Recurrent neural network models of multi-area computation underlying decision-making

Cognition emerges from coordinated computations across multiple brain areas. However, elucidating these computations within and across brain regions is challenging because intra- and inter-area connectivity are typically unknown. To study coordinated computation, we trained multi-area recurrent neural networks (RNNs) to discriminate the dominant color of a checker-board and output decision variables reflecting a direction decision, a task previously used to investigate decision-related dynamics in dorsal premotor cortex (PMd) of monkeys. We found that multi-area RNNs, trained with neurophysiological connectivity constraints and Dale’s law, recapitulated decision-related dynamics observed in PMd. The RNN solved this task by a dynamical mechanism where the direction decision was computed and outputted, via precisely oriented dynamics, on an axis that was nearly orthogonal to checkerboard color inputs. This orthogonal direction information was preferentially propagated through alignment with inter-area connections; in contrast, color information was filtered. These results suggest that cortex uses modular computation to generate minimal sufficient representations of task information. Finally, we used multi-area RNNs to produce experimentally testable hypotheses for computations that occur within and across multiple brain areas, enabling new insights into distributed computation in neural systems.

[1]  R. Dahlstrom,et al.  Challenges and opportunities , 2021, Foundations of a Sustainable Economy.

[2]  Alessandro Achille,et al.  Usable Information and Evolution of Optimal Representations During Training , 2020, ICLR.

[3]  Adam Kohn,et al.  Principles of Corticocortical Communication: Proposed Schemes and Design Considerations , 2020, Trends in Neurosciences.

[4]  Xiao-Jing Wang,et al.  Artificial Neural Networks for Neuroscientists: A Primer , 2020, Neuron.

[5]  William E. Allen,et al.  Cortical Observation by Synchronous Multifocal Optical Sampling Reveals Widespread Population Encoding of Actions , 2020, Neuron.

[6]  Niru Maheswaranathan,et al.  How recurrent networks implement contextual processing in sentiment analysis , 2020, ICML.

[7]  Adam Santoro,et al.  Backpropagation and the brain , 2020, Nature Reviews Neuroscience.

[8]  Carlos D. Brody,et al.  Task-Dependent Changes in the Large-Scale Dynamics and Necessity of Cortical Regions , 2019, Neuron.

[9]  Jonathan C Kao,et al.  Considerations in using recurrent neural networks to probe neural dynamics. , 2019, Journal of neurophysiology.

[10]  Nicholas A. Steinmetz,et al.  Distributed coding of choice, action, and engagement across the mouse brain , 2019, Nature.

[11]  Stefan Schaffelhofer,et al.  A neural network model of flexible grasp movement generation , 2019, bioRxiv.

[12]  Surya Ganguli,et al.  Reverse engineering recurrent networks for sentiment classification reveals line attractor dynamics , 2019, NeurIPS.

[13]  Alexander A. Alemi,et al.  On Variational Bounds of Mutual Information , 2019, ICML.

[14]  A. Arnsten,et al.  Loss of Prefrontal Cortical Higher Cognition with Uncontrollable Stress: Molecular Mechanisms, Changes with Age, and Relevance to Treatment , 2019, Brain sciences.

[15]  K. Shenoy,et al.  Macaque dorsal premotor cortex exhibits decision-related activity only when specific stimulus–response associations are known , 2018, Nature Communications.

[16]  Byron M. Yu,et al.  Cortical Areas Interact through a Communication Subspace , 2019, Neuron.

[17]  Xiao-Jing Wang,et al.  Task representations in neural networks trained to perform many cognitive tasks , 2019, Nature Neuroscience.

[18]  Kenneth W. Latimer Nonlinear demixed component analysis for neural population data as a low-rank kernel regression problem , 2018, 1812.08238.

[19]  Eva L. Dyer,et al.  Latent Factors and Dynamics in Motor Cortex and Their Application to Brain–Machine Interfaces , 2018, The Journal of Neuroscience.

[20]  Christian Ethier,et al.  Cortical population activity within a preserved neural manifold underlies multiple motor behaviors , 2018, Nature Communications.

