Meta-learning of human motor adaptation via the dorsal premotor cortex.

Meta-learning enables us to learn how to learn the same or similar tasks more efficiently. Decision-making literature theorizes that a prefrontal network, including the orbitofrontal and anterior cingulate cortices, underlies meta-learning of decision making by reinforcement learning. Recently, computationally similar meta-learning has been theorized and empirically demonstrated in motor adaptation. However, it remains unclear whether meta-learning of motor adaptation also relies on a prefrontal network. Considering hierarchical information flow from the prefrontal to motor cortices, this study explores whether meta-learning is processed in the dorsolateral prefrontal cortex (DLPFC) or in the dorsal premotor cortex (PMd), which is situated upstream of the primary motor cortex, but downstream of the DLPFC. Transcranial magnetic stimulation (TMS) was delivered to either PMd or DLPFC during a motor meta-learning task, in which human participants were trained to regulate the rate and retention of motor adaptation to maximize rewards. While motor adaptation itself was intact, TMS to PMd, but not DLPFC, attenuated meta-learning, impairing the ability to regulate motor adaptation to maximize rewards. Further analyses revealed that TMS to PMd attenuated meta-learning of memory retention. These results suggest that meta-learning of motor adaptation relies more on the premotor area than on a prefrontal network. Thus, while PMd is traditionally viewed as crucial for planning motor actions, this study suggests that PMd is also crucial for meta-learning of motor adaptation, processing goal-directed planning of how long motor memory should be retained to fit the long-term goal of motor adaptation.

The Role of Variability in Motor Learning.

Trial-to-trial variability in the execution of movements and motor skills is ubiquitous and widely considered to be the unwanted consequence of a noisy nervous system. However, recent studies have suggested that motor variability may also be a feature of how sensorimotor systems operate and learn. This view, rooted in reinforcement learning theory, equates motor variability with purposeful exploration of motor space that, when coupled with reinforcement, can drive motor learning. Here we review studies that explore the relationship between motor variability and motor learning in both humans and animal models. We discuss neural circuit mechanisms that underlie the generation and regulation of motor variability and consider the implications that this work has for our understanding of motor learning.

Prior Movement of One Arm Facilitates Motor Adaptation in the Other.

Many movements in daily life are embedded in motion sequences that involve more than one limb, demanding the motor system to monitor and control different body parts in quick succession. During such movements, systematic changes in the environment or the body might require motor adaptation of specific segments. However, previous motor adaptation research has focused primarily on motion sequences produced by a single limb, or on simultaneous movements of several limbs. For example, adaptation to opposing force fields is possible in unimanual reaching tasks when the direction of a prior or subsequent movement is predictive of force field direction. It is unclear, however, whether multilimb sequences can support motor adaptation processes in a similar way. In the present study (38 females, 38 males), we investigated whether reaches can be adapted to different force fields in a bimanual motor sequence when the information about the perturbation is associated with the prior movement direction of the other arm. In addition, we examined whether prior perceptual (visual or proprioceptive) feedback of the opposite arm contributes to force field-specific motor adaptation. Our key finding is that only active participation in the bimanual sequential task supports pronounced adaptation. This result suggests that active segments in bimanual motion sequences are linked across limbs. If there is a consistent association between movement kinematics of the linked and goal movement, the learning process of the goal movement can be facilitated. More generally, if motion sequences are repeated often, prior segments can evoke specific adjustments of subsequent movements.SIGNIFICANCE STATEMENT Movements in a limb's motion sequence can be adjusted based on linked movements. A prerequisite is that kinematics of the linked movements correctly predict which adjustments are needed. We show that use of kinematic information to improve performance is even possible when a prior linked movement is performed with a different limb. For example, a skilled juggler might have learned how to correctly adjust his catching movement of the left hand when the right hand performed a throwing action in a specific way. Linkage is possibly a key mechanism of the human motor system for learning complex bimanual skills. Our study emphasizes that learning of specific movements should not be studied in isolation but within their motor sequence context.

Older adults use fewer muscles to overcome perturbations during a seated locomotor task.

