Synaptic augmentation in a cortical circuit model reproduces serial dependence in visual working memory

Recent work has established that visual working memory is subject to serial dependence: current information in memory blends with that from the recent past as a function of their similarity. This tuned temporal smoothing likely promotes the stability of memory in the face of noise and occlusion. Serial dependence accumulates over several seconds in memory and deteriorates with increased separation between trials. While this phenomenon has been extensively characterized in behavior, its neural mechanism is unknown. In the present study, we investigate the circuit-level origins of serial dependence in a biophysical model of cortex. We explore two distinct kinds of mechanisms: stable persistent activity during the memory delay period and dynamic “activity-silent” synaptic plasticity. We find that networks endowed with both strong reverberation to support persistent activity and dynamic synapses can closely reproduce behavioral serial dependence. Specifically, elevated activity drives synaptic augmentation, which biases activity on the subsequent trial, giving rise to a spatiotemporally tuned shift in the population response. Our hybrid neural model is a theoretical advance beyond abstract mathematical characterizations, offers testable hypotheses for physiological research, and demonstrates the power of biological insights to provide a quantitative explanation of human behavior.

[1]  Paul M Bays,et al.  Evaluating and excluding swap errors in analogue tests of working memory , 2016, Scientific Reports.

[2]  D. Whitney,et al.  Serial dependence in visual perception , 2011 .

[3]  S. Funahashi Functions of delay-period activity in the prefrontal cortex and mnemonic scotomas revisited , 2015, Front. Syst. Neurosci..

[4]  Charalampos Papadimitriou,et al.  Ghosts in the Machine II: Neural Correlates of Memory Interference from the Previous Trial , 2016, Cerebral cortex.

[5]  Xiao-Jing Wang,et al.  Robust Spatial Working Memory through Homeostatic Synaptic Scaling in Heterogeneous Cortical Networks , 2003, Neuron.

[6]  S. Nelson,et al.  Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. , 2000, Journal of neurophysiology.

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

[8]  P. Bays Spikes not slots: noise in neural populations limits working memory , 2015, Trends in Cognitive Sciences.

[9]  A. Compte,et al.  Neural circuit basis of visuo-spatial working memory precision: a computational and behavioral study. , 2015, Journal of neurophysiology.

[10]  Romain Brette,et al.  Equation-oriented specification of neural models for simulations , 2013, Front. Neuroinform..

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

[12]  David Whitney,et al.  Facilitating Stable Representations: Serial Dependence in Vision , 2011, PloS one.

[13]  Paul M Bays,et al.  Dynamic Shifts of Limited Working Memory Resources in Human Vision , 2008, Science.

[14]  M. R. Riley,et al.  Role of Prefrontal Persistent Activity in Working Memory , 2016, Front. Syst. Neurosci..

[15]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[16]  L. M. Ward Mixed-modality psychophysical scaling: Inter- and intramodality sequential dependencies as a function of lag , 1985, Perception & psychophysics.

[17]  W. Ma,et al.  Changing concepts of working memory , 2014, Nature Neuroscience.

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

[19]  Daniel P. Bliss,et al.  Serial Dependence across Perception, Attention, and Memory , 2017, Trends in Cognitive Sciences.

[20]  R. Sekuler,et al.  Distortions in recall from visual memory: two classes of attractors at work. , 2010, Journal of vision.

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

[22]  David Whitney,et al.  Serial dependence in the perception of attractiveness , 2015, Journal of vision.

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

[24]  Paul M. Bays,et al.  A signature of neural coding at human perceptual limits , 2016, bioRxiv.

[25]  D. Whitney,et al.  Serial Dependence in the Perception of Faces , 2014, Current Biology.

[26]  Xiao-Jing Wang,et al.  Cannabinoid-mediated disinhibition and working memory: dynamical interplay of multiple feedback mechanisms in a continuous attractor model of prefrontal cortex. , 2007, Cerebral cortex.

[27]  F. D. Lange,et al.  Opposite Effects of Recent History on Perception and Decision , 2017, Current Biology.

[28]  Katsumi Watanabe,et al.  Influence of gender membership on sequential decisions of face attractiveness , 2013, Attention, Perception, & Psychophysics.

[29]  David J. Freedman,et al.  Choice-correlated activity fluctuations underlie learning of neuronal category representation , 2015, Nature Communications.

