Perceptual Relearning of Complex Visual Motion after V1 Damage in Humans

Damage to the adult, primary visual cortex (V1) causes severe visual impairment that was previously thought to be permanent, yet several visual pathways survive V1 damage, mediating residual, often unconscious functions known as “blindsight.” Because some of these pathways normally mediate complex visual motion perception, we asked whether specific training in the blind field could improve not just simple but also complex visual motion discriminations in humans with long-standing V1 damage. Global direction discrimination training was administered to the blind field of five adults with unilateral cortical blindness. Training returned direction integration thresholds to normal at the trained locations. Although retinotopically localized to trained locations, training effects transferred to multiple stimulus and task conditions, improving the detection of luminance increments, contrast sensitivity for drifting gratings, and the extraction of motion signal from noise. Thus, perceptual relearning of complex visual motion processing is possible without an intact V1 but only when specific training is administered in the blind field. These findings indicate a much greater capacity for adult visual plasticity after V1 damage than previously thought. Most likely, basic mechanisms of visual learning must operate quite effectively in extrastriate visual cortex, providing new hope and direction for the development of principled rehabilitation strategies to treat visual deficits resulting from permanent visual cortical damage.

[1]  P. Bach-y-Rita Controlling variables eliminates hemianopsia rehabilitation results , 1983, Behavioral and Brain Sciences.

[2]  K. And,et al.  Patterns of Recovery from Homonymous Hemianopia Subsequent to Infarction in the Distribution of the Posterior Cerebral Artery , 1991 .

[3]  L. Weiskrantz,et al.  Spatial and temporal response properties of residual vision in a case of hemianopia. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  A. Cowey,et al.  Motion discrimination in cortically blind patients. , 2001, Brain : a journal of neurology.

[5]  L. Weiskrantz,et al.  Parameters affecting conscious versus unconscious visual discrimination with damage to the visual cortex (V1). , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  T. Elbert,et al.  New treatments in neurorehabiliation founded on basic research , 2002, Nature Reviews Neuroscience.

[7]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Richard O. Duda,et al.  Pattern classification and scene analysis , 1974, A Wiley-Interscience publication.

[9]  G. Riddoch DISSOCIATION OF VISUAL PERCEPTIONS DUE TO OCCIPITAL INJURIES, WITH ESPECIAL REFERENCE TO APPRECIATION OF MOVEMENT , 1917 .

[10]  R. Näsänen,et al.  Temporal sensitivity in a hemianopic visual field can be improved by long-term training using flicker stimulation , 2006, Journal of Neurology Neurosurgery & Psychiatry.

[11]  U. Eysel,et al.  Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. , 1999, Cerebral cortex.

[12]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[13]  A. Cowey,et al.  Regional cerebral correlates of global motion perception: evidence from unilateral cerebral brain damage. , 2001, Brain : a journal of neurology.

[14]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  L M Vaina,et al.  Functional segregation of color and motion processing in the human visual cortex: clinical evidence. , 1994, Cerebral cortex.

[16]  L. Weiskrantz,et al.  Increased sensitivity after repeated stimulation of residual spatial channels in blindsight , 2006, Proceedings of the National Academy of Sciences.

[17]  S K Mannan,et al.  Scanning the visual world: a study of patients with homonymous hemianopia , 2000, Journal of neurology, neurosurgery, and psychiatry.

[18]  C. Gilbert,et al.  Perceptual learning of spatial localization: specificity for orientation, position, and context. , 1997, Journal of neurophysiology.

[19]  T. Pasternak,et al.  Training-induced recovery of visual motion perception after extrastriate cortical damage in the adult cat. , 2004, Cerebral cortex.

[20]  J Zihl,et al.  Visual field rehabilitation in the cortically blind? , 1986, Journal of neurology, neurosurgery, and psychiatry.

[21]  J. Zihl,et al.  Recovery of visual functions in patients with cerebral blindness , 1981, Experimental Brain Research.

[22]  S. Zeki,et al.  The Riddoch syndrome: insights into the neurobiology of conscious vision. , 1998, Brain : a journal of neurology.

[23]  A. Fiorentini,et al.  Perceptual learning specific for orientation and spatial frequency , 1980, Nature.

[24]  M. Cole When the left brain is not right the right brain may be left: report of personal experience of occipital hemianopia , 1999, Journal of neurology, neurosurgery, and psychiatry.

[25]  C. Furmanski,et al.  Learning Strengthens the Response of Primary Visual Cortex to Simple Patterns , 2004, Current Biology.

[26]  G. Kerkhoff,et al.  Neurovisual rehabilitation: recent developments and future directions , 2000, American journal of ophthalmology.

