Rate-distortion theory of neural coding and its implications for working memory

  1. Anthony MV Jakob  Is a corresponding author
  2. Samuel J Gershman
  1. Harvard University, United States

Abstract

Rate-distortion theory provides a powerful framework for understanding the nature of human memory by formalizing the relationship between information rate (the average number of bits per stimulus transmitted across the memory channel) and distortion (the cost of memory errors). Here we show how this abstract computational-level framework can be realized by a model of neural population coding. The model reproduces key regularities of visual working memory, including some that were not previously explained by population coding models. We verify a novel prediction of the model by reanalyzing recordings of monkey prefrontal neurons during an oculomotor delayed response task.

Data availability

The current manuscript is a computational study, so no data have been generated for this manuscript. Source code can be found at https://github.com/amvjakob/wm-rate-distortion. The previously published datasets are available upon request from the corresponding authors of the published papers, Souza and Oberauer (2015), Daniel Bliss at al. (2017), Panichello et al. (2019). A minimally processed dataset from Barbosa et al. (2020) is available online ((https://github.com/comptelab/interplayPFC), with the raw data available upon request from the corresponding author of the published paper (raw monkey data available upon request to Christos Constantinidis cconstan@wakehealth.edu, and raw EEG data available upon request to Heike Stein, heike.c.stein@gmail.com). There are no specific application or approval processes involved in requesting these datasets.

The following previously published data sets were used

Article and author information

Author details

  1. Anthony MV Jakob

    Department of Neurobiology, Harvard University, Cambridge, United States
    For correspondence
    anthony_jakob@hms.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0996-1356
  2. Samuel J Gershman

    Department of Psychology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6546-3298

Funding

Fondation Bertarelli (Bertarelli Fellowship)

  • Anthony MV Jakob

National Science Foundation (NSF STC award,CCF-1231216)

  • Samuel J Gershman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Jakob & Gershman

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,497
    views
  • 304
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Anthony MV Jakob
  2. Samuel J Gershman
(2023)
Rate-distortion theory of neural coding and its implications for working memory
eLife 12:e79450.
https://doi.org/10.7554/eLife.79450

Share this article

https://doi.org/10.7554/eLife.79450

Further reading

    1. Evolutionary Biology
    2. Neuroscience
    Jenny Chen, Phoebe R Richardson ... Hopi E Hoekstra
    Research Article

    Genetic variation is known to contribute to the variation of animal social behavior, but the molecular mechanisms that lead to behavioral differences are still not fully understood. Here, we investigate the cellular evolution of the hypothalamic preoptic area (POA), a brain region that plays a critical role in social behavior, across two sister species of deer mice (Peromyscus maniculatus and P. polionotus) with divergent social systems. These two species exhibit large differences in mating and parental care behavior across species and sex. Using single-nucleus RNA-sequencing, we build a cellular atlas of the POA for males and females of both Peromyscus species. We identify four cell types that are differentially abundant across species, two of which may account for species differences in parental care behavior based on known functions of these cell types. Our data further implicate two sex-biased cell types to be important for the evolution of sex-specific behavior. Finally, we show a remarkable reduction of sex-biased gene expression in P. polionotus, a monogamous species that also exhibits reduced sexual dimorphism in parental care behavior. Our POA atlas is a powerful resource to investigate how molecular neuronal traits may be evolving to give rise to innate differences in social behavior across animal species.

    1. Neuroscience
    Damian Koevoet, Laura Van Zantwijk ... Christoph Strauch
    Research Article

    What determines where to move the eyes? We recently showed that pupil size, a well-established marker of effort, also reflects the effort associated with making a saccade (‘saccade costs’). Here, we demonstrate saccade costs to critically drive saccade selection: when choosing between any two saccade directions, the least costly direction was consistently preferred. Strikingly, this principle even held during search in natural scenes in two additional experiments. When increasing cognitive demand experimentally through an auditory counting task, participants made fewer saccades and especially cut costly directions. This suggests that the eye-movement system and other cognitive operations consume similar resources that are flexibly allocated among each other as cognitive demand changes. Together, we argue that eye-movement behavior is tuned to adaptively minimize saccade-inherent effort.