Perceptual learning modifies untrained pursuit eye movements.

Perceptual learning improves detection and discrimination of relevant visual information in mature humans, revealing sensory plasticity. Whether visual perceptual learning affects motor responses is unknown. Here we implemented a protocol that enabled us to address this question. We tested a perceptual response (motion direction estimation, in which observers overestimate motion direction away from a reference) and a motor response (voluntary smooth pursuit eye movements). Perceptual training led to greater overestimation and, remarkably, it modified untrained smooth pursuit. In contrast, pursuit training did not affect overestimation in either pursuit or perception, even though observers in both training groups were exposed to the same stimuli for the same time period. A second experiment revealed that estimation training also improved discrimination, indicating that overestimation may optimize perceptual sensitivity. Hence, active perceptual training is necessary to alter perceptual responses, and an acquired change in perception suffices to modify pursuit, a motor response.

[1]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[2]  R. K. Simpson Nature Neuroscience , 2022 .

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

[4]  Brian H Scott,et al.  A comparison of pursuit eye movement and perceptual performance in speed discrimination. , 2003, Journal of vision.

[5]  Christopher J. Peck,et al.  The time course of the tonic oculomotor proprioceptive signal in area 3a of somatosensory cortex. , 2011, Journal of neurophysiology.

[6]  C. Law,et al.  Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area , 2008, Nature Neuroscience.

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

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

[9]  Robert L. Goldstone Effects of Categorization on Color Perception , 1995 .

[10]  Pascal Mamassian,et al.  More is not always better: adaptive gain control explains dissociation between perception and action , 2012, Nature Neuroscience.

[11]  M. Fahle Perceptual learning: specificity versus generalization , 2005, Current Opinion in Neurobiology.

[12]  Brent R Beutter,et al.  Human discrimination of visual direction of motion with and without smooth pursuit eye movements. , 2003, Journal of vision.

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

[14]  Barbara Anne Dosher,et al.  Task precision at transfer determines specificity of perceptual learning. , 2009, Journal of vision.

[15]  Alexander C. Schütz,et al.  Eye movements and perception: a selective review. , 2011, Journal of vision.

[16]  V. Goffaux,et al.  The horizontal tuning of face perception relies on the processing of intermediate and high spatial frequencies. , 2011, Journal of vision.

[17]  Marisa Carrasco,et al.  Apparent contrast differs across the vertical meridian: visual and attentional factors. , 2008, Journal of vision.

[18]  Nestor Matthews,et al.  Task-specific perceptual learning on speed and direction discrimination , 2003, Vision Research.

[19]  L. Welch,et al.  Velocity-dependent improvements in single-dot direction discrimination , 1997, Perception & psychophysics.

[20]  Dennis M. Levi,et al.  Perceptual learning as a potential treatment for amblyopia: A mini-review , 2009, Vision Research.

[21]  S. Edelman,et al.  Long-term learning in vernier acuity: Effects of stimulus orientation, range and of feedback , 1993, Vision Research.

[22]  Karl R Gegenfurtner,et al.  Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion. , 2011, Journal of neurophysiology.

[23]  Mingsha Zhang,et al.  The proprioceptive representation of eye position in monkey primary somatosensory cortex , 2007, Nature Neuroscience.

[24]  Miriam Spering,et al.  Tracking Without Perceiving , 2011, Psychology Science.

[25]  Dirk Kerzel,et al.  Improved visual sensitivity during smooth pursuit eye movements , 2010 .

[26]  Paul V. McGraw,et al.  A Weber-like law for perceptual learning , 2013, Scientific Reports.

[27]  D. Sagi Perceptual learning in Vision Research , 2011, Vision Research.

[28]  Shinichi Koyama,et al.  Task-Dependent Changes of the Psychophysical Motion-Tuning Functions in the Course of Perceptual Learning , 2004, Perception.

[29]  A. Montagnini,et al.  Do we track what we see? Common versus independent processing for motion perception and smooth pursuit eye movements: A review , 2011, Vision Research.

[30]  S. Harnad Categorical Perception: The Groundwork of Cognition , 1990 .

