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

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.

The dissociable effects of reward on sequential motor behavior.

Reward has consistently been shown to enhance motor behavior; however, its beneficial effects appear to be largely unspecific. For example, reward is associated with both rapid and training-dependent improvements in performance, with a mechanistic account of these effects currently lacking. Here we tested the hypothesis that these distinct reward-based improvements are driven by dissociable reward types: monetary incentive and performance feedback. Whereas performance feedback provides information on how well a motor task has been completed (knowledge of performance), monetary incentive increases the motivation to perform optimally without providing a performance-based learning signal. Experiment 1 showed that groups who received monetary incentive rapidly improved movement times (MTs), using a novel sequential reaching task. In contrast, only groups with correct performance-based feedback showed learning-related improvements. Importantly, pairing both maximized MT performance gains and accelerated movement fusion. Fusion describes an optimization process during which neighboring sequential movements blend together to form singular actions. Results from experiment 2 served as a replication and showed that fusion led to enhanced performance speed while also improving movement efficiency through increased smoothness. Finally, experiment 3 showed that these improvements in performance persist for 24 h even without reward availability. This highlights the dissociable impact of monetary incentive and performance feedback, with their combination maximizing performance gains and leading to stable improvements in the speed and efficiency of sequential actions.NEW & NOTEWORTHY Our work provides a mechanistic framework for how reward influences motor behavior. Specifically, we show that rapid improvements in speed and accuracy are driven by reward presented in the form of money, whereas knowledge of performance through performance feedback leads to training-based improvements. Importantly, combining both maximized performance gains and led to improvements in movement quality through fusion, which describes an optimization process during which sequential movements blend into a single action.

Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety.

Anxiety results in sub-optimal motor learning, but the precise mechanisms through which this effect occurs remain unknown. Using a motor sequence learning paradigm with separate phases for initial exploration and reward-based learning, we show that anxiety states in humans impair learning by attenuating the update of reward estimates. Further, when such estimates are perceived as unstable over time (volatility), anxiety constrains adaptive behavioral changes. Neurally, anxiety during initial exploration increased the amplitude and the rate of long bursts of sensorimotor and prefrontal beta oscillations (13-30 Hz). These changes extended to the subsequent learning phase, where phasic increases in beta power and burst rate following reward feedback were linked to smaller updates in reward estimates, with a higher anxiety-related increase explaining the attenuated belief updating. These data suggest that state anxiety alters the dynamics of beta oscillations during reward processing, thereby impairing proper updating of motor predictions when learning in unstable environments.

Feeling anxious can hinder how well someone performs a task, a phenomenon that is sometimes called "choking under pressure". Anxiety may also impair a person's ability to learn a new manual task, like juggling or playing the piano; however, it remains unclear exactly how this happens. People learn manual tasks more quickly if they can practice first, and the more someone varies their movements during these trial runs, the faster they learn afterwards. Yet, anxiety can affect movement; for example, anxious people often make repetitive motions like hand-wringing or fidgeting. There is also evidence that very anxious people may learn less from the outcomes of their actions. To understand how anxiety may affect the learning of manual tasks, Sporn et al designed experiments where people learned to play a short sequence of notes on a piano. The main experiment involved 60 participants and was split over two phases. In the first 'exploration' phase, participants had to play the piano sequence using any timing they liked and were encouraged to explore different rhythms. In the second 'learning' phase, participants were rewarded with a higher score the closer they got to playing the notes with a certain rhythm, without being told that this was their specific goal. To see how anxiety affected performance, the participants were split into three groups. One group were told in the initial exploration phase that they would give a public talk after they completed the piano task, which reliably made them more anxious. A second group were told about the anxiety-inducing public speaking only during the learning phase; while a third group ­ the controls ­ were not aware of any public speaking task. People in the second group could learn the rhythm as well as the controls. Participants who were made anxious during the exploration phase, however, scored fewer points and were less likely to learn the piano sequence in the second phase. They also varied their movements less in the first phase. As a follow-up, Sporn et al. repeated the experiment with 26 people but without the initial exploration phase. This time the anxious participants were less able to learn the piano sequence and scored fewer points. This suggests that the initial exploration in the previous experiment had enabled later anxious participants to succeed in the learning phase despite being anxious. Finally, Sporn et al. also used a technique called electroencephalography (or EEG for short) to record brain activity and observed differences in participants with and without anxiety, particularly when they received their scores. The EEG signals showed that anxiety altered rhythmic patterns of brain activity called "sensorimotor beta oscillations", which are known to be involved in both movement and learning.