Reward-based improvements in motor control are driven by multiple error-reducing mechanisms

Abstract

Reward has a remarkable ability to invigorate motor behaviour, enabling individuals to select 11 and execute actions with greater precision and speed. However, if reward is to be exploited 12 in applied settings such as rehabilitation, a thorough understanding of its underlying mech-13 anisms is required. Although reward-driven enhancement of movement execution has been 14 proposed to occur through enhanced feedback control, an untested alternative is that it is 15 driven by increased arm stiffness, an energy-consuming process that increases limb stability. 16First, we demonstrate that during reaching reward improves selection and execution per-17 formance concomitantly without interference. Computational analysis revealed that reward 18 led to both an increase in feedback correction during movement and a reduction in mo-19 tor noise near the target. We provide novel evidence that this noise reduction is driven by a 20 reward-dependent increase in arm stiffness. Therefore, reward drives multiple error-reduction 21 mechanisms which enable individuals to invigorate motor performance without compromising 22 accuracy. 23 24 1

Selecting and Executing Actions for Rewards

“…Another important finding of the study is that reward reduced motor noise through increased limb stiffness, limiting the potential negative consequence of high execution speed on accuracy. Interestingly, the movement pattern reported by Codol et al (2020), a parallel increase in movement speed and stiffness during rewarded trials, is similar to that observed when participants are exposed to unpredictable perturbations of their movements during execution (Crevecoeur et al, 2019). This pattern is thought to reflect the implementation of a specific strategy of the motor system (so-called "robust strategy"), minimizing the impact of perturbations on action execution in uncertain environments (Bian et al, 2020).…”

“…In a recent article published in The Journal of Neuroscience, Codol et al (2020) addressed the two issues mentioned above. In a series of experiments, the authors asked human subjects to use reaching movements to displace a manipulandum from a starting position to one of four target locations.…”

“…The first aim of the study was to test the impact of reward on the speed and accuracy of action selection and execution in a single setting. To do so, on 10p and 50p trials, Codol et al (2020) provided rewards that were inversely proportional to the RT and the MT combined together (reflecting the speed of selection and execution processes, respectively). Reward magnitude also depended on the accuracy of both selection and execution.…”

“…The roots of this idea lie so deep within the field that researchers often consider RTs and MTs together as a single measure, thought to reflect action vigor (Shadmehr et al, 2019). The findings of Codol et al (2020) ask us to reconsider carefully this vision, suggesting that, in some conditions, the speed of action selection and execution can be regulated by independent (yet likely interacting) neural structures. Consistent with this hypothesis, a recent study revealed the existence of distinct subpopulations of midbrain dopaminergic neurons, with some cells encoding behavioral choice and others sensitive to movement features (Engelhard et al, 2019).…”

Dopamine promotes instrumental motivation, but reduces reward-related vigour

“…Autocorrelation of eye position over time within saccades provides an indicator of motivation improving precision. This improvement, provided by corrective motor signals, can be increased by incentives and is revealed by late reductions in autocorrelation (Codol, Holland, Manohar, & Galea, 2019). In the current study, guaranteed rewards led to greater autocorrelation early in the saccades for PD OFF than ON (shown as the decrease in Fig.3f).…”