Sensorimotor feedback loops are selectively sensitive to reward

  1. Olivier Codol  Is a corresponding author
  2. Mehrdad Kashefi
  3. Christopher J Forgaard
  4. Joseph M Galea
  5. J Andrew Pruszynski
  6. Paul L Gribble
  1. Western University, Canada
  2. University of Birmingham, United Kingdom

Abstract

Although it is well established that motivational factors such as earning more money for performing well improve motor performance, how the motor system implements this improvement remains unclear. For instance, feedback-based control, which uses sensory feedback from the body to correct for errors in movement, improves with greater reward. But feedback control encompasses many feedback loops with diverse characteristics such as the brain regions involved and their response time. Which specific loops drive these performance improvements with reward is unknown, even though their diversity makes it unlikely that they are contributing uniformly. We systematically tested the effect of reward on the latency (how long for a corrective response to arise?) and gain (how large is the corrective response?) of seven distinct sensorimotor feedback loops in humans. Only the fastest feedback loops were insensitive to reward, and the earliest reward-driven changes were consistently an increase in feedback gains, not a reduction in latency. Rather, a reduction of response latencies only tended to occur in slower feedback loops. These observations were similar across sensory modalities (vision and proprioception). Our results may have implications regarding feedback control performance in athletic coaching. For instance, coaching methodologies that rely on reinforcement or 'reward shaping' may need to specifically target aspects of movement that rely on reward-sensitive feedback responses.

Data availability

All behavioural data and analysis code are freely available online on the Open Science Framework website at https://osf.io/7t8yj/

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

Article and author information

Author details

  1. Olivier Codol

    Brain and Mind Institute, Western University, London, Canada
    For correspondence
    codol.olivier@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0796-5457
  2. Mehrdad Kashefi

    Brain and Mind Institute, Western University, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5981-5923
  3. Christopher J Forgaard

    Brain and Mind Institute, Western University, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Joseph M Galea

    School of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0009-4049
  5. J Andrew Pruszynski

    Department of Physiology and Pharmacology, Western University, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0786-0081
  6. Paul L Gribble

    Brain and Mind Institute, Western University, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1368-032X

Funding

Natural Science and Engineering Council of Canada (RGPIN-2018-05458)

  • Paul L Gribble

Canadian Institue of Health Research (PJT-156241)

  • Paul L Gribble

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

Ethics

Human subjects: All participants signed a consent form to provide informed consent prior to the experimental session. Recruitment and data collection were done in accordance with the requirements of the research ethics board at Western University, Project ID # 115787.

Reviewing Editor

  1. Kunlin Wei, Peking University, China

Publication history

  1. Received: July 5, 2022
  2. Accepted: December 29, 2022
  3. Accepted Manuscript published: January 13, 2023 (version 1)

Copyright

© 2023, Codol 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

  • 663
    Page views
  • 120
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Olivier Codol
  2. Mehrdad Kashefi
  3. Christopher J Forgaard
  4. Joseph M Galea
  5. J Andrew Pruszynski
  6. Paul L Gribble
(2023)
Sensorimotor feedback loops are selectively sensitive to reward
eLife 12:e81325.
https://doi.org/10.7554/eLife.81325

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Sabrina A Jones, Jacob H Barfield ... Woodrow L Shew
    Research Article

    Naturally occurring body movements and collective neural activity both exhibit complex dynamics, often with scale-free, fractal spatiotemporal structure. Scale-free dynamics of both brain and behavior are important because each is associated with functional benefits to the organism. Despite their similarities, scale-free brain activity and scale-free behavior have been studied separately, without a unified explanation. Here we show that scale-free dynamics of mouse behavior and neurons in visual cortex are strongly related. Surprisingly, the scale-free neural activity is limited to specific subsets of neurons, and these scale-free subsets exhibit stochastic winner-take-all competition with other neural subsets. This observation is inconsistent with prevailing theories of scale-free dynamics in neural systems, which stem from the criticality hypothesis. We develop a computational model which incorporates known cell-type-specific circuit structure, explaining our findings with a new type of critical dynamics. Our results establish neural underpinnings of scale-free behavior and clear behavioral relevance of scale-free neural activity.

    1. Neuroscience
    Barna Zajzon, David Dahmen ... Renato Duarte
    Research Article

    Information from the sensory periphery is conveyed to the cortex via structured projection pathways that spatially segregate stimulus features, providing a robust and efficient encoding strategy. Beyond sensory encoding, this prominent anatomical feature extends throughout the neocortex. However, the extent to which it influences cortical processing is unclear. In this study, we combine cortical circuit modeling with network theory to demonstrate that the sharpness of topographic projections acts as a bifurcation parameter, controlling the macroscopic dynamics and representational precision across a modular network. By shifting the balance of excitation and inhibition, topographic modularity gradually increases task performance and improves the signal-to-noise ratio across the system. We demonstrate that in biologically constrained networks, such a denoising behavior is contingent on recurrent inhibition. We show that this is a robust and generic structural feature that enables a broad range of behaviorally-relevant operating regimes, and provide an in-depth theoretical analysis unravelling the dynamical principles underlying the mechanism.