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.

Reviewing Editor

  1. Kunlin Wei, Peking University, China

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.

Version history

  1. Preprint posted: September 20, 2021 (view preprint)
  2. Received: July 5, 2022
  3. Accepted: December 29, 2022
  4. Accepted Manuscript published: January 13, 2023 (version 1)
  5. Version of Record published: February 9, 2023 (version 2)

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

  • 1,860
    Page views
  • 256
    Downloads
  • 3
    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

Share this article

https://doi.org/10.7554/eLife.81325

Further reading

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Cell Biology
    2. Neuroscience
    Zhenyong Wu, Grant F Kusick ... Shigeki Watanabe
    Research Article

    Despite decades of intense study, the molecular basis of asynchronous neurotransmitter release remains enigmatic. Synaptotagmin (syt) 7 and Doc2 have both been proposed as Ca2+ sensors that trigger this mode of exocytosis, but conflicting findings have led to controversy. Here, we demonstrate that at excitatory mouse hippocampal synapses, Doc2α is the major Ca2+ sensor for asynchronous release, while syt7 supports this process through activity-dependent docking of synaptic vesicles. In synapses lacking Doc2α, asynchronous release after single action potentials is strongly reduced, while deleting syt7 has no effect. However, in the absence of syt7, docked vesicles cannot be replenished on millisecond timescales. Consequently, both synchronous and asynchronous release depress from the second pulse onward during repetitive activity. By contrast, synapses lacking Doc2α have normal activity-dependent docking, but continue to exhibit decreased asynchronous release after multiple stimuli. Moreover, disruption of both Ca2+ sensors is non-additive. These findings result in a new model whereby syt7 drives activity-dependent docking, thus providing synaptic vesicles for synchronous (syt1) and asynchronous (Doc2 and other unidentified sensors) release during ongoing transmission.