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From Distributed Resources to Limited Slots in Multiple-Item Working Memory: A Spiking Network Model with Normalization

  1. Da-Hui Wang1,2
  1. 1Department of Systems Science and National Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China,
  2. 2Department of Neurobiology and Kavli Institute for Neuroscience, Yale University School of Medicine, New Haven, Connecticut 06510,
  3. 3The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University, Baltimore, Maryland 21205, and
  4. 4Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147
  1. Author contributions: Z.W., X.-J.W., and D.-H.W. designed research; Z.W. and D.-H.W. performed research; Z.W. and D.-H.W. contributed unpublished reagents/analytic tools; Z.W., X.-J.W., and D.-H.W. analyzed data; Z.W., X.-J.W., and D.-H.W. wrote the paper.

Abstract

Recent behavioral studies have given rise to two contrasting models for limited working memory capacity: a “discrete-slot” model in which memory items are stored in a limited number of slots, and a “shared-resource” model in which the neural representation of items is distributed across a limited pool of resources. To elucidate the underlying neural processes, we investigated a continuous network model for working memory of an analog feature. Our model network fundamentally operates with a shared resource mechanism, and stimuli in cue arrays are encoded by a distributed neural population. On the other hand, the network dynamics and performance are also consistent with the discrete-slot model, because multiple objects are maintained by distinct localized population persistent activity patterns (bump attractors). We identified two phenomena of recurrent circuit dynamics that give rise to limited working memory capacity. As the working memory load increases, a localized persistent activity bump may either fade out (so the memory of the corresponding item is lost) or merge with another nearby bump (hence the resolution of mnemonic representation for the merged items becomes blurred). We identified specific dependences of these two phenomena on the strength and tuning of recurrent synaptic excitation, as well as network normalization: the overall population activity is invariant to set size and delay duration; therefore, a constant neural resource is shared by and dynamically allocated to the memorized items. We demonstrate that the model reproduces salient observations predicted by both discrete-slot and shared-resource models, and propose testable predictions of the merging phenomenon.

  • Received February 15, 2012.
  • Revision received May 31, 2012.
  • Accepted June 27, 2012.

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