[21]  Guillaume Hennequin,et al.  Motor primitives in space and time via targeted gain modulation in cortical networks , 2018, Nature Neuroscience.

[22]  K. Shenoy,et al.  Macaque dorsal premotor cortex exhibits decision-related activity only when specific stimulus–response associations are known , 2018, Nature Communications.

[23]  Jonathan C. Kao,et al.  Considerations in using recurrent neural networks to probe neural dynamics , 2018, bioRxiv.

[24]  Kenneth D Harris,et al.  Challenges and opportunities for large-scale electrophysiology with Neuropixels probes , 2018, Current Opinion in Neurobiology.

[25]  Razvan Pascanu,et al.  Vector-based navigation using grid-like representations in artificial agents , 2018, Nature.

[26]  Constant D. Beugré,et al.  The neural basis of decision making , 2018 .

[27]  K. Svoboda,et al.  Neural mechanisms of movement planning: motor cortex and beyond , 2018, Current Opinion in Neurobiology.

[28]  Devika Narain,et al.  Flexible Sensorimotor Computations through Rapid Reconfiguration of Cortical Dynamics , 2018, Neuron.

[29]  Wei Ji Ma,et al.  A diverse range of factors affect the nature of neural representations underlying short-term memory , 2018, Nature Neuroscience.

[30]  Francesca Mastrogiuseppe,et al.  Linking Connectivity, Dynamics, and Computations in Low-Rank Recurrent Neural Networks , 2017, Neuron.

[31]  Surya Ganguli,et al.  Unsupervised Discovery of Demixed, Low-Dimensional Neural Dynamics across Multiple Timescales through Tensor Component Analysis , 2017, Neuron.

[32]  Stefano Soatto,et al.  Emergence of Invariance and Disentanglement in Deep Representations , 2017, 2018 Information Theory and Applications Workshop (ITA).

[33]  Omri Barak,et al.  Recurrent neural networks as versatile tools of neuroscience research , 2017, Current Opinion in Neurobiology.

[34]  Krishna V Shenoy,et al.  Laminar differences in decision-related neural activity in dorsal premotor cortex , 2017, Nature Communications.

[35]  John P. Cunningham,et al.  Behaviorally Selective Engagement of Short-Latency Effector Pathways by Motor Cortex , 2017, Neuron.

[36]  Stephen I. Ryu,et al.  Motor Cortical Visuomotor Feedback Activity Is Initially Isolated from Downstream Targets in Output-Null Neural State Space Dimensions , 2017, Neuron.

[37]  Lee E. Miller,et al.  Neural Manifolds for the Control of Movement , 2017, Neuron.

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

[39]  Naftali Tishby,et al.  Opening the Black Box of Deep Neural Networks via Information , 2017, ArXiv.

[40]  Dean V Buonomano,et al.  Encoding sensory and motor patterns as time-invariant trajectories in recurrent neural networks , 2017, bioRxiv.

[41]  Ronald de Wolf,et al.  Optimal Quantum Sample Complexity of Learning Algorithms , 2016, CCC.

[42]  Hansjörg Scherberger,et al.  Neural Population Dynamics during Reaching Are Better Explained by a Dynamical System than Representational Tuning , 2016, PLoS Comput. Biol..

[43]  John P. Cunningham,et al.  Reorganization between preparatory and movement population responses in motor cortex , 2016, Nature Communications.

[44]  Ari S. Morcos,et al.  History-dependent variability in population dynamics during evidence accumulation in cortex , 2016, Nature Neuroscience.

[45]  Xiao-Jing Wang,et al.  Reward-based training of recurrent neural networks for cognitive and value-based tasks , 2016, bioRxiv.

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

[47]  Matthew T. Kaufman,et al.  The Largest Response Component in the Motor Cortex Reflects Movement Timing but Not Movement Type , 2016, eNeuro.

[48]  Naoshige Uchida,et al.  Demixed principal component analysis of neural population data , 2014, eLife.

