Efficient Coding in Visual Working Memory Accounts for Stimulus-Specific Variations in Recall

J Neurosci. 2018 Aug 8;38(32):7132-7142. doi: 10.1523/JNEUROSCI.1018-18.2018. Epub 2018 Jul 13.

Abstract

Recall of visual features from working memory varies in both bias and precision depending on stimulus parameters. Whereas a number of models can approximate the average distribution of recall error across target stimuli, attempts to model how error varies with the choice of target have been ad hoc Here we adapt a neural model of working memory to provide a principled account of these stimulus-specific effects, by allowing each neuron's tuning function to vary according to the principle of efficient coding, which states that neural responses should be optimized with respect to the frequency of stimuli in nature. For orientation, this means incorporating a prior that favors cardinal over oblique orientations. While continuing to capture the changes in error distribution with set size, the resulting model accurately described stimulus-specific variations as well, better than a slot-based competitor. Efficient coding produces a repulsive bias away from cardinal orientations, a bias that ought to be sensitive to changes in the environmental statistics. We subsequently tested whether shifts in the stimulus distribution influenced response bias to uniformly sampled target orientations in human subjects (of either sex). Across adaptation blocks, we manipulated the distribution of nontarget items by sampling from a bimodal congruent (incongruent) distribution with peaks centered on cardinal (oblique) orientations. Preadaptation responses were repulsed away from the cardinal axes. However, exposure to the incongruent distribution produced systematic decreases in repulsion that persisted after adaptation. This result confirms the role of prior expectation in generating stimulus-specific effects and validates the neural framework.SIGNIFICANCE STATEMENT Theories of neural coding have been used successfully to explain how errors in recall from working memory depend on the number of items stored. However, recall of visual features also shows stimulus-specific variation in bias and precision. Here we unify two previously unconnected theories, the neural resource model of working memory and the efficient coding framework, to provide a principled account of these stimulus-specific effects. Given the importance of working memory limitations to multiple aspects of human and animal behavior, and the recent high-profile advances in theories of efficient coding, our modeling framework provides a richer, yet parsimonious, description of how orientation encoding influences visual working memory performance.

Keywords: efficient coding; population coding; visual working memory.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / physiology
  • Adolescent
  • Adult
  • Female
  • Fixation, Ocular / physiology
  • Humans
  • Likelihood Functions
  • Male
  • Memory, Short-Term / physiology*
  • Mental Recall / physiology*
  • Models, Neurological*
  • Orientation, Spatial
  • Photic Stimulation / methods*
  • Statistical Distributions
  • Visual Perception / physiology*
  • Young Adult