Working Memory and Decision-Making in a Frontoparietal Circuit Model

Working memory (WM) and decision making (DM) are fundamental cognitive functions involving a distributed interacting network of brain areas, with the posterior parietal and prefrontal cortices (PPC and PFC) at the core. However, the shared and distinct roles of these areas and the nature of their coordination in cognitive function remain poorly understood. Biophysically-based computational models of cortical circuits have provided insights into the mechanisms supporting these functions, yet they have primarily focused on the local microcircuit level, raising questions about the principles for distributed cognitive computation in multi-regional networks. To examine these issues, we developed a distributed circuit model of two reciprocally interacting modules representing PPC and PFC circuits. The circuit architecture includes hierarchical differences in local recurrent structure and implements reciprocal long-range projections. This parsimonious model captures a range of behavioral and neuronal features of fronto-parietal circuits across multiple WM and DM paradigms. In the context of WM, both areas exhibit persistent activity, but in response to intervening distractors, PPC transiently encodes distractors, while PFC filters distractors and supports WM robustness. With regards to DM, the PPC module generates graded representations of accumulated evidence supporting target selection, while the PFC module generates more categorical responses related to action or choice. These findings suggest computational principles for distributed, hierarchical processing in cortex during cognitive function, and provide a framework for extension to multi-regional models.

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

[2]  Richard P. Heitz,et al.  Neural basis of the set-size effect in frontal eye field: timing of attention during visual search. , 2009, Journal of neurophysiology.

[3]  B Suresh Krishna,et al.  Spatial Representation and Cognitive Modulation of Response Variability in the Lateral Intraparietal Area Priority Map , 2013, The Journal of Neuroscience.

[4]  J. Schall,et al.  Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. , 1998, Journal of neurophysiology.

[5]  B Suresh Krishna,et al.  Surround Suppression Sharpens the Priority Map in the Lateral Intraparietal Area , 2022 .

[6]  E. Procyk,et al.  The primate working memory networks , 2004, Cognitive, affective & behavioral neuroscience.

[7]  Stephen J. Gotts,et al.  Cell-Type-Specific Synchronization of Neural Activity in FEF with V4 during Attention , 2012, Neuron.

[8]  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.

[9]  Ilya E Monosov,et al.  A perceptual representation in the frontal eye field during covert visual search that is more reliable than the behavioral report , 2008, The European journal of neuroscience.

[10]  Jay A. Hennig,et al.  Signal Multiplexing and Single-Neuron Computations in Lateral Intraparietal Area During Decision-Making , 2013, The Journal of Neuroscience.

[11]  Frances S. Chance,et al.  Drivers and modulators from push-pull and balanced synaptic input. , 2005, Progress in brain research.

[12]  J. Duncan,et al.  Filtering of neural signals by focused attention in the monkey prefrontal cortex , 2002, Nature Neuroscience.

[13]  C. Constantinidis,et al.  Early involvement of prefrontal cortex in visual bottom up attention , 2012, Nature Neuroscience.

[14]  Xiao-Jing Wang,et al.  Speed-accuracy tradeoff by a control signal with balanced excitation and inhibition. , 2015, Journal of neurophysiology.

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

[16]  Brian J. White,et al.  Separate Visual Signals for Saccade Initiation during Target Selection in the Primate Superior Colliculus , 2011, The Journal of Neuroscience.

[17]  M. Goldberg,et al.  Activity in the Lateral Intraparietal Area Predicts the Goal and Latency of Saccades in a Free-Viewing Visual Search Task , 2006, The Journal of Neuroscience.

[18]  G. Woodman,et al.  The Effect of Visual Search Efficiency on Response Preparation , 2008, Psychological science.

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

[20]  Jeffrey D Schall,et al.  Visuomotor Functions in the Frontal Lobe. , 2015, Annual review of vision science.

[21]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[22]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[23]  Jeffrey D Schall,et al.  Macrocircuits: Decision Networks This Review Comes from a Themed Issue on Macrocircuits Decide That — Categorization and Stimulus Selection , 2022 .

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

[25]  L.F. Abbott,et al.  Gating Multiple Signals through Detailed Balance of Excitation and Inhibition in Spiking Networks , 2009, Nature Neuroscience.

[26]  J. Duhamel,et al.  Differential effects of parietal and frontal inactivations on reaction times distributions in a visual search task , 2012, Front. Integr. Neurosci..