Locomotor perturbations provide insights into humans' response to motor errors. We investigated the differences in motor adaptation and muscle cocontraction between young and older adults during perturbed-arm and -leg recumbent stepping. We hypothesized that besides prolonged adaptation due to use-dependent learning, older adults would exhibit greater muscle cocontraction than young adults in response to the perturbations. Perturbations were brief increases in resistance applied during each stride at the extension onset or midextension of the left or right leg. Seventeen young adults and eleven older adults completed four 10-min perturbed stepping tasks. Subjects were instructed to follow a visual pacing cue, step smoothly, and use all their limbs to drive the stepper. Results showed that young and older adults did not decrease their errors with more perturbation experience, and errors did not wash out after perturbations were removed. Interestingly, older adults consistently had smaller motor errors than young adults in response to the perturbations. Older adults used fewer muscles to drive the stepper and had greater cocontraction than young adults. The results suggest that, despite similar motor error responses, young and older adults use distinctive muscle recruitment patterns to perform the motor task. Age-related motor strategies help track motor changes across the human life span and are a baseline for rehabilitation and performance assessment.NEW & NOTEWORTHY Older adults often demonstrate greater cocontraction and motor errors than young adults in response to motor perturbations. We demonstrated that older adults reduced their motor errors more than young adults with brief perturbations during recumbent stepping while maintaining greater muscle cocontraction. In doing so, older adults largely used one muscle pair to drive the stepper, tibialis anterior and soleus, whereas young adults used all muscles. These two muscles are crucial for maintaining upright balance.

Minimal impact of chronic proprioceptive loss on implicit sensorimotor adaptation and perceived movement outcome.

Implicit sensorimotor adaptation keeps our movements well calibrated amid changes in the body and environment. We have recently postulated that implicit adaptation is driven by a perceptual error: the difference between the desired and perceived movement outcome. According to this perceptual realignment model, implicit adaptation ceases when the perceived movement outcome-a multimodal percept determined by a prior belief conveying the intended action, the motor command, and feedback from proprioception and vision-is aligned with the desired movement outcome. Here, we examined the role of proprioception in implicit motor adaptation and perceived movement outcome by examining individuals who experience deafferentation (i.e., individuals with impaired proprioception and touch). We used a modified visuomotor rotation task designed to isolate implicit adaptation and probe perceived movement outcomes throughout the experiment. Surprisingly, both implicit adaptation and perceived movement outcome were minimally impacted by chronic deafferentation, posing a challenge to the perceptual realignment model of implicit adaptation.NEW & NOTEWORTHY We tested six individuals with chronic somatosensory deafferentation on a novel task that isolates implicit sensorimotor adaptation and probes perceived movement outcome. Strikingly, both implicit motor adaptation and perceptual movement outcome were not significantly impacted by chronic deafferentation, posing a challenge for theoretical models of adaptation that involve proprioception.

The influence of postural threat-induced anxiety on locomotor learning and updating.

The ability to adapt our locomotion in a feedforward (i.e., "predictive") manner is crucial for safe and efficient walking behavior. Equally important is the ability to quickly deadapt and update behavior that is no longer appropriate for the given context. It has been suggested that anxiety induced via postural threat may play a fundamental role in disrupting such deadaptation. We tested this hypothesis, using the "broken escalator" phenomenon: Fifty-six healthy young adults walked onto a stationary walkway ("BEFORE" condition, 5 trials), then onto a moving walkway akin to an airport travelator ("MOVING" condition, 10 trials), and then again onto the stationary walkway ("AFTER" condition, 5 trials). Participants completed all trials while wearing a virtual reality headset, which was used to induce postural threat-related anxiety (raised clifflike drop at the end of the walkway) during different phases of the paradigm. We found that performing the locomotor adaptation phase in a state of increased threat disrupted subsequent deadaptation during AFTER trials: These participants displayed anticipatory muscular activity as if expecting the platform to move and exhibited inappropriate anticipatory forward trunk movement that persisted during multiple AFTER trials. In contrast, postural threat induced during AFTER trials did not affect behavioral or neurophysiological outcomes. These findings highlight that actions learned in the presence of postural threat-induced anxiety are strengthened, leading to difficulties in deadapting these behaviors when no longer appropriate. Given the associations between anxiety and persistent maladaptive gait behaviors (e.g., "overly cautious" gait, functional gait disorders), the findings have implications for the understanding of such conditions.NEW & NOTEWORTHY Safe and efficient locomotion frequently requires movements to be adapted in a feedforward (i.e., "predictive") manner. These adaptations are not always correct, and thus inappropriate behavior must be quickly updated. Here we showed that increased threat disrupts this process. We found that locomotor actions learned in the presence of postural threat-induced anxiety are strengthened, subsequently impairing one's ability to update (or "deadapt") these actions when they are no longer appropriate for the current context.

