Cortical circuit-based lossless neural integrator for perceptual decision-making: A computational modeling study

The intrinsic uncertainty of sensory information (i.e., evidence) does not necessarily deter an observer from making a reliable decision. Indeed, uncertainty can be reduced by integrating (accumulating) incoming sensory evidence. It is widely thought that this accumulation is instantiated via recurrent rate-code neural networks. Yet, these networks do not fully explain important aspects of perceptual decision-making, such as a subject’s ability to retain accumulated evidence during temporal gaps in the sensory evidence. Here, we utilized computational models to show that cortical circuits can switch flexibly between ‘retention’ and ‘integration’ modes during perceptual decision-making. Further, we found that, depending on how the sensory evidence was readout, we could simulate ‘stepping’ and ‘ramping’ activity patterns, which may be analogous to those seen in different studies of decision-making in the primate parietal cortex. This finding may reconcile these previous empirical studies because it suggests these two activity patterns emerge from the same mechanism.

[1]  Kenneth D. Miller,et al.  Mathematical Equivalence of Two Common Forms of Firing Rate Models of Neural Networks , 2012, Neural Computation.

[2]  G. Fishell,et al.  Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons , 2011, Developmental neurobiology.

[3]  Henry Markram,et al.  Coding of temporal information by activity-dependent synapses. , 2002, Journal of neurophysiology.

[4]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[5]  Roozbeh Kiani,et al.  Integration of Direction Cues Is Invariant to the Temporal Gap between Them , 2013, The Journal of Neuroscience.

[6]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[7]  H. Adesnik,et al.  A neural circuit for spatial summation in visual cortex , 2012, Nature.

[8]  Daniel M. Wolpert,et al.  Comment on “Single-trial spike trains in parietal cortex reveal discrete steps during decision-making” , 2016, Science.

[9]  Y. Dan,et al.  Long-range and local circuits for top-down modulation of visual cortex processing , 2014, Science.

[10]  Marc-Oliver Gewaltig,et al.  NEST (NEural Simulation Tool) , 2007, Scholarpedia.

[11]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[12]  Y. Dan,et al.  Activity Recall in Visual Cortical Ensemble , 2012, Nature Neuroscience.

[13]  J. Gold,et al.  Neural correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field. , 2012, Cerebral cortex.

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

[15]  James L. McClelland,et al.  The time course of perceptual choice: the leaky, competing accumulator model. , 2001, Psychological review.

[16]  Thomas K. Berger,et al.  A synaptic organizing principle for cortical neuronal groups , 2011, Proceedings of the National Academy of Sciences.

[17]  Xiao-Jing Wang,et al.  Angular Path Integration by Moving “Hill of Activity”: A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System , 2005, The Journal of Neuroscience.

[18]  Tomoki Fukai,et al.  Layer-Dependent Attentional Processing by Top-down Signals in a Visual Cortical Microcircuit Model , 2011, Front. Comput. Neurosci..

[19]  Andrew D Huberman,et al.  Diverse Visual Features Encoded in Mouse Lateral Geniculate Nucleus , 2013, The Journal of Neuroscience.

[20]  Roger Ratcliff,et al.  The Diffusion Decision Model: Theory and Data for Two-Choice Decision Tasks , 2008, Neural Computation.

[21]  David Golomb,et al.  LTS and FS Inhibitory Interneurons, Short-Term Synaptic Plasticity, and Cortical Circuit Dynamics , 2011, PLoS Comput. Biol..

[22]  W T Newsome,et al.  Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task. , 2001, Journal of neurophysiology.

[23]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[24]  Joshua I. Gold,et al.  Temporal Integration of Auditory Information Is Invariant to Temporal Grouping Cues,, , 2015, eNeuro.

[25]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

[26]  Bruce L. McNaughton,et al.  A Model of the Neural Basis of the Rat's Sense of Direction , 1994, NIPS.

[27]  S. Romani,et al.  Short‐term plasticity based network model of place cells dynamics , 2015, Hippocampus.

[28]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[30]  John M. Beggs,et al.  Behavioral / Systems / Cognitive Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures , 2004 .

[31]  E. Rolls,et al.  Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. , 2002 .

[32]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[33]  Dohoung Kim,et al.  Distinct Roles of Parvalbumin- and Somatostatin-Expressing Interneurons in Working Memory , 2016, Neuron.

[34]  H. Markram,et al.  Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells , 2007, Neuron.

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

[36]  John M. Beggs,et al.  A Maximum Entropy Model Applied to Spatial and Temporal Correlations from Cortical Networks In Vitro , 2008, The Journal of Neuroscience.

[37]  P. Miller,et al.  Stochastic Transitions between Neural States in Taste Processing and Decision-Making , 2010, The Journal of Neuroscience.