[27]  Nikolaus Weiskopf,et al.  Causal evidence for frontal involvement in memory target maintenance by posterior brain areas during distracter interference of visual working memory , 2011, Proceedings of the National Academy of Sciences.

[28]  M. Paré,et al.  Temporal processing of saccade targets in parietal cortex area LIP during visual search. , 2007, Journal of neurophysiology.

[29]  M. Goldberg,et al.  Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade. , 2000, Journal of neurophysiology.

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

[31]  Charles M Gray,et al.  Frontoparietal Correlation Dynamics Reveal Interplay between Integration and Segregation during Visual Working Memory , 2014, The Journal of Neuroscience.

[32]  M. Landy,et al.  The effect of viewpoint on perceived visual roughness. , 2007, Journal of vision.

[33]  E. Salinas,et al.  Differences in intrinsic functional organization between dorsolateral prefrontal and posterior parietal cortex. , 2014, Cerebral cortex.

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

[35]  Xiao-Jing Wang,et al.  Linking microcircuit dysfunction to cognitive impairment: effects of disinhibition associated with schizophrenia in a cortical working memory model. , 2014, Cerebral cortex.

[36]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

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

[38]  Bingni W. Brunton,et al.  Distinct relationships of parietal and prefrontal cortices to evidence accumulation , 2014, Nature.

[39]  R. Bogacz,et al.  The neural basis of the speed–accuracy tradeoff , 2010, Trends in Neurosciences.

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

[41]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[42]  Joaquín M. Fuster,et al.  Cortex and Memory: Emergence of a New Paradigm , 2009, Journal of Cognitive Neuroscience.

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

[44]  Suliann Ben Hamed,et al.  A Functional Hierarchy within the Parietofrontal Network in Stimulus Selection and Attention Control , 2013, The Journal of Neuroscience.

[45]  Jonathan W. Pillow,et al.  Dissociated functional significance of decision-related activity in the primate dorsal stream , 2016, Nature.

[46]  C. Constantinidis,et al.  Unique and shared roles of the posterior parietal and dorsolateral prefrontal cortex in cognitive functions , 2012, Front. Integr. Neurosci..

[47]  Kenneth D. Miller,et al.  Coupling between One-Dimensional Networks Reconciles Conflicting Dynamics in LIP and Reveals Its Recurrent Circuitry , 2017, Neuron.

[48]  Jonathan D. Cohen,et al.  The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. , 2006, Psychological review.

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

[50]  E. Salinas,et al.  Perceptual decision making in less than 30 milliseconds , 2010, Nature Neuroscience.

[51]  Xiao-Jing Wang,et al.  A dendritic disinhibitory circuit mechanism for pathway-specific gating , 2016, Nature Communications.

[52]  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.

[53]  KongFatt Wong-Lin,et al.  Neural Circuit Dynamics Underlying Accumulation of Time-Varying Evidence During Perceptual Decision Making , 2007, Frontiers Comput. Neurosci..

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

[55]  E. Keller,et al.  Saccade target selection in the superior colliculus during a visual search task. , 2002, Journal of neurophysiology.

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

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

[58]  Takashi R Sato,et al.  Effects of Stimulus-Response Compatibility on Neural Selection in Frontal Eye Field , 2003, Neuron.

[59]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[60]  Lawrence H Snyder,et al.  Delay-period activity in visual, visuomovement, and movement neurons in the frontal eye field. , 2005, Journal of neurophysiology.

[61]  Jeffrey D. Schall,et al.  Neural basis of deciding, choosing and acting , 2001, Nature Reviews Neuroscience.

[62]  Xiao-Jing Wang,et al.  Probabilistic Decision Making by Slow Reverberation in Cortical Circuits , 2002, Neuron.

[63]  J. Gottlieb,et al.  Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe , 2012, Nature Neuroscience.

[64]  R. Wurtz,et al.  Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. , 2002, Journal of neurophysiology.

[65]  Etienne Koechlin,et al.  The Neuro-Computational Architecture of Value-Based Selection in the Human Brain , 2017, Cerebral cortex.

[66]  J. Schall,et al.  Neural selection and control of visually guided eye movements. , 1999, Annual review of neuroscience.

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

[68]  X. Wang,et al.  Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory , 1999, The Journal of Neuroscience.