Task-relevant visual feedback uncertainty attenuates visuomotor adaptation.

Motor adaptation is attenuated when sensory feedback about the movement is uncertain. Although this was initially shown for small visual errors, attenuation seems not to hold when visual errors are larger and the contributions of implicit adaptation are isolated with the error-clamp method, which makes visual feedback task-irrelevant. Here we ask whether adaptation to a similarly large perturbation is attenuated when task-relevant visual feedback is uncertain. In a first experiment, we tested participants on a 30° movement-contingent visuomotor rotation under both low (cursor) and high (cloud of moving dots) visual feedback uncertainty. In line with optimal integration, we found that the early increase in adaptation and final extent of adaptation were reduced with high feedback uncertainty. In a second experiment, we included several blocks of no-feedback trials during the perturbation block to quantify the contribution of implicit adaptation. Results showed that implicit adaptation was smaller with high compared to low feedback uncertainty throughout the perturbation block. The estimated contribution of explicit adaptation was overall small, particularly for high feedback uncertainty. Our results demonstrate an influence of task-relevant visual feedback, and the resulting target errors, on implicit adaptation. We show that our motor system is sensitive to the feedback it receives even for larger error sizes and accordingly adjusts its learning properties when our ability to achieve the task goal is affected.NEW & NOTEWORTHY Motor adaptation is linked to the estimation of our actions. Whereas uncertainty of task-irrelevant visual feedback appears not to influence implicit adaptation for errors beyond a certain size, here we tested whether this is still the case for task-relevant feedback. We show that implicit adaptation is attenuated when task-relevant visual feedback is uncertain, suggesting a dependency on the assessment of not just sensory prediction errors but also target errors.

Working memory constraints for visuomotor retrieval strategies.

Recent work has shown the fundamental role that cognitive strategies play in visuomotor adaptation. Although algorithmic strategies, such as mental rotation, are flexible and generalizable, they are computationally demanding. To avoid this computational cost, people can instead rely on memory retrieval of previously successful visuomotor solutions. However, such a strategy is likely subject to stimulus-response associations and rely heavily on working memory. In a series of five experiments, we sought to estimate the constraints in terms of capacity and precision of working memory retrieval for visuomotor adaptation. This was accomplished by leveraging different variations of visuomotor item-recognition and visuomotor rotation tasks where we associated unique rotations with specific targets in the workspace and manipulated the set size (i.e., number of rotation-target associations). Notably, from experiment 1 to 4, we found key signatures of working memory retrieval and not mental rotation. In particular, participants were less accurate and slower for larger set sizes and less recent items. Using a Bayesian latent-mixture model, we found that such decrease in performance was the result of increasing guessing behavior and less precise memories. In addition, we estimated that participants' working memory capacity was limited to two to five items, after which guessing increasingly dominated performance. Finally, in experiment 5, we showed how the constraints observed across experiments 1 to 4 can be overcome when relying on long-term memory retrieval. Our results point to the opportunity of studying other sources of memories where visuomotor solutions can be stored (e.g., episodic memories) to achieve successful adaptation.NEW & NOTEWORTHY We show that humans can adapt to feedback perturbations in different variations of the visuomotor rotation task by retrieving the successful solutions from working memory. In addition, using a Bayesian latent-mixture model, we reveal that guessing and low-precision memories are both responsible for the decrease in participants' performance as the number of solutions to memorize increases. These constraints can be overcome by relying on long-term memory retrieval resulting from extended practice with the visuomotor solutions.

