Tecilla, Margherita;
Großbach, Michael;
Gentile, Giovanni;
Holland, Peter;
Sporn, Sebastian;
Antonini, Angelo;
Herrojo Ruiz, Maria;
(2023)
Modulation of motor vigour by expectation of reward probability trial-by-trial is preserved in healthy ageing and Parkinson's disease patients.
The Journal of Neuroscience
10.1523/JNEUROSCI.1583-22.2022.
(In press).
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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 vigour 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 one-armed bandit decision-making 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 [13 males]) and older adults (HOA, 37 [20 males]), and medicated Parkinson's Disease patients (PD, 20 [13 males]). 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 [10 males]), we additionally showed that retrospective subjective inference about credit assignment did not contribute to differences in motor vigour effects. Last, Study 3 (HYA, 33 [6 males]) 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 vigour to inferences about the action-reward mapping in ageing 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 vigour trial-by-trial in healthy younger and older adults, and in Parkinson's Disease 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 vigour. This positive bias was not compromised by age or Parkinson's disease.
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