[49]  Bruce G Cumming,et al.  Feedforward and Feedback Sources of Choice Probability in Neural Population Responses This Review Comes from a Themed Issue on Neurobiology of Cognitive Behavior Evidence for Feed-forward Models and Optimal Linear Readout? , 2022 .

[50]  Stefano Fusi,et al.  Why neurons mix: high dimensionality for higher cognition , 2016, Current Opinion in Neurobiology.

[51]  Christopher D. Harvey,et al.  Recurrent Network Models of Sequence Generation and Memory , 2016, Neuron.

[52]  Nuo Li,et al.  Robust neuronal dynamics in premotor cortex during motor planning , 2016, Nature.

[53]  J. DiCarlo,et al.  Using goal-driven deep learning models to understand sensory cortex , 2016, Nature Neuroscience.

[54]  Naoshige Uchida,et al.  Author response: Demixed principal component analysis of neural population data , 2016 .

[55]  Anne-Marie M. Oswald,et al.  Balanced feedforward inhibition and dominant recurrent inhibition in olfactory cortex , 2016, Proceedings of the National Academy of Sciences.

[56]  Guangyu R. Yang,et al.  Training Excitatory-Inhibitory Recurrent Neural Networks for Cognitive Tasks: A Simple and Flexible Framework , 2016, PLoS Comput. Biol..

[57]  Roland R. Regoes,et al.  Investigating the Consequences of Interference between Multiple CD8+ T Cell Escape Mutations in Early HIV Infection , 2016, PLoS Comput. Biol..

[58]  Dora E Angelaki,et al.  Dissecting neural circuits for multisensory integration and crossmodal processing , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[59]  H. Barbas General cortical and special prefrontal connections: principles from structure to function. , 2015, Annual review of neuroscience.

[60]  Matthew T. Kaufman,et al.  A neural network that finds a naturalistic solution for the production of muscle activity , 2015, Nature Neuroscience.

[61]  Markus Siegel,et al.  Cortical information flow during flexible sensorimotor decisions , 2015, Science.

[62]  Geoffrey E. Hinton,et al.  Deep Learning , 2015, Nature.

[63]  Mark M Churchland,et al.  Vacillation, indecision and hesitation in moment-by-moment decoding of monkey motor cortex , 2015, eLife.

[64]  J. Kalaska,et al.  Dorsal premotor cortex: neural correlates of reach target decisions based on a color-location matching rule and conflicting sensory evidence. , 2015, Journal of neurophysiology.

[65]  David J. Anderson,et al.  Ventromedial hypothalamic neurons control a defensive emotion state , 2015, eLife.

[66]  Bingni W. Brunton,et al.  Distinct effects of prefrontal and parietal cortex inactivations on an accumulation of evidence task in the rat , 2015, bioRxiv.

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

[68]  Gustavo Deco,et al.  Task-driven intra- and interarea communications in primate cerebral cortex , 2014, Proceedings of the National Academy of Sciences.

[69]  Stefano Soatto,et al.  Visual Representations: Defining Properties and Deep Approximations , 2014, ICLR 2016.

[70]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[71]  W. Gerstner,et al.  Optimal Control of Transient Dynamics in Balanced Networks Supports Generation of Complex Movements , 2014, Neuron.

[72]  Ha Hong,et al.  Performance-optimized hierarchical models predict neural responses in higher visual cortex , 2014, Proceedings of the National Academy of Sciences.

[73]  Matthew T. Kaufman,et al.  Supplementary materials for : Cortical activity in the null space : permitting preparation without movement , 2014 .

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

[75]  Nikola T. Markov,et al.  Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex , 2013, The Journal of comparative neurology.

[76]  Nikola T. Markov,et al.  A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex , 2012, Cerebral cortex.

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

[78]  E. Hoshi Cortico-basal ganglia networks subserving goal-directed behavior mediated by conditional visuo-goal association , 2013, Front. Neural Circuits.

[79]  Dean V. Buonomano,et al.  ROBUST TIMING AND MOTOR PATTERNS BY TAMING CHAOS IN RECURRENT NEURAL NETWORKS , 2012, Nature Neuroscience.

