Circuit mechanisms for the maintenance and manipulation of information in working memory

Recently it has been proposed that information in working memory (WM) may not always be stored in persistent neuronal activity but can be maintained in ‘activity-silent’ hidden states, such as synaptic efficacies endowed with short-term synaptic plasticity. To test this idea computationally, we investigated recurrent neural network models trained to perform several WM-dependent tasks, in which WM representation emerges from learning and is not a priori assumed to depend on self-sustained persistent activity. We found that short-term synaptic plasticity can support the short-term maintenance of information, provided that the memory delay period is sufficiently short. However, in tasks that require actively manipulating information, persistent activity naturally emerges from learning, and the amount of persistent activity scales with the degree of manipulation required. These results shed insight into the current debate on WM encoding and suggest that persistent activity can vary markedly between short-term memory tasks with different cognitive demands. The role of persistent spiking activity in working memory has recently come under debate. Here the authors use biologically realistic recurrent neural networks to explain why the strength of persistent activity can vary markedly between tasks.

[1]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[2]  Joel Z. Leibo,et al.  Prefrontal cortex as a meta-reinforcement learning system , 2018, bioRxiv.

[3]  Stan B. Floresco,et al.  Thalamic–Cortical–Striatal Circuitry Subserves Working Memory during Delayed Responding on a Radial Arm Maze , 1999, The Journal of Neuroscience.

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

[5]  C. Koch,et al.  Persistent Single-Neuron Activity during Working Memory in the Human Medial Temporal Lobe , 2017, Current Biology.

[6]  Devika Narain,et al.  Flexible timing by temporal scaling of cortical responses , 2017, Nature Neuroscience.

[7]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[8]  J. Gordon,et al.  Thalamic projections sustain prefrontal activity during working memory maintenance , 2017, Nature Neuroscience.

[9]  Jonathan D. Wallis,et al.  Executive control processes underlying multi-item working memory , 2014, Nature Neuroscience.

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

[11]  Elias B. Issa,et al.  Neural dynamics at successive stages of the ventral visual stream are consistent with hierarchical error signals , 2018, eLife.

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

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

[14]  M. Stokes ‘Activity-silent’ working memory in prefrontal cortex: a dynamic coding framework , 2015, Trends in Cognitive Sciences.

[15]  S. Funahashi,et al.  Neural mechanisms of dual-task interference and cognitive capacity limitation in the prefrontal cortex , 2014, Nature Neuroscience.

[16]  Kartik K. Sreenivasan,et al.  Revisiting the role of persistent neural activity during working memory , 2014, Trends in Cognitive Sciences.

[17]  Julio C. Martinez-Trujillo,et al.  Sharp emergence of feature-selective sustained activity along the dorsal visual pathway , 2014, Nature Neuroscience.

[18]  B. Postle,et al.  Superior Parietal Cortex Is Critical for the Manipulation of Information in Working Memory , 2009, The Journal of Neuroscience.

[19]  Sebastian Schneegans,et al.  Restoration of fMRI Decodability Does Not Imply Latent Working Memory States , 2017, Journal of Cognitive Neuroscience.

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

[21]  Bruno A Olshausen,et al.  Sparse coding of sensory inputs , 2004, Current Opinion in Neurobiology.

[22]  Dwight J. Kravitz,et al.  Goal-dependent dissociation of visual and prefrontal cortices during working memory , 2013, Nature Neuroscience.

[23]  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.

[24]  Markus Siegel,et al.  Neural substrates of cognitive capacity limitations , 2011, Proceedings of the National Academy of Sciences.

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

[26]  Elkan G. Akyürek,et al.  Dynamic hidden states underlying working memory guided behaviour , 2017, Nature Neuroscience.

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

[28]  Stanislas Dehaene,et al.  Probing the limits of activity-silent non-conscious working memory , 2018, Proceedings of the National Academy of Sciences.

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

[30]  Nicolas Y. Masse,et al.  Mnemonic Encoding and Cortical Organization in Parietal and Prefrontal Cortices , 2017, The Journal of Neuroscience.

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

[32]  S. Funahashi,et al.  Population vector analysis of primate prefrontal activity during spatial working memory. , 2004, Cerebral cortex.

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

[34]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[35]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

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

[37]  Jürgen Schmidhuber,et al.  Long Short-Term Memory , 1997, Neural Computation.

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

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

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

[41]  James J. DiCarlo,et al.  Author response: Neural dynamics at successive stages of the ventral visual stream are consistent with hierarchical error signals , 2018 .

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

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

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

[45]  J. Morrison,et al.  NMDA Receptors Subserve Persistent Neuronal Firing during Working Memory in Dorsolateral Prefrontal Cortex , 2013, Neuron.

[46]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[47]  Adam C. Riggall,et al.  Reactivation of latent working memories with transcranial magnetic stimulation , 2016, Science.

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

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

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

[51]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.