[44]  A. Karni,et al.  Learning perceptual skills: behavioral probes into adult cortical plasticity , 1997, Current Opinion in Neurobiology.

[45]  L. Cohen,et al.  Enhanced excitability of the human visual cortex induced by short-term light deprivation. , 2000, Cerebral cortex.

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

[47]  David C. Burr,et al.  Brief periods of monocular deprivation disrupt ocular balance in human adult visual cortex , 2011, Current Biology.

[48]  Massimo Riani,et al.  Stochastic Models and Fluctuations in Reversal Time of Ambiguous Figures , 1977, Perception.

[49]  Frank Sengpiel,et al.  Neural mechanisms of recovery following early visual deprivation , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[51]  P. Cavanagh,et al.  Onset rivalry: the initial dominance phase is independent of ongoing perceptual alternations , 2011, Front. Hum. Neurosci..

[52]  Michael A Crognale,et al.  Development, maturation, and aging of chromatic visual pathways: VEP results. , 2002, Journal of vision.

[53]  Catherine J. Mondloch,et al.  Missing sights: consequences for visual cognitive development , 2005, Trends in Cognitive Sciences.

[54]  Alex R. Wade,et al.  Long-term deprivation affects visual perception and cortex , 2003, Nature Neuroscience.

[55]  J. Pettigrew,et al.  A Common Oscillator for Perceptual Rivalries? , 2003, Perception.

[56]  R. M. Boynton,et al.  Chromaticity diagram showing cone excitation by stimuli of equal luminance. , 1979, Journal of the Optical Society of America.

[57]  S. Engel,et al.  Effects of Orientation-Specific Visual Deprivation Induced with Altered Reality , 2009, Current Biology.

[58]  H. Smallman,et al.  Visual function before and after the removal of bilateral congenital cataracts in adulthood , 2002, Vision Research.

[59]  Dennis M Levi,et al.  Perceptual learning in adults with amblyopia: a reevaluation of critical periods in human vision. , 2005, Developmental psychobiology.

[60]  P. Schiller,et al.  Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. , 1978, Journal of neurophysiology.

[61]  P. Cavanagh,et al.  Onset Rivalry: Brief Presentation Isolates an Early Independent Phase of Perceptual Competition , 2007, PloS one.

[62]  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.

[63]  J M Wolfe,et al.  Fatigue and structural change: two consequences of visual pattern adaptation. , 1986, Investigative ophthalmology & visual science.

[64]  Aaron S. Andalman,et al.  Vision Following Extended Congenital Blindness , 2006, Psychological science.

[65]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[66]  D. Hubel,et al.  Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. , 1965, Journal of neurophysiology.