Attention Alters Visual Plasticity during Exposure-Based Learning

It is generally believed that attention enhances the processing of sensory information during perception and learning. Here we report that, contrary to common belief, attention limits the degree of plasticity induced by repeated exposure to image features. Specifically, daily exposure to oriented stimuli that are not linked to a specific task causes an orientation-specific improvement in perceptual performance along the "exposed" axes. This effect is modulated by attention: human subjects showed a larger improvement in orientation discrimination when attention is directed toward the location where stimuli are presented. However, the capacity to perform discriminations away from the exposed orientation is enhanced when the exposure stimuli are unattended. Importantly, the improvement in orientation discrimination at the unattended location leads to a robust enhancement in the discrimination of complex stimuli, such as natural texture images, with orientation components along the exposed axes, whereas the improvement in orientation discrimination at the attended location exhibits only weak transfer to complex stimuli. These results indicate that sensory adaptation by passive stimulus exposure should be viewed as a form of perceptual learning that is complementary to practice-based learning in that it reduces constraints on generalization.

[1]  Frances S. Chance,et al.  Synaptic Depression and the Temporal Response Characteristics of V1 Cells , 1998, The Journal of Neuroscience.

[2]  Misha Tsodyks,et al.  Associative learning in early vision , 2004, Neural Networks.

[3]  M. Bear,et al.  Instructive Effect of Visual Experience in Mouse Visual Cortex , 2006, Neuron.

[4]  Valentin Dragoi,et al.  Asymmetric synaptic depression in cortical networks. , 2008, Cerebral cortex.

[5]  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.

[6]  Mitsuo Kawato,et al.  Effect of spatial distance to the task stimulus on task-irrelevant perceptual learning of static Gabors. , 2007, Journal of vision.

[7]  M. Sur,et al.  Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex , 2000, Neuron.

[8]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[9]  G. Orban,et al.  The effect of practice on the oblique effect in line orientation judgments , 1985, Vision Research.

[10]  Valentin Dragoi,et al.  Adaptive coding of visual information in neural populations , 2008, Nature.

[11]  D. Regan,et al.  Postadaptation orientation discrimination. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[12]  E. Miller,et al.  Dynamics of neuronal sensitivity in visual cortex and local feature discrimination , 2002, Nature Neuroscience.

[13]  Mriganka Sur,et al.  Image Structure at the Center of Gaze during Free Viewing , 2006, Journal of Cognitive Neuroscience.

[14]  Martin Tegenthoff,et al.  Differential effects of synchronous and asynchronous multifinger coactivation on human tactile performance , 2007, BMC Neuroscience.

[15]  Aaron R. Seitz,et al.  Psychophysics: Is subliminal learning really passive? , 2003, Nature.

[16]  D Purves,et al.  The distribution of oriented contours in the real world. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Takeo Watanabe,et al.  Perceptual learning without perception , 2001, Nature.

[18]  Valentin Dragoi,et al.  Asymmetric Synaptic Depression in , 2008 .

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

[20]  D Regan,et al.  Visual responses to vorticity and the neural analysis of optic flow. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[21]  Carrie J. McAdams,et al.  Effects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex , 1999, Neuron.

[22]  Sygal Amitay,et al.  Discrimination learning induced by training with identical stimuli , 2006, Nature Neuroscience.

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

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

[25]  Aaron R. Seitz,et al.  Task-irrelevant learning occurs only when the irrelevant feature is weak , 2008, Current Biology.

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

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

[28]  M. Sur,et al.  Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. , 2000, Journal of neurophysiology.

[29]  Aaron R. Seitz,et al.  A unified model for perceptual learning , 2005, Trends in Cognitive Sciences.

[30]  Derek H. Arnold,et al.  Orthogonal adaptation improves orientation discrimination , 2001, Vision Research.

[31]  I. Biederman,et al.  Subliminal visual priming , 1997, Neuroscience Letters.

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

[33]  Eero P. Simoncelli,et al.  Natural image statistics and neural representation. , 2001, Annual review of neuroscience.

[34]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[35]  R. Zajonc Attitudinal effects of mere exposure. , 1968 .

[36]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[37]  Yang Dan,et al.  Dynamic Modification of Cortical Orientation Tuning Mediated by Recurrent Connections , 2002, Neuron.

[38]  H. Levitt Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[39]  S. Klein,et al.  Measuring, estimating, and understanding the psychometric function: A commentary , 2001, Perception & psychophysics.

[40]  T Poggio,et al.  Fast perceptual learning in visual hyperacuity. , 1991, Science.

[41]  Chuan Yi Tang,et al.  A 2.|E|-Bit Distributed Algorithm for the Directed Euler Trail Problem , 1993, Inf. Process. Lett..