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

[70]  Robert Clewley,et al.  Hybrid Models and Biological Model Reduction with PyDSTool , 2012, PLoS Comput. Biol..

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

[72]  M. Paré,et al.  Neuronal activity in superior colliculus signals both stimulus identity and saccade goals during visual conjunction search. , 2007, Journal of vision.

[73]  Ranulfo Romo,et al.  Flexible Control of Mutual Inhibition: A Neural Model of Two-Interval Discrimination , 2005, Science.

[74]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[75]  Xiao-Jing Wang,et al.  Reconciling Coherent Oscillation with Modulationof Irregular Spiking Activity in Selective Attention:Gamma-Range Synchronization between Sensoryand Executive Cortical Areas , 2010, The Journal of Neuroscience.

[76]  Martin Paré,et al.  Persistent storage capability impairs decision making in a biophysical network model , 2011, Neural Networks.

[77]  Christos Constantinidis,et al.  A Neural Circuit Basis for Spatial Working Memory , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[78]  N. P. Bichot,et al.  Frontal eye field activity before visual search errors reveals the integration of bottom-up and top-down salience. , 2005, Journal of neurophysiology.

[79]  Richard P. Heitz,et al.  Neural Mechanisms of Speed-Accuracy Tradeoff , 2012, Neuron.

[80]  Daniel J Mitchell,et al.  A Putative Multiple-Demand System in the Macaque Brain , 2016, The Journal of Neuroscience.

[81]  J. Schall,et al.  Visual and Motor Connectivity and the Distribution of Calcium-Binding Proteins in Macaque Frontal Eye Field: Implications for Saccade Target Selection , 2009, Front. Neuroanat..

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

[83]  Jesper Tegnér,et al.  Mechanism for top-down control of working memory capacity , 2009, Proceedings of the National Academy of Sciences.

[84]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

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

[86]  Xiao-Jing Wang,et al.  Similarity Effect and Optimal Control of Multiple-Choice Decision Making , 2008, Neuron.

[87]  Rodrigo F. Salazar,et al.  Content-Specific Fronto-Parietal Synchronization During Visual Working Memory , 2012, Science.

[88]  P. Goldman-Rakic,et al.  Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Takashi R Sato,et al.  Search Efficiency but Not Response Interference Affects Visual Selection in Frontal Eye Field , 2001, Neuron.

[90]  Christos Constantinidis,et al.  Comparison of Neural Activity Related to Working Memory in Primate Dorsolateral Prefrontal and Posterior Parietal Cortex , 2010, Front. Syst. Neurosci..

[91]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[92]  Etienne Olivier,et al.  A Deficit in Covert Attention after Parietal Cortex Inactivation in the Monkey , 2004, Neuron.

[93]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[94]  Richard P. Heitz,et al.  Biophysical support for functionally distinct cell types in the frontal eye field. , 2009, Journal of neurophysiology.

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

[96]  Richard P. Heitz,et al.  Neurally constrained modeling of perceptual decision making. , 2010, Psychological review.

[97]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[98]  Xiao-Jing Wang The Prefrontal Cortex as a Quintessential “Cognitive-Type” Neural Circuit , 2013 .

[99]  David J. Freedman,et al.  A hierarchy of intrinsic timescales across primate cortex , 2014, Nature Neuroscience.

[100]  J. Duhamel,et al.  Saccadic Target Selection Deficits after Lateral Intraparietal Area Inactivation in Monkeys , 2002, The Journal of Neuroscience.

[101]  Matthew T. Kaufman,et al.  A category-free neural population supports evolving demands during decision-making , 2014, Nature Neuroscience.

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

[103]  Jacqueline Gottlieb,et al.  Neuronal Correlates of the Set-Size Effect in Monkey Lateral Intraparietal Area , 2008, PLoS biology.

[104]  H. Kennedy,et al.  A Large-Scale Circuit Mechanism for Hierarchical Dynamical Processing in the Primate Cortex , 2015, Neuron.

[105]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[106]  P. Roelfsema,et al.  The Distributed Nature of Working Memory , 2017, Trends in Cognitive Sciences.

[107]  Gunnar Blohm,et al.  On the neural implementation of the speed-accuracy trade-off , 2014, Front. Neurosci..

[108]  Timothy D. Hanks,et al.  Neural underpinnings of the evidence accumulator , 2016, Current Opinion in Neurobiology.