Literature DB >> 32234779

Reward-Based Improvements in Motor Control Are Driven by Multiple Error-Reducing Mechanisms.

Olivier Codol1, Peter J Holland2, Sanjay G Manohar3,4, Joseph M Galea2.   

Abstract

Reward has a remarkable ability to invigorate motor behavior, enabling individuals to select and execute actions with greater precision and speed. However, if reward is to be exploited in applied settings, such as rehabilitation, a thorough understanding of its underlying mechanisms is required. In a series of experiments, we first demonstrate that reward simultaneously improves the selection and execution components of a reaching movement. Specifically, reward promoted the selection of the correct action in the presence of distractors, while also improving execution through increased speed and maintenance of accuracy. These results led to a shift in the speed-accuracy functions for both selection and execution. In addition, punishment had a similar impact on action selection and execution, although it enhanced execution performance across all trials within a block, that is, its impact was noncontingent to trial value. Although the reward-driven enhancement of movement execution has been proposed to occur through enhanced feedback control, an untested possibility is that it is also driven by increased arm stiffness, an energy-consuming process that enhances limb stability. Computational analysis revealed that reward led to both an increase in feedback correction in the middle of the movement and a reduction in motor noise near the target. In line with our hypothesis, we provide novel evidence that this noise reduction is driven by a reward-dependent increase in arm stiffness. Therefore, reward drives multiple error-reduction mechanisms which enable individuals to invigorate motor performance without compromising accuracy.SIGNIFICANCE STATEMENT While reward is well-known for enhancing motor performance, how the nervous system generates these improvements is unclear. Despite recent work indicating that reward leads to enhanced feedback control, an untested possibility is that it also increases arm stiffness. We demonstrate that reward simultaneously improves the selection and execution components of a reaching movement. Furthermore, we show that punishment has a similar positive impact on performance. Importantly, by combining computational and biomechanical approaches, we show that reward leads to both improved feedback correction and an increase in stiffness. Therefore, reward drives multiple error-reduction mechanisms which enable individuals to invigorate performance without compromising accuracy. This work suggests that stiffness control plays a vital, and underappreciated, role in the reward-based imporvemenets in motor control.
Copyright © 2020 the authors.

Entities:  

Keywords:  action execution.; action selection; feedback control; reaching; reinforcement; stiffness

Mesh:

Year:  2020        PMID: 32234779      PMCID: PMC7189755          DOI: 10.1523/JNEUROSCI.2646-19.2020

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  65 in total

1.  Modulation of saccadic eye movements by predicted reward outcome.

Authors:  Yoriko Takikawa; Reiko Kawagoe; Hideaki Itoh; Hiroyuki Nakahara; Okihide Hikosaka
Journal:  Exp Brain Res       Date:  2001-11-28       Impact factor: 1.972

2.  The role of execution noise in movement variability.

Authors:  Robert J van Beers; Patrick Haggard; Daniel M Wolpert
Journal:  J Neurophysiol       Date:  2003-10-15       Impact factor: 2.714

3.  THE MECHANICS OF HUMAN SACCADIC EYE MOVEMENT.

Authors:  D A ROBINSON
Journal:  J Physiol       Date:  1964-11       Impact factor: 5.182

4.  Reward anticipation modulates primary motor cortex excitability during task preparation.

Authors:  Carsten Bundt; Elger L Abrahamse; Senne Braem; Marcel Brass; Wim Notebaert
Journal:  Neuroimage       Date:  2016-07-07       Impact factor: 6.556

5.  Increased reward in ankle robotics training enhances motor control and cortical efficiency in stroke.

Authors:  Ronald N Goodman; Jeremy C Rietschel; Anindo Roy; Brian C Jung; Jason Diaz; Richard F Macko; Larry W Forrester
Journal:  J Rehabil Res Dev       Date:  2014

6.  The intrinsic value of visual information affects saccade velocities.

Authors:  Minnan Xu-Wilson; David S Zee; Reza Shadmehr
Journal:  Exp Brain Res       Date:  2009-06-14       Impact factor: 1.972

7.  Spinal stretch reflexes support efficient hand control.

Authors:  Jeffrey Weiler; Paul L Gribble; J Andrew Pruszynski
Journal:  Nat Neurosci       Date:  2019-02-11       Impact factor: 24.884

Review 8.  A tale of two species: Neural integration in zebrafish and monkeys.

Authors:  M Joshua; S G Lisberger
Journal:  Neuroscience       Date:  2014-05-02       Impact factor: 3.590

9.  Reward Pays the Cost of Noise Reduction in Motor and Cognitive Control.

Authors:  Sanjay G Manohar; Trevor T-J Chong; Matthew A J Apps; Amit Batla; Maria Stamelou; Paul R Jarman; Kailash P Bhatia; Masud Husain
Journal:  Curr Biol       Date:  2015-06-18       Impact factor: 10.834

10.  Opposing effects of reward and punishment on human vigor.

Authors:  Benjamin Griffiths; Ulrik R Beierholm
Journal:  Sci Rep       Date:  2017-02-13       Impact factor: 4.379

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  11 in total

1.  Selecting and Executing Actions for Rewards.

Authors:  Pierre Vassiliadis; Gerard Derosiere
Journal:  J Neurosci       Date:  2020-08-19       Impact factor: 6.167

2.  Expectation of volitional arm movement has prolonged effects on the grip force exerted on a pinched object.

Authors:  Anvesh Naik; Satyajit Ambike
Journal:  Exp Brain Res       Date:  2022-08-11       Impact factor: 2.064

3.  Different Patterns of Neural Activity Characterize Motor Skill Performance During Acquisition and Retention.

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Journal:  Front Hum Neurosci       Date:  2022-06-13       Impact factor: 3.473

4.  Hasty sensorimotor decisions rely on an overlap of broad and selective changes in motor activity.

Authors:  Gerard Derosiere; David Thura; Paul Cisek; Julie Duque
Journal:  PLoS Biol       Date:  2022-04-07       Impact factor: 9.593

5.  Cognitive Control as a Multivariate Optimization Problem.

Authors:  Harrison Ritz; Xiamin Leng; Amitai Shenhav
Journal:  J Cogn Neurosci       Date:  2022-03-05       Impact factor: 3.225

6.  Reward-driven enhancements in motor control are robust to TMS manipulation.

Authors:  Olivier Codol; Joseph M Galea; Roya Jalali; Peter J Holland
Journal:  Exp Brain Res       Date:  2020-04-09       Impact factor: 1.972

7.  The dissociable effects of reward on sequential motor behavior.

Authors:  Sebastian Sporn; Xiuli Chen; Joseph M Galea
Journal:  J Neurophysiol       Date:  2022-06-01       Impact factor: 2.974

8.  Dopamine promotes instrumental motivation, but reduces reward-related vigour.

Authors:  John P Grogan; Timothy R Sandhu; Michele T Hu; Sanjay G Manohar
Journal:  Elife       Date:  2020-10-01       Impact factor: 8.140

9.  Reward boosts reinforcement-based motor learning.

Authors:  Pierre Vassiliadis; Gerard Derosiere; Cecile Dubuc; Aegryan Lete; Frederic Crevecoeur; Friedhelm C Hummel; Julie Duque
Journal:  iScience       Date:  2021-07-07

10.  Reward-Dependent Selection of Feedback Gains Impacts Rapid Motor Decisions.

Authors:  Antoine De Comite; Frédéric Crevecoeur; Philippe Lefèvre
Journal:  eNeuro       Date:  2022-03-28
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