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Numerous studies have proposed that our adaptive motor behaviors depend on learning a map between sensory information and limb movement,1-3 called an "internal model." From this perspective, how the brain represents internal models is a critical issue in motor learning, especially regarding their association with spatial frames processed in motor planning.4,5 Extensive experimental evidence suggests that during planning stages for visually guided hand reaching, the brain transforms visual target representations in gaze-centered coordinates to motor commands in limb coordinates, via hand-target vectors in workspace coordinates.6-9 While numerous studies have intensively investigated whether the learning for reaching occurs in workspace or limb coordinates,10-20 the association of the learning with gaze coordinates still remains untested.21 Given the critical role of gaze-related spatial coding in reaching planning,22-26 the potential role of gaze states for learning is worth examining. Here, we show that motor memories for reaching are separately learned according to target location in gaze coordinates. Specifically, two opposing visuomotor rotations, which normally interfere with each other, can be simultaneously learned when each is associated with reaching to a foveal target and peripheral one. We also show that this gaze-dependent learning occurs in force-field adaptation. Furthermore, generalization of gaze-coupled reach adaptation is limited across central, right, and left visual fields. These results suggest that gaze states are available in the formation and recall of multiple internal models for reaching. Our findings provide novel evidence that a gaze-dependent spatial representation can provide a spatial coordinate framework for context-dependent motor learning.

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Reinforcement learning has been used as an experimental model of motor skill acquisition, where at times movements are successful and thus reinforced. One fundamental problem is to understand how humans select exploration over exploitation during learning. The decision could be influenced by factors such as task demands and reward availability. In this study, we applied a clustering algorithm to examine how a change in the accuracy requirements of a task affected the choice of exploration over exploitation. Participants made reaching movements to an unseen target using a planar robot arm and received reward after each successful movement. For one group of participants, the width of the hidden target decreased after every other training block. For a second group, it remained constant. The clustering algorithm was applied to the kinematic data to characterize motor learning on a trial-to-trial basis as a sequence of movements, each belonging to one of the identified clusters. By the end of learning, movement trajectories across all participants converged primarily to a single cluster with the greatest number of successful trials. Within this analysis framework, we defined exploration and exploitation as types of behavior in which two successive trajectories belong to different or similar clusters, respectively. The frequency of each mode of behavior was evaluated over the course of learning. It was found that by reducing the target width, participants used a greater variety of different clusters and displayed more exploration than exploitation. Excessive exploration relative to exploitation was found to be detrimental to subsequent motor learning.NEW & NOTEWORTHY The choice of exploration versus exploitation is a fundamental problem in learning new motor skills through reinforcement. In this study, we employed a data-driven approach to characterize movements on a trial-by-trial basis with an unsupervised clustering algorithm. Using this technique, we found that changes in task demands and, in particular, in the required accuracy of movements, influenced the ratio of exploration to exploitation. This analysis framework provides an attractive tool to investigate mechanisms of explorative and exploitative behavior while studying motor learning.

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The introduction of rest intervals interspersed with practice strengthens wakeful consolidation of skill. The mechanisms by which the brain binds discrete action representations into consolidated, highly temporally resolved skill sequences during waking rest are not known. To address this question, we recorded magnetoencephalography (MEG) during acquisition and rapid consolidation of a sequential motor skill. We report the presence of prominent, fast waking neural replay during the same rest periods in which rapid consolidation occurs. The observed replay is temporally compressed by approximately 20-fold relative to the acquired skill, is selective for the trained sequence, and predicts the magnitude of skill consolidation. Replay representations extend beyond the hippocampus and entorhinal cortex to the contralateral sensorimotor cortex. These results document the presence of robust hippocampo-neocortical replay supporting rapid wakeful consolidation of skill.

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Motor skill retention is typically measured by asking participants to reproduce previously learned movements from memory. The analog of this retention test (recall memory) in human verbal memory is known to underestimate how much learning is actually retained. Here we asked whether information about previously learned movements, which can no longer be reproduced, is also retained. Following visuomotor adaptation, we used tests of recall that involved reproduction of previously learned movements and tests of recognition in which participants were asked whether a candidate limb displacement, produced by a robot arm held by the subject, corresponded to a movement direction that was experienced during active training. The main finding was that 24 h after training, estimates of recognition memory were about twice as accurate as those of recall memory. Thus, there is information about previously learned movements that is not retrieved using recall testing but can be accessed in tests of recognition. We conducted additional tests to assess whether, 24 h after learning, recall for previously learned movements could be improved by presenting passive movements as retrieval cues. These tests were conducted immediately prior to recall testing and involved the passive playback of a small number of movements, which were spread across the workspace and included both adapted and baseline movements, without being marked as such. This technique restored recall memory for movements to levels close to those of recognition memory performance. Thus, somatic information may enable retrieval of otherwise inaccessible motor memories.

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The brain strengthens memories through consolidation, defined as resistance to interference (stabilization) or performance improvements between the end of a practice session and the beginning of the next (offline gains) [1]. Typically, consolidation has been measured hours or days after the completion of training [2], but the same concept may apply to periods of rest that occur interspersed in a series of practice bouts within the same session. Here, we took an unprecedented close look at the within-seconds time course of early human procedural learning over alternating short periods of practice and rest that constitute a typical online training session. We found that performance did not markedly change over short periods of practice. On the other hand, performance improvements in between practice periods, when subjects were at rest, were significant and accounted for early procedural learning. These offline improvements were more prominent in early training trials when the learning curve was steep and no performance decrements during preceding practice periods were present. At the neural level, simultaneous magnetoencephalographic recordings showed an anatomically defined signature of this phenomenon. Beta-band brain oscillatory activity in a predominantly contralateral frontoparietal network predicted rest-period performance improvements. Consistent with its role in sensorimotor engagement [3], modulation of beta activity may reflect replay of task processes during rest periods. We report a rapid form of offline consolidation that substantially contributes to early skill learning and may extend the concept of consolidation to a time scale in the order of seconds, rather than the hours or days traditionally accepted.

