Sensitivity to error during visuomotor adaptation is similarly modulated by abrupt, gradual, and random perturbation schedules.

It has been suggested that sensorimotor adaptation involves at least two processes (i.e., fast and slow) that differ in retention and error sensitivity. Previous work has shown that repeated exposure to an abrupt force field perturbation results in greater error sensitivity for both the fast and slow processes. Although this implies that the faster relearning is associated with increased error sensitivity, it remains unclear what aspects of prior experience modulate error sensitivity. In the present study, we manipulated the initial training using different perturbation schedules, thought to differentially affect fast and slow learning processes based on error magnitude, and then observed what effect prior learning had on subsequent adaptation. During initial training of a visuomotor rotation task, we exposed three groups of participants to either an abrupt, a gradual, or a random perturbation schedule. During a testing session, all three groups were subsequently exposed to an abrupt perturbation schedule. Comparing the two sessions of the control group who experienced repetition of the same perturbation, we found an increased error sensitivity for both processes. We found that the error sensitivity was increased for both the fast and slow processes, with no reliable changes in the retention, for both the gradual and structural learning groups when compared to the first session of the control group. We discuss the findings in the context of how fast and slow learning processes respond to a history of errors.NEW & NOTEWORTHY We investigated what aspects of prior experience modulate error sensitivity, within the framework of a two-state model of short-term sensorimotor adaptation. We manipulated initial training on a visuomotor adaptation reaching task using specific perturbation schedules that are thought to differentially affect fast and slow learning processes, and we tested what effect these had on subsequent adaptation. We found that sensitivity to adaptation error was similarly modulated by abrupt, gradual, and random perturbation schedules.

Time course of changes in the long-latency feedback response parallels the fast process of short-term motor adaptation.

Adapting to novel dynamics involves modifying both feedforward and feedback control. We investigated whether the motor system alters feedback responses during adaptation to a novel force field in a manner similar to adjustments in feedforward control. We simultaneously tracked the time course of both feedforward and feedback systems via independent probes during a force field adaptation task. Participants (n = 35) grasped the handle of a robotic manipulandum and performed reaches to a visual target while the hand and arm were occluded. We introduced an abrupt counterclockwise velocity-dependent force field during a block of reaching trials. We measured movement kinematics and shoulder and elbow muscle activity with surface EMG electrodes. We tracked the feedback stretch response throughout the task. Using force channel trials, we measured overall learning, which was later decomposed into a fast and slow process. We found that the long-latency feedback response (LLFR) was upregulated in the early stages of learning and was correlated with the fast component of feedforward adaptation. The change in feedback response was specific to the long-latency epoch (50-100 ms after muscle stretch) and was observed only in the triceps muscle, which was the muscle required to counter the force field during adaptation. The similarity in time course for the LLFR and the estimated time course of the fast process suggests both are supported by common neural circuits. While some propose that the fast process reflects an explicit strategy, we argue instead that it may be a proxy for the feedback controller.NEW & NOTEWORTHY We investigated whether changes in the feedback stretch response were related to the proposed fast and slow processes of motor adaptation. We found that the long-latency component of the feedback stretch response was upregulated in the early stages of learning and the time course was correlated with the fast process. While some propose that the fast process reflects an explicit strategy, we argue instead that it may be a proxy for the feedback controller.

The gradient of the reinforcement landscape influences sensorimotor learning.

Consideration of previous successes and failures is essential to mastering a motor skill. Much of what we know about how humans and animals learn from such reinforcement feedback comes from experiments that involve sampling from a small number of discrete actions. Yet, it is less understood how we learn through reinforcement feedback when sampling from a continuous set of possible actions. Navigating a continuous set of possible actions likely requires using gradient information to maximize success. Here we addressed how humans adapt the aim of their hand when experiencing reinforcement feedback that was associated with a continuous set of possible actions. Specifically, we manipulated the change in the probability of reward given a change in motor action-the reinforcement gradient-to study its influence on learning. We found that participants learned faster when exposed to a steep gradient compared to a shallow gradient. Further, when initially positioned between a steep and a shallow gradient that rose in opposite directions, participants were more likely to ascend the steep gradient. We introduce a model that captures our results and several features of motor learning. Taken together, our work suggests that the sensorimotor system relies on temporally recent and spatially local gradient information to drive learning.

Both fast and slow learning processes contribute to savings following sensorimotor adaptation.

Recent work suggests that the rate of learning in sensorimotor adaptation is likely not fixed, but rather can change based on previous experience. One example is savings, a commonly observed phenomenon whereby the relearning of a motor skill is faster than the initial learning. Sensorimotor adaptation is thought to be driven by sensory prediction errors, which are the result of a mismatch between predicted and actual sensory consequences. It has been proposed that during motor adaptation the generation of sensory prediction errors engages two processes (fast and slow) that differ in learning and retention rates. We tested the idea that a history of errors would influence both the fast and slow processes during savings. Participants were asked to perform the same force field adaptation task twice in succession. We found that adaptation to the force field a second time led to increases in estimated learning rates for both fast and slow processes. While it has been proposed that savings is explained by an increase in learning rate for the fast process, here we observed that the slow process also contributes to savings. Our work suggests that fast and slow adaptation processes are both responsive to a history of error and both contribute to savings. NEW & NOTEWORTHY We studied the underlying mechanisms of savings during motor adaptation. Using a two-state model to represent fast and slow processes that contribute to motor adaptation, we found that a history of error modulates performance in both processes. While previous research has attributed savings to only changes in the fast process, we demonstrated that an increase in both processes is needed to account for the measured behavioral data.

Myomatrix arrays for high-definition muscle recording.

Neurons coordinate their activity to produce an astonishing variety of motor behaviors. Our present understanding of motor control has grown rapidly thanks to new methods for recording and analyzing populations of many individual neurons over time. In contrast, current methods for recording the nervous system's actual motor output - the activation of muscle fibers by motor neurons - typically cannot detect the individual electrical events produced by muscle fibers during natural behaviors and scale poorly across species and muscle groups. Here we present a novel class of electrode devices ("Myomatrix arrays") that record muscle activity at unprecedented resolution across muscles and behaviors. High-density, flexible electrode arrays allow for stable recordings from the muscle fibers activated by a single motor neuron, called a "motor unit", during natural behaviors in many species, including mice, rats, primates, songbirds, frogs, and insects. This technology therefore allows the nervous system's motor output to be monitored in unprecedented detail during complex behaviors across species and muscle morphologies. We anticipate that this technology will allow rapid advances in understanding the neural control of behavior and in identifying pathologies of the motor system.

Myomatrix arrays for high-definition muscle recording.

Neurons coordinate their activity to produce an astonishing variety of motor behaviors. Our present understanding of motor control has grown rapidly thanks to new methods for recording and analyzing populations of many individual neurons over time. In contrast, current methods for recording the nervous system's actual motor output - the activation of muscle fibers by motor neurons - typically cannot detect the individual electrical events produced by muscle fibers during natural behaviors and scale poorly across species and muscle groups. Here we present a novel class of electrode devices ('Myomatrix arrays') that record muscle activity at unprecedented resolution across muscles and behaviors. High-density, flexible electrode arrays allow for stable recordings from the muscle fibers activated by a single motor neuron, called a 'motor unit,' during natural behaviors in many species, including mice, rats, primates, songbirds, frogs, and insects. This technology therefore allows the nervous system's motor output to be monitored in unprecedented detail during complex behaviors across species and muscle morphologies. We anticipate that this technology will allow rapid advances in understanding the neural control of behavior and identifying pathologies of the motor system.