Flexible control of representational dynamics in a disinhibition-based model of decision making

  1. Bo Shen  Is a corresponding author
  2. Kenway Louie
  3. Paul W Glimcher
  1. New York University, United States

Abstract

Inhibition is crucial for brain function, regulating network activity by balancing excitation and implementing gain control. Recent evidence suggests that beyond simply inhibiting excitatory activity, inhibitory neurons can also shape circuit function through disinhibition. While disinhibitory circuit motifs have been implicated in cognitive processes including learning, attentional selection, and input gating, the role of disinhibition is largely unexplored in the study of decision-making. Here, we show that disinhibition provides a simple circuit motif for fast, dynamic control of network state and function. This dynamic control allows a disinhibition-based decision model to reproduce both value normalization and winner-take-all dynamics, the two central features of neurobiological decision-making captured in separate existing models with distinct circuit motifs. In addition, the disinhibition model exhibits flexible attractor dynamics consistent with different forms of persistent activity seen in working memory. Fitting the model to empirical data shows it captures well both the neurophysiological dynamics of value coding and psychometric choice behavior. Furthermore, the biological basis of disinhibition provides a simple mechanism for flexible top-down control of the network states, enabling the circuit to capture diverse task-dependent neural dynamics. These results suggest a biologically plausible unifying mechanism for decision-making and emphasize the importance of local disinhibition in neural processing.

Data availability

The empirical data presented in this paper and MATLAB code used for simulations and fitting the empirical data is available at DOI 10.17605/OSF.IO/YGR57.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Bo Shen

    Neuroscience Institute, New York University, New York, United States
    For correspondence
    bs3667@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5796-0844
  2. Kenway Louie

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Paul W Glimcher

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (R01DA038063)

  • Paul W Glimcher

National Institutes of Health (R01DA043676)

  • Paul W Glimcher

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

Reviewing Editor

  1. Timothy Verstynen, Carnegie Mellon University, United States

Version history

  1. Preprint posted: April 18, 2022 (view preprint)
  2. Received: August 3, 2022
  3. Accepted: May 24, 2023
  4. Accepted Manuscript published: June 1, 2023 (version 1)
  5. Version of Record published: June 30, 2023 (version 2)

Copyright

© 2023, Shen et al.

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

  • 1,230
    views
  • 153
    downloads
  • 1
    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. Bo Shen
  2. Kenway Louie
  3. Paul W Glimcher
(2023)
Flexible control of representational dynamics in a disinhibition-based model of decision making
eLife 12:e82426.
https://doi.org/10.7554/eLife.82426

Share this article

https://doi.org/10.7554/eLife.82426

Further reading

    1. Computational and Systems Biology
    Antony M Jose
    Research Article

    Interacting molecules create regulatory architectures that can persist despite turnover of molecules. Although epigenetic changes occur within the context of such architectures, there is limited understanding of how they can influence the heritability of changes. Here, I develop criteria for the heritability of regulatory architectures and use quantitative simulations of interacting regulators parsed as entities, their sensors, and the sensed properties to analyze how architectures influence heritable epigenetic changes. Information contained in regulatory architectures grows rapidly with the number of interacting molecules and its transmission requires positive feedback loops. While these architectures can recover after many epigenetic perturbations, some resulting changes can become permanently heritable. Architectures that are otherwise unstable can become heritable through periodic interactions with external regulators, which suggests that mortal somatic lineages with cells that reproducibly interact with the immortal germ lineage could make a wider variety of architectures heritable. Differential inhibition of the positive feedback loops that transmit regulatory architectures across generations can explain the gene-specific differences in heritable RNA silencing observed in the nematode Caenorhabditis elegans. More broadly, these results provide a foundation for analyzing the inheritance of epigenetic changes within the context of the regulatory architectures implemented using diverse molecules in different living systems.

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.