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When we speak, we get correlated sensory feedback from speech sounds and from the muscles and soft tissues of the vocal tract. Here we dissociate the contributions of auditory and somatosensory feedback to identify brain networks that underlie the somatic contribution to speech motor learning. The technique uses a robotic device that selectively alters somatosensory inputs in combination with resting-state fMRI scans that reveal learning-related changes in functional connectivity. A partial correlation analysis is used to identify connectivity changes that are not explained by the time course of activity in any other learning-related areas. This analysis revealed changes related to behavioral improvements in movement and separately, to changes in auditory perception: Speech motor adaptation itself was associated with connectivity changes that were primarily in non-motor areas of brain, specifically, to a strengthening of connectivity between auditory and somatosensory cortex and between presupplementary motor area and the inferior parietal lobule. In contrast, connectively changes associated with alterations to auditory perception were restricted to speech motor areas, specifically, primary motor cortex and inferior frontal gyrus. Overall, our findings show that during adaptation, somatosensory inputs result in a broad range of changes in connectivity in areas associated with speech motor control and learning.

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Pneumatically actuated muscles (PAMs) provide a low cost, lightweight, and high power-to-weight ratio solution for many robotic applications. In addition, the antagonist pair configuration for robotic arms make it open to biologically inspired control approaches. In spite of these advantages, they have not been widely adopted in human-in-the-loop control and learning applications. In this study, we propose a biologically inspired multimodal human-in-the-loop control system for driving a one degree-of-freedom robot, and realize the task of hammering a nail into a wood block under human control. We analyze the human sensorimotor learning in this system through a set of experiments, and show that effective autonomous hammering skill can be readily obtained through the developed human-robot interface. The results indicate that a human-in-the-loop learning setup with anthropomorphically valid multi-modal human-robot interface leads to fast learning, thus can be used to effectively derive autonomous robot skills for ballistic motor tasks that require modulation of impedance.

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This paper presents an efficient hybrid feedback feedforward (HFF) adaptive approximation-based control (AAC) strategy for a class of uncertain Euler-Lagrange systems. The control structure includes a proportional-derivative (PD) control term in the feedback loop and a radial-basis-function (RBF) neural network (NN) in the feedforward loop, which mimics the human motor learning control mechanism. At the presence of discontinuous friction, a sigmoid-jump-function NN is incorporated to improve control performance. The major difference of the proposed HFF-AAC design from the traditional feedback AAC (FB-AAC) design is that only desired outputs, rather than both tracking errors and desired outputs, are applied as RBF-NN inputs. Yet, such a slight modification leads to several attractive properties of HFF-AAC, including the convenient choice of an approximation domain, the decrease of the number of RBF-NN inputs, and semiglobal practical asymptotic stability dominated by control gains. Compared with previous HFF-AAC approaches, the proposed approach possesses the following two distinctive features: (i) all above attractive properties are achieved by a much simpler control scheme; (ii) the bounds of plant uncertainties are not required to be known. Consequently, the proposed approach guarantees a minimum configuration of the control structure and a minimum requirement of plant knowledge for the AAC design, which leads to a sharp decrease of implementation cost in terms of hardware selection, algorithm realization and system debugging. Simulation results have demonstrated that the proposed HFF-AAC can perform as good as or even better than the traditional FB-AAC under much simpler control synthesis and much lower computational cost.

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Humans have the remarkable ability to adapt their motor behaviour to changes in body properties and/or environmental conditions, based on sensory feedback such as vision and proprioception. The role of proprioception has been highlighted for the adaptation to new upper-limb dynamics, which is known to generalize to the opposite, non-adapted limb in healthy individuals. Such interlimb transfer seems to depend on sensory feedback, and the present study assessed whether the chronic loss of proprioception precludes interlimb transfer of dynamic adaptation by testing two well-characterized proprioceptively-deafferented subjects. These had to reach toward visual targets with vision of the limb. For both deafferented subjects, we observed adaptation of the dominant arm to Coriolis forces and after-effects on non-dominant arm movements in different movement directions, thus indicating interlimb transfer. Overall, our findings show that motor learning can generalize across limbs and movement directions despite the loss of proprioceptive afferents.

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There is accumulating evidence from behavioral, neurophysiological, and neuroimaging studies that the acquisition of motor skills involves both perceptual and motor learning. Perceptual learning alters movements, motor learning, and motor networks of the brain. Motor learning changes perceptual function and the sensory circuits of the brain. Here, we review studies of both human limb movement and speech that indicate that plasticity in sensory and motor systems is reciprocally linked. Taken together, this points to an approach to motor learning in which perceptual learning and sensory plasticity have a fundamental role.

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It is well known that the central nervous system automatically reduces a mismatch in the visuomotor coordination. Can the underlying learning strategy be modified by environmental factors or a subject's learning experiences? To elucidate this matter, two groups of subjects learned to execute reaching arm movements in environments with task-irrelevant visual cues. However, one group had previous experience of learning these movements using task-relevant visual cues. The results demonstrate that the two groups used different learning strategies for the same visual environment and that the learning strategy was influenced by prior learning experience.

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