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.

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

  • 2,345
    views
  • 299
    downloads
  • 9
    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. 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
    Moritz F Wurm, Doruk Yiğit Erigüç
    Research Article

    Recognizing goal-directed actions is a computationally challenging task, requiring not only the visual analysis of body movements, but also analysis of how these movements causally impact, and thereby induce a change in, those objects targeted by an action. We tested the hypothesis that the analysis of body movements and the effects they induce relies on distinct neural representations in superior and anterior inferior parietal lobe (SPL and aIPL). In four fMRI sessions, participants observed videos of actions (e.g. breaking stick, squashing plastic bottle) along with corresponding point-light-display (PLD) stick figures, pantomimes, and abstract animations of agent–object interactions (e.g. dividing or compressing a circle). Cross-decoding between actions and animations revealed that aIPL encodes abstract representations of action effect structures independent of motion and object identity. By contrast, cross-decoding between actions and PLDs revealed that SPL is disproportionally tuned to body movements independent of visible interactions with objects. Lateral occipitotemporal cortex (LOTC) was sensitive to both action effects and body movements. These results demonstrate that parietal cortex and LOTC are tuned to physical action features, such as how body parts move in space relative to each other and how body parts interact with objects to induce a change (e.g. in position or shape/configuration). The high level of abstraction revealed by cross-decoding suggests a general neural code supporting mechanical reasoning about how entities interact with, and have effects on, each other.

    1. Neuroscience
    Gyeong Hee Pyeon, Hyewon Cho ... Yong Sang Jo
    Research Article Updated

    Recent studies suggest that calcitonin gene-related peptide (CGRP) neurons in the parabrachial nucleus (PBN) represent aversive information and signal a general alarm to the forebrain. If CGRP neurons serve as a true general alarm, their activation would modulate both passive nad active defensive behaviors depending on the magnitude and context of the threat. However, most prior research has focused on the role of CGRP neurons in passive freezing responses, with limited exploration of their involvement in active defensive behaviors. To address this, we examined the role of CGRP neurons in active defensive behavior using a predator-like robot programmed to chase mice. Our electrophysiological results revealed that CGRP neurons encode the intensity of aversive stimuli through variations in firing durations and amplitudes. Optogenetic activation of CGRP neurons during robot chasing elevated flight responses in both conditioning and retention tests, presumably by amplifying the perception of the threat as more imminent and dangerous. In contrast, animals with inactivated CGRP neurons exhibited reduced flight responses, even when the robot was programmed to appear highly threatening during conditioning. These findings expand the understanding of CGRP neurons in the PBN as a critical alarm system, capable of dynamically regulating active defensive behaviors by amplifying threat perception, and ensuring adaptive responses to varying levels of danger.