[38]  Tobias C. Potjans,et al.  The Cell-Type Specific Cortical Microcircuit: Relating Structure and Activity in a Full-Scale Spiking Network Model , 2012, Cerebral cortex.

[39]  Gustavo Deco,et al.  Computational significance of transient dynamics in cortical networks , 2007, The European journal of neuroscience.

[40]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

[41]  E. Seidemann,et al.  Simultaneously recorded single units in the frontal cortex go through sequences of discrete and stable states in monkeys performing a delayed localization task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  C. Petersen,et al.  Layer-Dependent Short-Term Synaptic Plasticity Between Excitatory Neurons in the C2 Barrel Column of Mouse Primary Somatosensory Cortex , 2017, Cerebral cortex.

[43]  Xiao-Jing Wang Neural dynamics and circuit mechanisms of decision-making , 2012, Current Opinion in Neurobiology.

[44]  T. Collett,et al.  Animal Navigation: Path Integration, Visual Landmarks and Cognitive Maps , 2004, Current Biology.

[45]  Tatsuo K Sato,et al.  Traveling Waves in Visual Cortex , 2012, Neuron.

[46]  F. Pulvermüller,et al.  Spatiotemporal Signatures of Large-Scale Synfire Chains for Speech Processing as Revealed by MEG , 2008, Cerebral cortex.

[47]  Alessandro Treves,et al.  A model for the differentiation between grid and conjunctive units in medial entorhinal cortex , 2013, Hippocampus.

[48]  B. Connors,et al.  Two dynamically distinct inhibitory networks in layer 4 of the neocortex. , 2003, Journal of neurophysiology.

[49]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[50]  Jonathan W. Pillow,et al.  Single-trial spike trains in parietal cortex reveal discrete steps during decision-making , 2015, Science.

[51]  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.

[52]  C. Clopath,et al.  The emergence of functional microcircuits in visual cortex , 2013, Nature.

[53]  D. LaBerge A recruitment theory of simple behavior , 1962 .

[54]  E. Miller,et al.  Task-Dependent Changes in Short-Term Memory in the Prefrontal Cortex , 2010, The Journal of Neuroscience.

[55]  David Terman,et al.  Mathematical foundations of neuroscience , 2010 .

[56]  C. Petersen,et al.  Short-term dynamics of synaptic transmission within the excitatory neuronal network of rat layer 4 barrel cortex. , 2002, Journal of neurophysiology.

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

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

[59]  S. Epstein,et al.  Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model , 2008, Proceedings of the National Academy of Sciences.

[60]  Eric Shea-Brown,et al.  Neural integrators for decision making: a favorable tradeoff between robustness and sensitivity , 2011, Journal of neurophysiology.

[61]  Patrice Perny,et al.  Decision-making models , 1998 .

[62]  Mark C. W. van Rossum,et al.  Recurrent networks with short term synaptic depression , 2009, Journal of Computational Neuroscience.

[63]  Li I. Zhang,et al.  Visual Representations by Cortical Somatostatin Inhibitory Neurons—Selective But with Weak and Delayed Responses , 2010, The Journal of Neuroscience.

[64]  Albert Compte,et al.  Neural Integrator Models , 2009 .

[65]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[66]  A. Reyes,et al.  Linking the Response Properties of Cells in Auditory Cortex with Network Architecture: Cotuning versus Lateral Inhibition , 2008, The Journal of Neuroscience.

[67]  J. Gold,et al.  Caudate Encodes Multiple Computations for Perceptual Decisions , 2010, The Journal of Neuroscience.

[68]  Alexander S. Ecker,et al.  Principles of connectivity among morphologically defined cell types in adult neocortex , 2015, Science.

[69]  Claire E. J. Cheetham,et al.  Presynaptic Development at L4 to L2/3 Excitatory Synapses Follows Different Time Courses in Visual and Somatosensory Cortex , 2010, The Journal of Neuroscience.

[70]  Philip L. Smith,et al.  A comparison of sequential sampling models for two-choice reaction time. , 2004, Psychological review.

[71]  Peter Jonas,et al.  Fast-spiking, parvalbumin+ GABAergic interneurons: From cellular design to microcircuit function , 2014, Science.

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

[73]  M. Shadlen,et al.  A role for neural integrators in perceptual decision making. , 2003, Cerebral cortex.

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

[75]  Xiao-Jing Wang,et al.  An Integrated Microcircuit Model of Attentional Processing in the Neocortex , 2007, The Journal of Neuroscience.

[76]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[77]  Philip L. Smith,et al.  Psychology and neurobiology of simple decisions , 2004, Trends in Neurosciences.

[78]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[79]  E. Miller,et al.  Gamma and Beta Bursts Underlie Working Memory , 2016, Neuron.

[80]  Russell L. De Valois,et al.  PII: S0042-6989(00)00210-8 , 2000 .

[81]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.