Biased Associative Representations in Parietal Cortex

Neurons in cortical sensory areas respond selectively to sensory stimuli, and the preferred stimulus typically varies among neurons so as to continuously span the sensory space. However, some neurons reflect sensory features that are learned or task dependent. For example, neurons in the lateral intraparietal area (LIP) reflect learned associations between visual stimuli. One might expect that roughly even numbers of LIP neurons would prefer each set of associated stimuli. However, in two associative learning experiments and a perceptual decision experiment, we found striking asymmetries: nearly all neurons recorded from an animal had a similar order of preference among associated stimuli. Behavioral factors could not account for these neuronal biases. A recent computational study proposed that population-firing patterns in parietal cortex have one-dimensional dynamics on long timescales, a possible consequence of recurrent connections that could drive persistent activity. One-dimensional dynamics would predict the biases in selectivity that we observed.

[1]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[2]  Y. Miyashita,et al.  Activity of primate inferotemporal neurons related to a sought target in pair-association task. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

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

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

[6]  A. Sereno,et al.  Attention and memory-related responses of neurons in the lateral intraparietal area during spatial and shape-delayed match-to-sample tasks. , 2006, Journal of neurophysiology.

[7]  Xiao-Jing Wang Decision Making in Recurrent Neuronal Circuits , 2008, Neuron.

[8]  Keiji Tanaka,et al.  Statistics of visual responses in primate inferotemporal cortex to object stimuli. , 2011, Journal of neurophysiology.

[9]  David J. Freedman,et al.  The prefrontal cortex: categories, concepts and cognition. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[11]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[12]  Gregory C DeAngelis,et al.  Coding of horizontal disparity and velocity by MT neurons in the alert macaque. , 2003, Journal of neurophysiology.

[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]  T. Albright Centrifugal directional bias in the middle temporal visual area (MT) of the macaque , 1989, Visual Neuroscience.

[15]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[16]  M. Goldberg,et al.  Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior. , 2006, Progress in brain research.

[17]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  E. Miller,et al.  Prospective Coding for Objects in Primate Prefrontal Cortex , 1999, The Journal of Neuroscience.

[19]  Joshua I Gold,et al.  Correlates of Perceptual Learning in an Oculomotor Decision Variable , 2009, The Journal of Neuroscience.

[20]  James W Bisley,et al.  Neural correlates of attention and distractibility in the lateral intraparietal area. , 2006, Journal of neurophysiology.

[21]  Sylvia Wirth,et al.  Representation of Well-Learned Information in the Monkey Hippocampus , 2004, Neuron.

[22]  Y. Miyashita,et al.  Backward spreading of memory-retrieval signal in the primate temporal cortex. , 2001, Science.

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

[24]  Andreas Nieder,et al.  Active encoding of decisions about stimulus absence in primate prefrontal cortex neurons , 2012, Proceedings of the National Academy of Sciences.

[25]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[26]  P. O. Bishop,et al.  Responses to moving slits by single units in cat striate cortex , 2004, Experimental Brain Research.

[27]  S. Sutherland Eye, brain and vision , 1993, Nature.

[28]  J. Gold,et al.  Distinct Representations of a Perceptual Decision and the Associated Oculomotor Plan in the Monkey Lateral Intraparietal Area , 2011, The Journal of Neuroscience.

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

[30]  David J. Freedman,et al.  Generalized associative representations in parietal cortex , 2011, Nature Neuroscience.

[31]  Xiao-Jing Wang,et al.  A Recurrent Network Mechanism of Time Integration in Perceptual Decisions , 2006, The Journal of Neuroscience.

[32]  C. Cassanello,et al.  Frontal Eye Field Neurons Signal Changes in Decision Criteria , 2009, Nature Neuroscience.

[33]  David J. Freedman,et al.  Experience-dependent representation of visual categories in parietal cortex , 2006, Nature.

[34]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[35]  D. Amit,et al.  Retrospective and prospective persistent activity induced by Hebbian learning in a recurrent cortical network , 2003, The European journal of neuroscience.

[36]  Yasushi Miyashita,et al.  Delay‐period activities in two subdivisions of monkey inferotemporal cortex during pair association memory task , 2003, The European journal of neuroscience.

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

[38]  J. Hegdé,et al.  A comparative study of shape representation in macaque visual areas v2 and v4. , 2007, Cerebral cortex.

[39]  Jefferson E. Roy,et al.  Prefrontal Cortex Activity during Flexible Categorization , 2010, The Journal of Neuroscience.

[40]  Bevil R. Conway,et al.  Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex , 2009, Proceedings of the National Academy of Sciences.

[41]  K. Miller,et al.  One-Dimensional Dynamics of Attention and Decision Making in LIP , 2008, Neuron.

[42]  Jefferson E. Roy,et al.  Representation of Multiple, Independent Categories in the Primate Prefrontal Cortex , 2010, Neuron.

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

[44]  J. Assad,et al.  Direction selectivity of neurons in the macaque lateral intraparietal area. , 2009, Journal of neurophysiology.