Interaction between neuronal encoding and population dynamics during categorization task switching in parietal cortex

Primates excel at categorization, a cognitive process for assigning stimuli into behaviorally relevant groups. Categories are encoded in multiple brain areas and tasks, yet it remains unclear how neural encoding and dynamics support cognitive tasks with different demands. We recorded from parietal cortex during flexible switching between categorization tasks with distinct cognitive and motor demands and also studied recurrent neural networks (RNNs) trained on the same tasks. In the one-interval categorization task (OIC), monkeys rapidly reported their decisions with a saccade. In the delayed match-to-category (DMC) task, monkeys decided whether sequentially presented stimuli were categorical matches. Neuronal category encoding generalized across tasks, but categorical encoding was more binary-like in the DMC task and more graded in the OIC task. Furthermore, analysis of trained RNNs supports the hypothesis that binary-like encoding in DMC arises through compression of graded feature encoding by attractor dynamics underlying stimulus maintenance and/or comparison in working memory.

[1]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[2]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

[3]  Christos Constantinidis,et al.  Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex , 2016, Proceedings of the National Academy of Sciences.

[4]  Jonathan W Pillow,et al.  Error-correcting dynamics in visual working memory , 2018, Nature Communications.

[5]  David J. Freedman,et al.  Dynamic population coding of category information in inferior temporal and prefrontal cortex. , 2008, Journal of neurophysiology.

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

[7]  David J. Freedman,et al.  Posterior parietal cortex plays a causal role in perceptual and categorical decisions , 2019, Science.

[8]  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.

[9]  David J. Freedman,et al.  Preferential Encoding of Visual Categories in Parietal Cortex Compared to Prefrontal Cortex , 2011, Nature Neuroscience.

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

[11]  David J. Freedman,et al.  Computing by Robust Transience: How the Fronto-Parietal Network Performs Sequential, Category-Based Decisions , 2017, Neuron.

[12]  David J. Freedman,et al.  Neuronal Mechanisms of Visual Categorization: An Abstract View on Decision Making. , 2016, Annual review of neuroscience.

[13]  Vladimir Vapnik,et al.  Support-vector networks , 2004, Machine Learning.

[14]  Jonathan I. Flombaum,et al.  Why some colors appear more memorable than others: A model combining categories and particulars in color working memory. , 2015, Journal of experimental psychology. General.

[15]  Jimmy Ba,et al.  Adam: A Method for Stochastic Optimization , 2014, ICLR.

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

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

[18]  M. Goldberg,et al.  Attention, intention, and priority in the parietal lobe. , 2010, Annual review of neuroscience.

[19]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[20]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[21]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[22]  Nicolas Y. Masse,et al.  Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices , 2015, Nature Neuroscience.

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

[24]  David Sussillo,et al.  FixedPointFinder: A Tensorflow toolbox for identifying and characterizing fixed points in recurrent neural networks , 2018, J. Open Source Softw..

[25]  Martín Abadi,et al.  TensorFlow: Large-Scale Machine Learning on Heterogeneous Distributed Systems , 2016, ArXiv.

[26]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[27]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[28]  Stephen I. Ryu,et al.  Neural Dynamics of Reaching following Incorrect or Absent Motor Preparation , 2014, Neuron.

[29]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Jonathan I. Flombaum,et al.  Stimulus-specific variability in color working memory with delayed estimation. , 2014, Journal of vision.

[31]  David J. Freedman,et al.  Independent Category and Spatial Encoding in Parietal Cortex , 2013, Neuron.

[32]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

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

[34]  David J. Freedman,et al.  Biased Associative Representations in Parietal Cortex , 2013, Neuron.

[35]  Nicolas Y. Masse,et al.  A Comparison of Lateral and Medial Intraparietal Areas during a Visual Categorization Task , 2013, The Journal of Neuroscience.

[36]  Nicolas Y. Masse,et al.  Circuit mechanisms for the maintenance and manipulation of information in working memory , 2018, Nature Neuroscience.

[37]  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.

[38]  A. Compte,et al.  Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory , 2014, Nature Neuroscience.