Error-correcting dynamics in visual working memory

Working memory is critical to cognition, decoupling behavior from the immediate world. Yet, it is imperfect; internal noise introduces errors into memory representations. Such errors have been shown to accumulate over time and increase with the number of items simultaneously held in working memory. Here, we show that discrete attractor dynamics mitigate the impact of noise on working memory. These dynamics pull memories towards a few stable representations in mnemonic space, inducing a bias in memory representations but reducing the effect of random diffusion. Model-based and model-free analyses of human and monkey behavior show that discrete attractor dynamics account for the distribution, bias, and precision of working memory reports. Furthermore, attractor dynamics are adaptive. They increase in strength as noise increases with memory load and experiments in humans show these dynamics adapt to the statistics of the environment, such that memories drift towards contextually-predicted values. Together, our results suggest attractor dynamics mitigate errors in working memory by counteracting noise and integrating contextual information into memories. Neural representations in working memory are susceptible to internal noise, which scales with memory load. Here, the authors show that attractor dynamics mitigate the influence of internal noise by pulling memories towards a few stable representations.

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

[2]  Jonathan D. Cohen,et al.  Constraints associated with cognitive control and the stability-flexibility dilemma , 2018, CogSci.

[3]  S. Luck,et al.  Sudden Death and Gradual Decay in Visual Working Memory , 2009, Psychological science.

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

[5]  Ranulfo Romo,et al.  Basic mechanisms for graded persistent activity: discrete attractors, continuous attractors, and dynamic representations , 2003, Current Opinion in Neurobiology.

[6]  Timothy F. Brady,et al.  Hierarchical Encoding in Visual Working Memory , 2010, Psychological science.

[7]  Sergej N. Yendrikhovskij,et al.  Computing Color Categories from Statistics of Natural Images , 2001, Journal of Imaging Science and Technology.

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

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

[10]  Masud Husain,et al.  Rapid Forgetting Results From Competition Over Time Between Items in Visual Working Memory , 2016, Journal of experimental psychology. Learning, memory, and cognition.

[11]  R. O’Reilly,et al.  Discrete Representations in Working Memory : A Hypothesis and Computational Investigations , 1999 .

[12]  Frank Tong,et al.  Accounting for Stimulus-Specific Variation in Precision Reveals a Discrete Capacity Limit in Visual Working Memory , 2017, Journal of experimental psychology. Human perception and performance.

[13]  Rishidev Chaudhuri,et al.  Computational principles of memory , 2016, Nature Neuroscience.

[14]  Evie Vergauwe,et al.  Categorical Working Memory Representations Are Used in Delayed Estimation of Continuous Colors , 2017, Journal of experimental psychology. Human perception and performance.

[15]  Flora Bouchacourt,et al.  A Flexible Model of Working Memory , 2019, Neuron.

[16]  Paul M Bays,et al.  Temporal dynamics of encoding, storage, and reallocation of visual working memory. , 2011, Journal of vision.

[17]  James L. McClelland,et al.  On the control of automatic processes: a parallel distributed processing account of the Stroop effect. , 1990, Psychological review.

[18]  Onur Ozan Koyluoglu,et al.  Fundamental bound on the persistence and capacity of short-term memory stored as graded persistent activity , 2017, eLife.

[19]  Edward Awh,et al.  Clear evidence for item limits in visual working memory , 2017, Cognitive Psychology.

[20]  Yoram Burak,et al.  Fundamental limits on persistent activity in networks of noisy neurons , 2012, Proceedings of the National Academy of Sciences.

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

[22]  Jonathan I. Flombaum,et al.  Stimulus-specific variability in color working memory with delayed estimation. , 2014, Journal of vision.

[23]  Timothy F. Brady,et al.  Contextual effects in visual working memory reveal hierarchically structured memory representations. , 2015, Journal of vision.

[24]  Paul M Bays,et al.  Drift in Neural Population Activity Causes Working Memory to Deteriorate Over Time , 2018, The Journal of Neuroscience.

[25]  Charles D. Kopec,et al.  Posterior parietal cortex represents sensory history and mediates its effects on behaviour , 2017, Nature.

[26]  Wei Ji Ma,et al.  The effects of delay duration on visual working memory for orientation , 2017, Journal of vision.

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

[28]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Gavan P. McNally,et al.  Visualizing Infralimbic Control over Incubation of Cocaine Craving , 2019, Neuron.

[30]  E. Wagenmakers,et al.  AIC model selection using Akaike weights , 2004, Psychonomic bulletin & review.

[31]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[32]  GeniusMoon 2010 Looking back and looking forward , 2010 .

[33]  Frank Tong,et al.  Evidence of Gradual Loss of Precision for Simple Features and Complex Objects in Visual Working Memory , 2018, Journal of experimental psychology. Human perception and performance.

[34]  Jonathan I. Flombaum,et al.  Why some colors appear more memorable than others: A model combining categories and particulars in color working memory. , 2015, Journal of experimental psychology. General.

[35]  Edward K. Vogel,et al.  The capacity of visual working memory for features and conjunctions , 1997, Nature.

[36]  Carlos D. Brody,et al.  Rat Prefrontal Cortex Inactivations during Decision Making Are Explained by Bistable Attractor Dynamics , 2017, Neural Computation.

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

[38]  Zachary P. Kilpatrick Synaptic mechanisms of interference in working memory , 2017 .

[39]  Earl K. Miller Faculty Opinions recommendation of Spikes not slots: noise in neural populations limits working memory. , 2015 .

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

[41]  John J. Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities , 1999 .

[42]  James L. McClelland,et al.  Automaticity , Attention and the Strength of Processing : A Parallel Distributed Processing Account of the Stroop Effect , 2001 .

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

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

[45]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[46]  Brent Doiron,et al.  Optimizing Working Memory with Heterogeneity of Recurrent Cortical Excitation , 2013, The Journal of Neuroscience.

[47]  Manabu Iguchi,et al.  Entry of inclined hydrophobic and hydrophilic circular cylinders into water , 2011, J. Vis..

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

[49]  Sandro Romani,et al.  Discrete attractor dynamics underlies persistent activity in the frontal cortex , 2019, Nature.

[50]  Gerald Westheimer,et al.  Quantifying target conspicuity in contextual modulation by visual search. , 2011, Journal of vision.

[51]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[52]  Julie C. Helmers,et al.  Chunking as a rational strategy for lossy data compression in visual working memory , 2017, bioRxiv.

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

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

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