Experience-dependent representation of visual categories in parietal cortex

Categorization is a process by which the brain assigns meaning to sensory stimuli. Through experience, we learn to group stimuli into categories, such as ‘chair’, ‘table’ and ‘vehicle’, which are critical for rapidly and appropriately selecting behavioural responses. Although much is known about the neural representation of simple visual stimulus features (for example, orientation, direction and colour), relatively little is known about how the brain learns and encodes the meaning of stimuli. We trained monkeys to classify 360° of visual motion directions into two discrete categories, and compared neuronal activity in the lateral intraparietal (LIP) and middle temporal (MT) areas, two interconnected brain regions known to be involved in visual motion processing. Here we show that neurons in LIP—an area known to be centrally involved in visuo-spatial attention, motor planning and decision-making—robustly reflect the category of motion direction as a result of learning. The activity of LIP neurons encoded directions of motion according to their category membership, and that encoding shifted after the monkeys were retrained to group the same stimuli into two new categories. In contrast, neurons in area MT were strongly direction selective but carried little, if any, explicit category information. This indicates that LIP might be an important nexus for the transformation of visual direction selectivity to more abstract representations that encode the behavioural relevance, or meaning, of stimuli.

[1]  [Neurophysiology and behavior]. , 1973, Tidsskrift for den Norske laegeforening : tidsskrift for praktisk medicin, ny raekke.

[2]  L. Barsalou Cognitive Psychology: An Overview for Cognitive Scientists , 1992 .

[3]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[5]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[6]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[7]  A. Poling,et al.  Neurophysiology and Behavior , 1998 .

[8]  J. Assad,et al.  Dissociation of visual, motor and predictive signals in parietal cortex during visual guidance , 1999, Nature Neuroscience.

[9]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[10]  A P Batista,et al.  Reach plans in eye-centered coordinates. , 1999, Science.

[11]  R. Vogels Categorization of complex visual images by rhesus monkeys. Part 2: single‐cell study , 1999, The European journal of neuroscience.

[12]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[13]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[14]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[15]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[16]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[17]  N. Sigala,et al.  Visual categorization shapes feature selectivity in the primate temporal cortex , 2002, Nature.

[18]  B. Cohen,et al.  Spatial orientation of caloric nystagmus in semicircular canal-plugged monkeys. , 2002, Journal of neurophysiology.

[19]  R. Romo,et al.  Neuronal correlates of decision-making in secondary somatosensory cortex , 2002, Nature Neuroscience.

[20]  David J. Freedman,et al.  Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. , 2002, Journal of neurophysiology.

[21]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[22]  J. Assad,et al.  Dynamic coding of behaviourally relevant stimuli in parietal cortex , 2002, Nature.

[23]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[24]  Emad N Eskandar,et al.  Parietal activity and the perceived direction of ambiguous apparent motion , 2003, Nature Neuroscience.

[25]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[26]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[27]  M. Goldberg,et al.  A Rapid and Precise On-Response in Posterior Parietal Cortex , 2004, The Journal of Neuroscience.

[28]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

[29]  W. Newsome,et al.  Matching Behavior and the Representation of Value in the Parietal Cortex , 2004, Science.

[30]  Lawrence H Snyder,et al.  Single Neurons in Posterior Parietal Cortex of Monkeys Encode Cognitive Set , 2004, Neuron.

[31]  Andreas Nieder,et al.  A parieto-frontal network for visual numerical information in the monkey. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Geoffrey M Ghose,et al.  Learning in mammalian sensory cortex , 2004, Current Opinion in Neurobiology.

[33]  M. Shadlen,et al.  Neural Activity in Macaque Parietal Cortex Reflects Temporal Integration of Visual Motion Signals during Perceptual Decision Making , 2005, The Journal of Neuroscience.

[34]  David L. Faigman,et al.  Human category learning. , 2005, Annual review of psychology.

[35]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[36]  E. Miller,et al.  Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. , 2005, Cerebral cortex.