[27]  M. Ptito,et al.  Activation of Human Extrageniculostriate Pathways after Damage to Area V1 , 1999, NeuroImage.

[28]  Z Liu,et al.  Perceptual learning in motion discrimination that generalizes across motion directions. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  N. Newman,et al.  Natural history of homonymous hemianopia , 2006, Neurology.

[30]  L. Vaina,et al.  Learning to ignore: psychophysics and computational modeling of fast learning of direction in noisy motion stimuli. , 1995, Brain research. Cognitive brain research.

[31]  Robert A. Jacobs,et al.  Comparing perceptual learning across tasks: A review , 2002 .

[32]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[33]  T. Pasternak,et al.  Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey. , 1999, Cerebral cortex.

[34]  Lawrence Weiskrantz,et al.  Spatial channels of visual processing in cortical blindness , 2003, The European journal of neuroscience.

[35]  K. Huxlin,et al.  A neurochemical signature of visual recovery after extrastriate cortical damage in the adult cat , 2008, The Journal of comparative neurology.

[36]  G. Holmes DISTURBANCES OF VISION BY CEREBRAL LESIONS , 1918, The British journal of ophthalmology.

[37]  Rainer Goebel,et al.  Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients , 2001, Vision Research.

[38]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[39]  C. Gilbert,et al.  Learning to see: experience and attention in primary visual cortex , 2001, Nature Neuroscience.

[40]  Alan Cowey,et al.  The neurobiology of blindsight , 1991, Trends in Neurosciences.

[41]  S. Hochstein,et al.  Task difficulty and the specificity of perceptual learning , 1997, Nature.

[42]  H. Pashler,et al.  Improvement in line orientation discrimination is retinally local but dependent on cognitive set , 1992, Perception & psychophysics.

[43]  J. Zihl,et al.  Cerebral Akinetopsia (Visual motion blindness). , 1999 .

[44]  Hiroshi Tsukagoshi,et al.  Eye-fixation patterns in homonymous hemianopia and unilateral spatial neglect , 1987, Neuropsychologia.

[45]  Z L Lu,et al.  Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[46]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[47]  P. Maquet,et al.  Neural correlates of perceptual learning: A functional MRI study of visual texture discrimination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  G. Pourtois,et al.  Effects of perceptual learning on primary visual cortex activity in humans , 2008, Vision Research.

[49]  Ning Qian,et al.  Learning motion discrimination with suppressed MT , 2004, Vision Research.

[50]  S. Zeki,et al.  Cerebral akinetopsia (visual motion blindness). A review. , 1991, Brain : a journal of neurology.

[51]  Zili Liu,et al.  Learning motion discrimination with suppressed and un-suppressed MT , 2006, Vision Research.

[52]  Bernhard A. Sabel,et al.  Computer-based training for the treatment of partial blindness , 1998, Nature Medicine.

[53]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[54]  R. Shillcock,et al.  Patients with hemianopic alexia adopt an inefficient eye movement strategy when reading text. , 2006, Brain : a journal of neurology.

[55]  E. Kasten,et al.  Does visual restitution training change absolute homonymous visual field defects? A fundus controlled study , 2004, British Journal of Ophthalmology.

[56]  M A Goodale,et al.  Visuomotor control: Where does vision end and action begin? , 1998, Current Biology.

[57]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[58]  O Braddick,et al.  Orientation-Specific Learning in Stereopsis , 1973, Perception.

[59]  R. Sekuler,et al.  Direction-specific improvement in motion discrimination , 1987, Vision Research.

[60]  R. Mcdonald,et al.  Hemianopic visual field loss as the first clinical evidence of occipital arteriovenous malformation , 2004, Clinical and experimental optometry.

[61]  Robert Stickgold,et al.  Cerebral Cortex doi:10.1093/cercor/bhi043 The Functional Anatomy of Sleep-dependent Visual Skill Learning , 2005 .

[62]  G. Orban,et al.  Reorganization in the visual cortex after retinal and cortical damage. , 1999, Restorative neurology and neuroscience.

[63]  Paul Azzopardi,et al.  Blindsight and Visual Awareness , 1998, Consciousness and Cognition.

[64]  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.

[65]  G. Orban,et al.  Practising orientation identification improves orientation coding in V1 neurons , 2001, Nature.

[66]  R. Sekuler,et al.  A specific and enduring improvement in visual motion discrimination. , 1982, Science.

[67]  C. Kennard,et al.  Can visual function be restored in patients with homonymous hemianopia? , 1997, The British journal of ophthalmology.

[68]  Mark Hallett,et al.  Plasticity of the human motor cortex and recovery from stroke , 2001, Brain Research Reviews.