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Research Articles, Behavioral/Cognitive

Modulation of Motor Vigor by Expectation of Reward Probability Trial-by-Trial Is Preserved in Healthy Ageing and Parkinson's Disease Patients

Margherita Tecilla, Michael Großbach, Giovanni Gentile, Peter Holland, Sebastian Sporn, Angelo Antonini and Maria Herrojo Ruiz
Journal of Neuroscience 8 March 2023, 43 (10) 1757-1777; DOI: https://doi.org/10.1523/JNEUROSCI.1583-22.2022
Margherita Tecilla
1Department of Psychology, Goldsmiths, University of London, London SE146NW, United Kingdom
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Michael Großbach
2Institute of Music Physiology and Musicians' Medicine, Hannover University of Music Drama and Media, Hannover 30175, Germany
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Giovanni Gentile
3Parkinson and Movement Disorders Unit, Study Center for Neurodegeneration (CESNE), Department of Neuroscience, University of Padua, Padua 35131, Italy
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Peter Holland
1Department of Psychology, Goldsmiths, University of London, London SE146NW, United Kingdom
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Sebastian Sporn
4Department of Clinical and Movement Neuroscience, Queen Square Institute of Neurology, University College London, London WC1N3BG, United Kingdom
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Angelo Antonini
3Parkinson and Movement Disorders Unit, Study Center for Neurodegeneration (CESNE), Department of Neuroscience, University of Padua, Padua 35131, Italy
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Maria Herrojo Ruiz
1Department of Psychology, Goldsmiths, University of London, London SE146NW, United Kingdom
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Abstract

Motor improvements, such as faster movement times or increased velocity, have been associated with reward magnitude in deterministic contexts. Yet whether individual inferences on reward probability influence motor vigor dynamically remains undetermined. We investigated how dynamically inferring volatile action-reward contingencies modulated motor performance trial-by-trial. We conducted three studies that coupled a reversal learning paradigm with a motor sequence task and used a validated hierarchical Bayesian model to fit trial-by-trial data. In Study 1, we tested healthy younger [HYA; 37 (24 females)] and older adults [HOA; 37 (17 females)], and medicated Parkinson's disease (PD) patients [20 (7 females)]. We showed that stronger predictions about the tendency of the action-reward contingency led to faster performance tempo, commensurate with movement time, on a trial-by-trial basis without robustly modulating reaction time (RT). Using Bayesian linear mixed models, we demonstrated a similar invigoration effect on performance tempo in HYA, HOA, and PD, despite HOA and PD being slower than HYA. In Study 2 [HYA, 39 (29 females)], we additionally showed that retrospective subjective inference about credit assignment did not contribute to differences in motor vigor effects. Last, Study 3 [HYA, 33 (27 females)] revealed that explicit beliefs about the reward tendency (confidence ratings) modulated performance tempo trial-by-trial. Our study is the first to reveal that the dynamic updating of beliefs about volatile action-reward contingencies positively biases motor performance through faster tempo. We also provide robust evidence for a preserved sensitivity of motor vigor to inferences about the action-reward mapping in aging and medicated PD.

SIGNIFICANCE STATEMENT Navigating a world rich in uncertainty relies on updating beliefs about the probability that our actions lead to reward. Here, we investigated how inferring the action-reward contingencies in a volatile environment modulated motor vigor trial-by-trial in healthy younger and older adults, and in Parkinson's disease (PD) patients on medication. We found an association between trial-by-trial predictions about the tendency of the action-reward contingency and performance tempo, with stronger expectations speeding the movement. We additionally provided evidence for a similar sensitivity of performance tempo to the strength of these predictions in all groups. Thus, dynamic beliefs about the changing relationship between actions and their outcome enhanced motor vigor. This positive bias was not compromised by age or Parkinson's disease.

  • action-reward contingency
  • motor vigor
  • Parkinson's disease
  • predictive coding
  • reward
  • uncertainty

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The Journal of Neuroscience: 43 (10)
Journal of Neuroscience
Vol. 43, Issue 10
8 Mar 2023
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Modulation of Motor Vigor by Expectation of Reward Probability Trial-by-Trial Is Preserved in Healthy Ageing and Parkinson's Disease Patients
Margherita Tecilla, Michael Großbach, Giovanni Gentile, Peter Holland, Sebastian Sporn, Angelo Antonini, Maria Herrojo Ruiz
Journal of Neuroscience 8 March 2023, 43 (10) 1757-1777; DOI: 10.1523/JNEUROSCI.1583-22.2022

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Modulation of Motor Vigor by Expectation of Reward Probability Trial-by-Trial Is Preserved in Healthy Ageing and Parkinson's Disease Patients
Margherita Tecilla, Michael Großbach, Giovanni Gentile, Peter Holland, Sebastian Sporn, Angelo Antonini, Maria Herrojo Ruiz
Journal of Neuroscience 8 March 2023, 43 (10) 1757-1777; DOI: 10.1523/JNEUROSCI.1583-22.2022
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Keywords

  • action-reward contingency
  • motor vigor
  • Parkinson's disease
  • predictive coding
  • reward
  • uncertainty

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