Visual recovery in cortical blindness is limited by high internal noise.

Damage to the primary visual cortex typically causes cortical blindness (CB) in the hemifield contralateral to the damaged hemisphere. Recent evidence indicates that visual training can partially reverse CB at trained locations. Whereas training induces near-complete recovery of coarse direction and orientation discriminations, deficits in fine motion processing remain. Here, we systematically disentangle components of the perceptual inefficiencies present in CB fields before and after coarse direction discrimination training. In seven human CB subjects, we measured threshold versus noise functions before and after coarse direction discrimination training in the blind field and at corresponding intact field locations. Threshold versus noise functions were analyzed within the framework of the linear amplifier model and the perceptual template model. Linear amplifier model analysis identified internal noise as a key factor differentiating motion processing across the tested areas, with visual training reducing internal noise in the blind field. Differences in internal noise also explained residual perceptual deficits at retrained locations. These findings were confirmed with perceptual template model analysis, which further revealed that the major residual deficits between retrained and intact field locations could be explained by differences in internal additive noise. There were no significant differences in multiplicative noise or the ability to process external noise. Together, these results highlight the critical role of altered internal noise processing in mediating training-induced visual recovery in CB fields, and may explain residual perceptual deficits relative to intact regions of the visual field.

[1]  J. Movshon,et al.  Creation of direction selectivity in adult strobe-reared cats , 1981, Nature.

[2]  Paul B Hibbard,et al.  Consciousness of the first order in blindsight , 2010, Proceedings of the National Academy of Sciences.

[3]  George J. Andersen,et al.  Aging, perceptual learning, and changes in efficiency of motion processing , 2012, Vision Research.

[4]  G. J. van der Wildt,et al.  Visual training of cerebral blindness patients gradually enlarges the visual field , 2009, British Journal of Ophthalmology.

[5]  B. Dosher,et al.  Characterizing observers using external noise and observer models: assessing internal representations with external noise. , 2008, Psychological review.

[6]  J. E. Albano,et al.  The role of directionally selective neurons in the perception of global motion , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Barbara Anne Dosher,et al.  The spatial window of the perceptual template and endogenous attention , 2004, Vision Research.

[8]  Steven C. Dakin,et al.  Local and global limitations on direction integration assessed using equivalent noise analysis , 2005, Vision Research.

[9]  Georgios A Keliris,et al.  Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects , 2014, Proceedings of the National Academy of Sciences.

[10]  Mary Hayhoe,et al.  Perceptual Relearning of Complex Visual Motion after V1 Damage in Humans , 2009, The Journal of Neuroscience.

[11]  B. Dosher,et al.  External noise distinguishes attention mechanisms , 1998, Vision Research.

[12]  Barbara Anne Dosher,et al.  Perceptual learning of motion direction discrimination in fovea: Separable mechanisms , 2006, Vision Research.

[13]  B. Dosher,et al.  PSYCHOLOGICAL SCIENCE Research Article NOISE EXCLUSION IN SPATIAL ATTENTION , 2022 .

[14]  Barbara A Dosher,et al.  Perceptual learning retunes the perceptual template in foveal orientation identification. , 2004, Journal of vision.

[15]  Luis A. Lesmes,et al.  Spatial attention excludes external noise at the target location. , 2002, Journal of vision.

[16]  K. Huxlin,et al.  Visual cortical activity reflects faster accumulation of information from cortically blind fields. , 2012, Brain : a journal of neurology.

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

[18]  J. Pettigrew,et al.  Single units in visual cortex of kittens reared in stroboscopic illumination. , 1974, Brain research.

[19]  T. Pasternak,et al.  Pattern and motion vision in cats with selective loss of cortical directional selectivity , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  B. Dosher,et al.  Characterizing human perceptual inefficiencies with equivalent internal noise. , 1999, Journal of the Optical Society of America. A, Optics, image science, and vision.

[21]  A. Cowey,et al.  Is blindsight like normal, near-threshold vision? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[22]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[23]  J. Movshon,et al.  A new perceptual illusion reveals mechanisms of sensory decoding , 2007, Nature.

[24]  Pengjing Xu,et al.  Identify mechanisms of amblyopia in Gabor orientation identification with external noise , 2006, Vision Research.

[25]  R. F. Wagner,et al.  Efficiency of human visual signal discrimination. , 1981, Science.

[26]  P. Bennett,et al.  Effects of aging on calculation efficiency and equivalent noise. , 1999, Journal of the Optical Society of America. A, Optics, image science, and vision.

[27]  B. Sabel,et al.  Visual field enlargement after computer training in brain-damaged patients with homonymous deficits: an open pilot trial. , 1995, Restorative neurology and neuroscience.

[28]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[29]  Bosco S. Tjan,et al.  Learning letter identification in peripheral vision , 2005, Vision Research.

[30]  B. Dosher,et al.  Mechanisms of perceptual learning , 1999, Vision Research.

[31]  The National Academy of Sciences , 1928, Science.

[32]  B. Dosher,et al.  An integrated reweighting theory of perceptual learning , 2013, Proceedings of the National Academy of Sciences.

[33]  M. Carrasco,et al.  How spatial and feature-based attention affect the gain and tuning of population responses , 2009, Vision Research.

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

[35]  Chang-Bing Huang,et al.  Mechanisms underlying perceptual learning of contrast detection in adults with anisometropic amblyopia. , 2009, Journal of vision.

[36]  Denis G. Pelli,et al.  The visual filter mediating letter identification , 1994, Nature.

[37]  B. Sabel,et al.  Vision restoration therapy (VRT) efficacy as assessed by comparative perimetric analysis and subjective questionnaires. , 2004, Restorative neurology and neuroscience.

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

[39]  A. B. Sekuler,et al.  Signal but not noise changes with perceptual learning , 1999, Nature.

[40]  D G Pelli,et al.  Why use noise? , 1999, Journal of the Optical Society of America. A, Optics, image science, and vision.

[41]  Barbara Anne Dosher,et al.  Independent perceptual learning in monocular and binocular motion systems. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  G. Legge,et al.  Contrast discrimination in noise. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[43]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.

[44]  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.

[45]  Denis G Pelli,et al.  Using visual noise to characterize amblyopic letter identification. , 2004, Journal of vision.

[46]  A Hein,et al.  Cats reared in stroboscopic illumination: effects on receptive fields in visual cortex. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Dennis M Levi,et al.  Noise Provides Some New Signals About the Spatial Vision of Amblyopes , 2003, The Journal of Neuroscience.

[48]  Helle K. Falkenberg,et al.  Sampling efficiency and internal noise for motion detection, discrimination, and summation , 2003, Vision Research.

[49]  Duje Tadin,et al.  Beyond Blindsight: Properties of Visual Relearning in Cortically Blind Fields , 2014, The Journal of Neuroscience.

[50]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[51]  W. Merigan,et al.  Mechanisms of Sensitivity Loss due to Visual Cortex Lesions in Humans and Macaques. , 2006, Cerebral cortex.

[52]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  Debbie Y. Dao,et al.  Adaptation to sine-wave gratings selectively reduces the contrast gain of the adapted stimuli. , 2006, Journal of vision.

[54]  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.

[55]  A. Pouget,et al.  Perceptual learning as improved probabilistic inference in early sensory areas , 2011, Nature Neuroscience.

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

[57]  G. J. van der Wildt,et al.  Transfer Effects of Training-Induced Visual Field Recovery in Patients With Chronic Stroke , 2012, Topics in stroke rehabilitation.

[58]  Marisa Carrasco,et al.  Covert attention enhances letter identification without affecting channel tuning. , 2004, Journal of vision.