Colin C. Korbisch

Movements become more vigorous when rewards are expected, suggesting that motivational signals influence motor control. Dopaminergic neurons, known to encode reward expectation and prediction error, are prime candidates for linking value and vigor. Here, we show that human reach vigor dynamically tracks canonical dopaminergic learning signals not only at movement onset but also during ongoing motion. Using a reaching task with probabilistic rewards (0, 33, 66, and 100%), we observed that peak velocity scaled with expected value. Crucially, following feedback, reach velocity was transiently invigorated or enervated in proportion to the sign and magnitude of the reward prediction error. Trial-by-trial changes in kinematics reflected value updating, consistent with dopaminergic phasic learning signals. These results demonstrate that movement vigor is modulated by reward-learning signals on rapid timescales, revealing a real-time behavioral readout of motivational computation in the brain.

Movement vigor across multiple modalities increases with reward, suggesting that the neural circuits that represent value influence the control of movement. Dopaminergic neuron (DAN) activity in the basal ganglia has been suggested as the potential mediator of this response. If DAN activity is the bridge between value and vigor, then vigor should track canonical mediators of this activity, namely reward expectation and reward prediction error. Here we ask if a similar time-locked response is present in vigor of reaching movements. We explore this link by leveraging the known phasic dopaminergic response to stochastic rewards, where activity is modulated by both reward expectation at cue and the prediction error at feedback. We used probabilistic rewards to create a reaching task rich in reward expectation, reward prediction error, and learning. In one experiment, target reward probabilities were explicitly stated, and in the other, were left unknown and to be learned by the participants. We included two stochastic rewards (probabilities 33% and 66%) and two deterministic ones (probabilities 100% and 0%). Outgoing peak velocity in both experiments increased with increasing reward expectation. Furthermore, we observed a short-latency response in the vigor of the ongoing movement, that tracked reward prediction error: either invigorating or enervating velocity consistent with the sign and magnitude of the error. Reaching kinematics also revealed the value-update process in a trial-to-trial fashion, similar to the effect of prediction error signals typical in dopamine-mediated striatal phasic activity. Lastly, reach vigor increased with reward history over trials, mirroring the motivational effects often linked to fluctuating dopamine levels. Taken together, our results demonstrate and exquisite link between known short-latency reward signals and the invigoration of both discrete and ongoing movements. NEW & NOTEWORTHY Previous research has demonstrated the invigorating effects of reward on movement. Growing evidence suggests this is causally explained by midbrain dopamine transients. Here, we demonstrate that reach vigor tracks canonical variables of learning and motivation across time scales ranging from milliseconds to minutes. Velocity was modulated by reward expectation, reward prediction error and reward rate, key variables that have also been associated with striatal dopaminergic fluctuations. These results point to a potential neural mechanism by which dopamine can influence both decision making and movement control and support the proposition that reward-based invigoration of movement is in part influenced by dopaminergic circuits.

During deliberation, as the brain considers its options, the neural activity representing the goodness of each option rises toward a threshold, and the choice is often dictated by the option for which the rise is fastest. Here we report a surprising correlate of these activities: saccade vigor. We engaged human subjects in a decision-making task in which they considered effortful options, each requiring walking various durations and inclines. As they deliberated, they made saccades between the symbolic representations of those options. These saccades had no bearing on the effort that they would later expend, yet as they deliberated, saccade velocities increased. The rate of rise in vigor was faster for saccades toward the option that they later indicated as their choice, and encoded the difference in the subjective value of the two effortful options. Once deliberation ended, following a brief delay the subjects indicated their choice by making another saccade. Remarkably, vigor for this saccade dropped to baseline and no longer encoded subjective value. These results are consistent with an urgency model of decision-making in which a global signal in the brain drives both the neural circuits that make decisions, and the neural circuits that make movements. Paradoxically, this common drive is shared between the oculomotor circuits and the decision-making circuits, even when the decision involves effortful expenditure during a future event. Significance There is a link between the decisions we make and the movements that follow. Not only do we prefer options of greater value, but we also move faster to acquire them. When deliberating between options, neural activity rises to a threshold and the option that wins this race is the one chosen. We report a potential correlate of this in the motor control circuits; during deliberation, saccade vigor to both options rise, but faster for the option ultimately chosen. Thus, our movements appear to mirror the neural activity conducting the decision-making process. Paradoxically, this is true even when the movements have no direct bearing on the decision at hand.