[80]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[81]  Bingni W. Brunton,et al.  Rats and Humans Can Optimally Accumulate Evidence for Decision-Making , 2013, Science.

[82]  R. Romo,et al.  Conversion of sensory signals into perceptual decisions , 2013, Progress in Neurobiology.

[83]  David Sussillo,et al.  Opening the Black Box: Low-Dimensional Dynamics in High-Dimensional Recurrent Neural Networks , 2013, Neural Computation.

[84]  Razvan Pascanu,et al.  On the difficulty of training recurrent neural networks , 2012, ICML.

[85]  P. Cisek Making decisions through a distributed consensus , 2012, Current Opinion in Neurobiology.

[86]  E. Hoshi,et al.  Multisynaptic projections from the ventrolateral prefrontal cortex to the dorsal premotor cortex in macaques – anatomical substrate for conditional visuomotor behavior , 2012, The European journal of neuroscience.

[87]  D. Buonomano,et al.  Complexity without chaos: Plasticity within random recurrent networks generates robust timing and motor control , 2012, 1210.2104.

[88]  Jun Tanji,et al.  Distinct Information Representation and Processing for Goal-Directed Behavior in the Dorsolateral and Ventrolateral Prefrontal Cortex and the Dorsal Premotor Cortex , 2012, The Journal of Neuroscience.

[89]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[90]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

[91]  D. Pandya,et al.  The cortical connectivity of the prefrontal cortex in the monkey brain , 2012, Cortex.

[92]  J. Rothwell,et al.  Cortical Connectivity , 2012, Springer Berlin Heidelberg.

[93]  Byron M. Yu,et al.  Single-Trial Neural Correlates of Arm Movement Preparation , 2011, Neuron.

[94]  J. S. Montijn Neural Mechanisms of Visual Attention , 2011 .

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

[96]  E. Miller,et al.  Buschman and Posterior Parietal Cortices Top-Down Versus Bottom-Up Control of Attention in the Prefrontal , 2011 .

[97]  S. Kastner,et al.  Mechanisms of Spatial Attention Control in Frontal and Parietal Cortex , 2010, The Journal of Neuroscience.

[98]  Invariant Object Identification A Neural Network Model of , 2010 .

[99]  G. Luppino,et al.  Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. , 2010, Cerebral cortex.

[100]  Bevil R. Conway,et al.  Color Vision, Cones, and Color-Coding in the Cortex , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[101]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[102]  B. Cumming,et al.  Decision-related activity in sensory neurons reflects more than a neuron’s causal effect , 2009, Nature.

[103]  Jeffrey W. Cooney,et al.  Hierarchical cognitive control deficits following damage to the human frontal lobe , 2009, Nature Neuroscience.

[104]  Asif A Ghazanfar,et al.  Interactions between the Superior Temporal Sulcus and Auditory Cortex Mediate Dynamic Face/Voice Integration in Rhesus Monkeys , 2008, The Journal of Neuroscience.

[105]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

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

[107]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[108]  Robert Oostenveld,et al.  Neural Mechanisms of Visual Attention : How Top-Down Feedback Highlights Relevant Locations , 2007 .

[109]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[110]  R. Kass,et al.  Multiple neural spike train data analysis: state-of-the-art and future challenges , 2004, Nature Neuroscience.

[111]  David Barber,et al.  The IM algorithm: a variational approach to Information Maximization , 2003, NIPS 2003.

[112]  G. Luppino,et al.  ß Federation of European Neuroscience Societies Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey , 2022 .

[113]  Jessica Lowell Neural Network , 2001 .

[114]  S. Wise,et al.  Arbitrary associations between antecedents and actions , 2000, Trends in Neurosciences.

[115]  Naftali Tishby,et al.  The information bottleneck method , 2000, ArXiv.

[116]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

[117]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

[118]  Roger Ratcliff,et al.  A Theory of Memory Retrieval. , 1978 .

[119]  D. Perkel,et al.  Simultaneously Recorded Trains of Action Potentials: Analysis and Functional Interpretation , 1969, Science.