Motor learning and adaptation are important functions of the nervous system. Classical studies have characterized how humans adapt to changes in the environment during tasks such as reaching, and have documented improvements in behavior across movements. Yet little is known about how quickly the nervous system adapts to such disturbances. In particular, recent work has suggested that adaptation could be sufficiently fast to alter the control strategies of an ongoing movement. To further address the possibility that learning occurred within a single movement, we designed a series of human reaching experiments to extract from muscles recordings the latency of feedback adaptation. Our results confirmed that participants adapted their feedback responses to unanticipated force fields applied randomly. In addition, our analyses revealed that the feedback response was specifically and finely tuned to the ongoing perturbation not only across trials with the same force field, but also across different kinds of force fields. Finally, changes in muscle activity consistent with feedback adaptation occurred in about 250ms following reach onset. The adaptation that we observed across trials presented in a random context was similar to the one observed when the force fields could be anticipated, suggesting that these two adaptive processes may be closely linked to each other. In such case, our measurement of 250ms may correspond to the latency of motor adaptation in the nervous system. Significance Statement We measure the latency of feedback adaptation in a human reaching experiment by applying force field trials randomly. In spite of the fact that these disturbances could not be anticipated, we measured improvement in feedback corrections that paralleled standard adaptation. Correlates in muscle recordings occurred within about 250ms following movement onset. Such a short timescale of adaptation suggested that rapid adaptation complements feedback control of an ongoing movement. To further test this hypothesis, we demonstrate that indeed participants are able to 3 adapt their feedback responses to different kinds of force fields and directions applied randomly. 65 These findings support the existence of very rapid, possibly online, adaptation in the nervous system. 66

Visual Abstract

Visual Abstract

Gouirand N, Mathew J, Brenner E, Danion FR. Eye movements do not play an important role in the adaptation of hand tracking to a visuomotor rotation. Adapting hand movements to changes in our body or the environment is essential for skilled motor behavior. Although eye movements are known to assist hand movement control, how eye movements might contribute to the adaptation of hand movements remains largely unexplored. To determine to what extent eye movements contribute to visuomotor adaptation of hand tracking, participants were asked to track a visual target that followed an unpredictable trajectory with a cursor using a joystick. During blocks of trials, participants were either allowed to look wherever they liked or required to fixate a cross at the center of the screen. Eye movements were tracked to ensure gaze fixation as well as to examine free gaze behavior. The cursor initially responded normally to the joystick, but after several trials, the direction in which it responded was rotated by 90°. Although fixating the eyes had a detrimental influence on hand tracking performance, participants exhibited a rather similar time course of adaptation to rotated visual feedback in the gaze-fixed and gaze-free conditions. More importantly, there was extensive transfer of adaptation between the gazefixed and gaze-free conditions. We conclude that although eye movements are relevant for the online control of hand tracking, they do not play an important role in the visuomotor adaptation of such tracking. These results suggest that participants do not adapt by changing the mapping between eye and hand movements, but rather by changing the mapping between hand movements and the cursor's motion independently of eye movements.NEW & NOTEWORTHY Eye movements assist hand movements in everyday activities, but their contribution to visuomotor adaptation remains largely unknown. We compared adaptation of hand tracking under free gaze and fixed gaze. Although our results confirm that following the target with the eyes increases the accuracy of hand movements, they unexpectedly demonstrate that gaze fixation does not hinder adaptation. These results suggest that eye movements have distinct contributions for online control and visuomotor adaptation of hand movements.

Humans adapt to mechanical perturbations such as force fields during reaching within tens of trials. However, recent findings suggested that this adaptation may start within one single trial, i.e., online corrective movements can become tuned to the unanticipated perturbations within a trial. This was highlighted in previous works with a reaching experiment in which participants had to stop at a via-point (VP) located between the start and the goal. A force field was applied during the first and second parts of the movement and then occasionally unexpectedly switched off at the VP during catch trials. The results showed an after-effect during the second part of the movement when participants exited the VP. This behavioural result was interpreted as a standard after-effect, but it remained unclear how it was related to conventional trial-by-trial learning. The current study aimed to investigate how long do such changes in movement representations last in memory. For this, we have studied the same reaching task with VP in two situations: one with very short residing time in the VP and the second with an imposed minimum 500ms dwell time in the VP. In both situations, during the unexpected absence of the force field after VP, after-effects were observed. This suggests that online corrections to the internal representation of reach dynamics can be preserved in memory for around 850ms of resting time on average. Therefore, rapid changes occurring within movements can thus be preserved in memory long enough to influence trial-by-trial motor adaptation. SIGNIFICANCE STATEMENT Recent studies suggested that adaptive feedback control happens within a reach movement and the feedback responses are tuned specifically to the single-trial perturbation. Here we show that these feedback mediated changes in movement representations can last for around 850ms and are available to reproduce the characteristics of the newly acquired correction process. Current data replicate previous studies showing that feedback corrections are associated with changes 3 in online representations, and demonstrate that these changes are preserved in memory long enough to be an important component of standard trial-by-trial adaptation.