[30]  Yang Dan,et al.  Dynamic Modification of Cortical Orientation Tuning Mediated by Recurrent Connections , 2002, Neuron.

[31]  Misha Tsodyks,et al.  Persistent Activity in Neural Networks with Dynamic Synapses , 2007, PLoS Comput. Biol..

[32]  G. Stanley,et al.  Rapid Sensory Adaptation Redux: A Circuit Perspective , 2016, Neuron.

[33]  Carson C. Chow,et al.  Variability in neuronal activity in primate cortex during working memory tasks , 2007, Neuroscience.

[34]  S. Luck,et al.  Discrete fixed-resolution representations in visual working memory , 2008, Nature.

[35]  Xiao-Jing Wang,et al.  Downstream Effect of Ramping Neuronal Activity through Synapses with Short-Term Plasticity , 2016, Neural Computation.

[36]  Eric Jones,et al.  SciPy: Open Source Scientific Tools for Python , 2001 .

[37]  W. Ma,et al.  Factorial comparison of working memory models. , 2014, Psychological review.

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

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

[40]  W. Ma,et al.  A detection theory account of change detection. , 2004, Journal of vision.

[41]  Xiao-Jing Wang,et al.  From Distributed Resources to Limited Slots in Multiple-Item Working Memory: A Spiking Network Model with Normalization , 2012, The Journal of Neuroscience.

[42]  A. Nobre,et al.  Prioritizing Information during Working Memory: Beyond Sustained Internal Attention , 2017, Trends in Cognitive Sciences.

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

[44]  L. Abbott,et al.  Synaptic computation , 2004, Nature.

[45]  E. Vogel,et al.  Visual working memory capacity: from psychophysics and neurobiology to individual differences , 2013, Trends in Cognitive Sciences.

[46]  Kohske Takahashi,et al.  Sequential Effects in Face-Attractiveness Judgment , 2012, Perception.

[47]  P. Petzold,et al.  The influence of category membership of stimuli on sequential effects in magnitude judgment , 2004, Perception & psychophysics.

[48]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

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

[50]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[51]  Paul M Bays,et al.  The precision of visual working memory is set by allocation of a shared resource. , 2009, Journal of vision.

[52]  G. Woodman,et al.  Voluntary and automatic attentional control of visual working memory , 2002 .

[53]  Paul M Bays,et al.  Noise in Neural Populations Accounts for Errors in Working Memory , 2014, The Journal of Neuroscience.

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

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

[56]  D. Whitney,et al.  Serial dependence promotes object stability during occlusion , 2016, Journal of vision.

[57]  M. Tsodyks,et al.  Working models of working memory , 2014, Current Opinion in Neurobiology.

[58]  Daniel P. Bliss,et al.  Serial dependence is absent at the time of perception but increases in visual working memory , 2017, bioRxiv.

[59]  Charalampos Papadimitriou,et al.  Ghosts in the machine: memory interference from the previous trial. , 2015, Journal of neurophysiology.

[60]  R. Romo,et al.  Neuronal Population Coding of Parametric Working Memory , 2010, The Journal of Neuroscience.

[61]  Lawrence M. Ward,et al.  Response system processes in absolute judgment , 1971 .

[62]  Wei Ji Ma,et al.  Variability in encoding precision accounts for visual short-term memory limitations , 2012, Proceedings of the National Academy of Sciences.

[63]  R. Romo,et al.  Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. , 2003, Cerebral cortex.

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

[65]  David Alais,et al.  Different coding strategies for the perception of stable and changeable facial attributes , 2016, Scientific Reports.

[66]  Thomas K. Berger,et al.  Heterogeneity in the pyramidal network of the medial prefrontal cortex , 2006, Nature Neuroscience.

[67]  George A. Alvarez,et al.  Variability in the quality of visual working memory , 2012, Nature Communications.

[68]  Justus-Liebig-University Giessen,et al.  Higher order sequential effects in psychophysical judgments , 2010 .

[69]  T. Foulsham,et al.  The where, what and when of gaze allocation in the lab and the natural environment , 2011, Vision Research.

[70]  Tatiana A. Engel,et al.  Same or Different? A Neural Circuit Mechanism of Similarity-Based Pattern Match Decision Making , 2011, The Journal of Neuroscience.

[71]  D. Burr,et al.  Compressive mapping of number to space reflects dynamic encoding mechanisms, not static logarithmic transform , 2014, Proceedings of the National Academy of Sciences.