Induced Discomfort Promotes Executive Function While Walking With(out) an Artificial Neuromuscular Impairment.

Neuromotor disorders can degrade one's ability to locomote and attend to salient stimuli in the environment. Many disorders are physiologically complex, making it difficult to tease apart interactions between motor adaptation and executive function processes. We address this challenge by giving participants a controlled artificial impairment, using electrical stimulation to produce an uncomfortable disruption in normal muscular coordination during locomotion. While adapting to this gait perturbation, participants performed an executive function task containing neutral and affectively charged stimuli. The artificial impairment was counterbalanced against control and sham (discomfort-only stimulation) walking conditions. Our twofold hypothesis that discomfort would selectively tax hot, emotionally-charged executive function and motor adaptation would challenge cold, logical executive function was not supported. However, we found that the discomfort experienced with both stimulation conditions improved participants' ability to inhibit distracting information, enhancing this aspect of executive function, and the effect did not depend on whether the task was affectively charged. Moderate discomfort during physical activity may have improved inhibitory control by increasing arousal, a known factor mediating executive function. These results show that using a sensorimotor perturbation that acts internally and bridges multiple physiological domains, including discomfort, can reveal effects not seen with purely environmental manipulations. The broader implications are that when high cognitive performance is needed during physical activity, it may be beneficial to, quite literally, operate outside one's comfort zone.

Multisensory perception depends on the reliability of the type of judgment.

The brain engages the processes of multisensory integration and recalibration to deal with discrepant multisensory signals. These processes consider the reliability of each sensory input, with the more reliable modality receiving the stronger weight. Sensory reliability is typically assessed via the variability of participants' judgments, yet these can be shaped by factors both external and internal to the nervous system. For example, motor noise and participant's dexterity with the specific response method contribute to judgment variability, and different response methods applied to the same stimuli can result in different estimates of sensory reliabilities. Here we ask how such variations in reliability induced by variations in the response method affect multisensory integration and sensory recalibration, as well as motor adaptation, in a visuomotor paradigm. Participants performed center-out hand movements and were asked to judge the position of the hand or rotated visual feedback at the movement end points. We manipulated the variability, and thus the reliability, of repeated judgments by asking participants to respond using either a visual or a proprioceptive matching procedure. We find that the relative weights of visual and proprioceptive signals, and thus the asymmetry of multisensory integration and recalibration, depend on the reliability modulated by the judgment method. Motor adaptation, in contrast, was insensitive to this manipulation. Hence, the outcome of multisensory binding is shaped by the noise introduced by sensorimotor processing, in line with perception and action being intertwined.NEW & NOTEWORTHY Our brain tends to combine multisensory signals based on their respective reliability. This reliability depends on sensory noise in the environment, noise in the nervous system, and, as we show here, variability induced by the specific judgment procedure.

Potentiation of Motor Adaptation Via Cerebellar tACS: Characterization of the Stimulation Frequency.

Motor adaptation is critical to update motor tasks in new or modified environmental conditions. While the cerebellum supports error-based adaptations, its neural implementation is partially known. By controlling the frequency of cerebellar transcranial alternating current stimulation (c-tACS), we can test the influence of neural oscillation from the cerebellum for motor adaptation. Two independent experiments were conducted. In Experiment 1, 16 participants received four c-tACS protocols (45 Hz, 50 Hz, 55 Hz, and sham) on four different days while they practiced a visuomotor adaptation task (30 degrees CCW) with variable intensity (within-subject design). In Experiment 2, 45 participants separated into three groups received the effect of 45 Hz, 55 Hz c-tACS, and sham, respectively (between-subject design), performing the same visuomotor task with a fixed intensity (0.9 mA). In Experiment 1, 45 Hz and 50 Hz of c-tACS accelerated motor adaptation when participants performed the task only for the first time, independent of the time interval between sessions or the stimulation intensity. The effect of active c-tACS was ratified in Experiment 2, where 45 Hz c-tACS benefits motor adaptation during the complete practice period. Reaction time, velocity, or duration of reaching are not affected by c-tACS. Cerebellar alternating current stimulation is an effective strategy to potentiate visuomotor adaptations. Frequency-dependent effects on the gamma band, especially for 45 Hz c-tACS, ratify the oscillatory profile of cerebellar processes behind the motor adaptation. This can be exploited in future interventions to enhance motor learning.