[31]  Nicholas S C Price,et al.  Reflexive tracking eye movements and motion perception: one or two neural populations? , 2014, Journal of vision.

[32]  K. Nakayama,et al.  Categorical perception of face identity in noise isolates configural processing. , 2001, Journal of experimental psychology. Human perception and performance.

[33]  R. Krauzlis,et al.  Shared motion signals for human perceptual decisions and oculomotor actions. , 2003, Journal of vision.

[34]  Marisa Carrasco,et al.  Perceptual Learning and Dynamic Changes in Primary Visual Cortex , 2008, Neuron.

[35]  M Carrasco,et al.  The interaction of objective and subjective organizations in a localization search task , 1995, Perception & psychophysics.

[36]  S. Appelle Perception and discrimination as a function of stimulus orientation: the "oblique effect" in man and animals. , 1972, Psychological bulletin.

[37]  David Whitney,et al.  Reference repulsion in the categorical perception of biological motion , 2012, Vision Research.

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

[39]  Stephen G Lisberger,et al.  Visual Guidance of Smooth-Pursuit Eye Movements: Sensation, Action, and What Happens in Between , 2010, Neuron.

[40]  Jennifer L. Raymond,et al.  Motor Learning Reduces Eye Movement Variability through Reweighting of Sensory Inputs , 2010, The Journal of Neuroscience.

[41]  Miriam Spering,et al.  Similar Effects of Feature-Based Attention on Motion Perception and Pursuit Eye Movements at Different Levels of Awareness , 2012, The Journal of Neuroscience.

[42]  S. Harnad Psychophysical and cognitive aspects of categorical perception: A critical overview , 1987 .

[43]  Eileen Kowler,et al.  Sensitivity of smooth eye movement to small differences in target velocity , 1987, Vision Research.

[44]  Gunnar Blohm,et al.  Catch-up saccades in head-unrestrained conditions reveal that saccade amplitude is corrected using an internal model of target movement. , 2014, Journal of vision.

[45]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[46]  M. Carrasco,et al.  Attention alters appearance , 2004, Nature Neuroscience.

[47]  Jared Abrams,et al.  Voluntary attention increases perceived spatial frequency , 2010, Attention, perception & psychophysics.

[48]  Marisa Carrasco,et al.  Perceptual asymmetries are preserved in short-term memory tasks , 2009, Attention, perception & psychophysics.

[49]  M. Hawken,et al.  Smooth pursuit eye movements to isoluminant targets. , 2008, Journal of neurophysiology.

[50]  David J. Freedman,et al.  A proposed common neural mechanism for categorization and perceptual decisions , 2011, Nature Neuroscience.

[51]  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.

[52]  L. Jakobson,et al.  A neurological dissociation between perceiving objects and grasping them , 1991, Nature.

[53]  Stefan Treue,et al.  Reference Repulsion When Judging the Direction of Visual Motion , 1998, Perception.

[54]  N. Logothetis,et al.  Neuronal correlates of subjective visual perception. , 1989, Science.

[55]  H. J. Rauder Reference repulision when judging the direction of visual motion , 1998 .

[56]  Dario L. Ringach,et al.  When your eyes see more than you do , 2010, Current Biology.

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

[58]  Zili Liu,et al.  Transfer in motion perceptual learning depends on the difficulty of the training task. , 2013, Journal of vision.

[59]  R. Wurtz,et al.  Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. , 1988, Journal of neurophysiology.

[60]  Tandra Ghose,et al.  Generalization between canonical and non-canonical views in object recognition. , 2013, Journal of vision.

[61]  Karl R Gegenfurtner,et al.  Contrast and assimilation in motion perception and smooth pursuit eye movements. , 2007, Journal of neurophysiology.

[62]  Anne-Kathrin Warzecha,et al.  Open-loop speed discrimination performance of ocular following response and perception , 2010, Vision Research.

[63]  Maninder K. Kahlon,et al.  Visual Motion Analysis for Pursuit Eye Movements in Area MT of Macaque Monkeys , 1999, The Journal of Neuroscience.

[64]  Takeo Watanabe,et al.  Advances in visual perceptual learning and plasticity , 2010, Nature Reviews Neuroscience.