Perceptual learning of line orientation modifies the effects of transcranial magnetic stimulation of visual cortex

Perceptual learning may be accompanied by physiological changes in early visual cortex. We used transcranial magnetic stimulation (TMS) to test the postulate that perceptual learning of a visual task initially performed at 60–65% accuracy strengthens visual processing in early visual cortex. Single pulse TMS was delivered to human occipital cortex at time delays of 70–154 ms after the onset of an odd-element, line orientation discrimination task. When TMS was delivered at a delay of 84 ms or later the accuracy of visual discrimination was transiently degraded in ten subjects. As visual performance in control trials without TMS improved with training, the absolute magnitude of TMS suppression of performance decreased in parallel. This result occurred both when TMS was delivered to broad areas of occipital cortex and when TMS was optimally delivered to early occipital cortex. No change in TMS suppression was observed when three new subjects were given feedback during an odd-element task that did not require substantial perceptual learning. Thus, perceptual learning improved visual performance and reduced TMS suppression of early visual cortex in parallel.

[1]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[2]  Robert H. Anderson,et al.  On Technical Considerations , 1995, Writing Ethnography (Second Edition).

[3]  N. Logothetis,et al.  The Effect of Learning on the Function of Monkey Extrastriate Visual Cortex , 2004, PLoS biology.

[4]  Shaul Hochstein,et al.  Learning pop-out detection: building representations for conflicting target-distractor relationships , 1998, Vision Research.

[5]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[6]  G. Orban,et al.  Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. , 1995, The Journal of physiology.

[7]  Georg Schweigart,et al.  Activity‐dependent receptive field changes in the surround of adult cat visual cortex lesions , 2002, The European journal of neuroscience.

[8]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

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

[10]  Misha Tsodyks,et al.  Context-enabled learning in the human visual system , 2002, Nature.

[11]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[12]  U Polat,et al.  Spatial interactions in human vision: from near to far via experience-dependent cascades of connections. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Thomas Kammer,et al.  Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship , 1998, Neuropsychologia.

[14]  S. Anand,et al.  Transcranial magnetic stimulation: Neurophysiological applications and safety , 2002, Brain and Cognition.

[15]  Gianluca Campana,et al.  Priming of motion direction and area V5/MT: a test of perceptual memory. , 2002, Cerebral cortex.

[16]  John H. R. Maunsell,et al.  Physiological correlates of perceptual learning in monkey V1 and V2. , 2002, Journal of neurophysiology.

[17]  G. Orban,et al.  Neuronal Mechanisms of Perceptual Learning: Changes in Human Brain Activity with Training in Orientation Discrimination , 1999, NeuroImage.

[18]  S. Bandinelli,et al.  Effects of coil design on delivery of focal magnetic stimulation. Technical considerations. , 1990, Electroencephalography and clinical neurophysiology.

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

[20]  B. Godde,et al.  Tactile Coactivation-Induced Changes in Spatial Discrimination Performance , 2000, The Journal of Neuroscience.

[21]  John R. Hotson,et al.  Tracing the timing of human analysis of motion and chromatic signals from occipital to temporo-parieto-occipital cortex: A transcranial magnetic stimulation study , 1998, Vision Research.

[22]  J C Rothwell,et al.  Effect of transcranial magnetic stimulation over the cerebellum on the excitability of human motor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[23]  S. Anand,et al.  The selectivity and timing of motion processing in human temporo–parieto–occipital and occipital cortex: a transcranial magnetic stimulation study , 1998, Neuropsychologia.

[24]  K. H. Britten,et al.  Neuronal plasticity that underlies improvement in perceptual performance. , 1994, Science.

[25]  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.

[26]  Keiji Tanaka,et al.  Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. , 1998, Journal of neurophysiology.

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

[28]  D. Scott Perceptual learning. , 1974, Queen's nursing journal.

[29]  V. Ramachandran,et al.  Learning-like phenomena in stereopsis , 1976, Nature.

[30]  U. Ziemann,et al.  Transient visual field defects induced by transcranial magnetic stimulation over human occipital pole , 1998, Experimental Brain Research.

[31]  José E. Náñez,et al.  Greater plasticity in lower-level than higher-level visual motion processing in a passive perceptual learning task , 2002, Nature Neuroscience.

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

[33]  Chi-Hung Juan,et al.  Feedback to V1: a reverse hierarchy in vision , 2003, Experimental Brain Research.

[34]  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.

[35]  H. Dinse,et al.  Shifts in cortical representations predict human discrimination improvement , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. McKee,et al.  Improvement in vernier acuity with practice , 1978, Perception & psychophysics.

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

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

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

[40]  M. Sur,et al.  Foci of orientation plasticity in visual cortex , 2001, Nature.

[41]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[42]  N. Qian,et al.  Learning and adaptation in a recurrent model of V1 orientation selectivity. , 2003, Journal of neurophysiology.

[43]  G. Westheimer,et al.  Effects of practice and the separation of test targets on foveal and peripheral stereoacuity , 1983, Vision Research.

[44]  J. Kaas,et al.  Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina , 1992, Vision Research.

[45]  T. Poggio,et al.  Fast perceptual learning in hyperacuity , 1995, Vision Research.

[46]  D. Braun,et al.  Transcranial magnetic stimulation of extrastriate cortex degrades human motion direction discrimination , 1994, Vision Research.

[47]  C. Furmanski,et al.  Perceptual learning in object recognition: object specificity and size invariance , 2000, Vision Research.

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

[49]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[50]  S. Hochstein,et al.  Attentional control of early perceptual learning. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Patrick Ragert,et al.  Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans , 2004, Neuroscience Letters.

[52]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[53]  J. Maunsell,et al.  The Effect of Perceptual Learning on Neuronal Responses in Monkey Visual Area V4 , 2004, The Journal of Neuroscience.

[54]  Hubert R. Dinse,et al.  Associative pairing of tactile stimulation induces somatosensory cortical reorganization in rats and humans , 1996, Neuroreport.

[55]  C. Gilbert,et al.  Improvement in visual sensitivity by changes in local context: Parallel studies in human observers and in V1 of alert monkeys , 1995, Neuron.

[56]  D. Mumford,et al.  Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency , 2002, Nature Neuroscience.

[57]  V. Amassian,et al.  Suppression of visual perception by magnetic coil stimulation of human occipital cortex. , 1989, Electroencephalography and clinical neurophysiology.

[58]  Alan Cowey,et al.  Plasticity revealed by transcranial magnetic stimulation of early visual cortex , 2000, Neuroreport.

[59]  M Hallett,et al.  A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[60]  M Hallett,et al.  Topographic mapping of the human motor cortex with magnetic stimulation: factors affecting accuracy and reproducibility. , 1992, Electroencephalography and clinical neurophysiology.

[61]  Alan Cowey,et al.  Cortical plasticity in perceptual learning demonstrated by transcranial magnetic stimulation , 1998, Neuropsychologia.

[62]  Alan P. Rudell,et al.  Unmasking human visual perception with the magnetic coil and its relationship to hemispheric asymmetry , 1993, Brain Research.