The dual timescales of gait adaptation: Initial stability adjustments followed by subsequent energetic cost adjustments.

Gait adaptation during bipedal walking allows people to adjust their walking patterns to maintain balance, avoid obstacles, and avoid injury. Adaptation involves complex processes that function to maintain stability and reduce energy expenditure. However, the processes that influence walking patterns during different points in the adaptation period remain to be investigated. We recruited seventeen young adults ages 19-35 to assess split-belt adaptation. We also assessed individual aerobic capacity to understand how aerobic capacity influences adaptation. We analyzed step lengths, step length asymmetry (SLA), mediolateral margins of stability, positive, negative, and net mechanical work rates, as well as metabolic rate during adaptation. We used dual-rate exponential mixed-effects regressions to estimate the adaptation of each measure over two timescales. Our results indicate that mediolateral stability adapts over a single timescale in under 1 minute, while mechanical work rates, metabolic rate, step lengths, and step length asymmetry adapt over two distinct timescales, ranging from 3.5 to 11.2 minutes. We then regressed mediolateral margins of stability, net mechanical work rate, and metabolic rate on step length asymmetry during early and late adaptation phases to determine if stability drives early adaptation and energetic cost drives late adaptation. Stability predicted SLA during the initial rapid onset of adaptation, and mechanical work rate predicted SLA during the latter part of adaptation. These findings suggest that stability optimization may contribute to early gait changes and that mechanical work contributes to later changes during adaptation. A final sub-analysis assessed the effect of aerobic capacity on step length asymmetry adaptation. Aerobic capacity levels below 36 and above 43 ml/kg/min resulted in greater adaptation, underscoring the metabolic influences on gait adaptation. This study illuminates the complex interplay between biomechanical and metabolic factors in gait adaptation, shedding light on fundamental mechanisms underlying human locomotion.

Unlike overt movement, motor imagery cannot update internal models.

In overt movement, internal models make predictions about the sensory consequences of a desired movement, generating the appropriate motor commands to achieve that movement. Using available sensory feedback, internal models are updated to allow for movement adaptation and in-turn better performance. Whether internal models are updated during motor imagery, the mental rehearsal of movement, is not well established. To investigate internal modelling during motor imagery, 66 participants were exposed to a leftwards prism shift while performing actual pointing movements (physical practice; PP), imagined pointing movements (motor imagery; MI), or no pointing movements (control). If motor imagery updates internal models, we hypothesized that aftereffects (pointing in the direction opposite the prism shift) would be observed in MI, like that of PP, and unlike that of control. After prism exposure, the magnitude of aftereffects was significant in PP (4.73° ± 1.56°), but not in MI (0.34° ± 0.96°) and control (0.34° ± 1.04°). Accordingly, PP differed significantly from MI and control. Our results show that motor imagery does not update internal models, suggesting that it is not a direct simulation of overt movement. Furthering our understanding of the mechanisms that underlie learning through motor imagery will lead to more effective applications of motor imagery.

Effect of movement-evoked and tonic experimental pain on muscle force production.

INTRODUCTION: When performing an exercise or a functional test, pain that is evoked by movement or muscle contraction could be a stronger stimulus for changing how individuals move compared to tonic pain. We investigated whether the decrease in muscle force production is larger when experimentally-induced knee pain is directly associated to the torque produced (movement-evoked) compared to a constant painful stimulation (tonic). METHODS: Twenty-one participants performed three isometric knee extension maximal voluntary contractions without pain (baseline), during pain, and after pain. Knee pain was induced using sinusoidal electrical stimuli at 10 Hz over the infrapatellar fat pad, applied continuously or modulated proportionally to the knee extension torque. Peak torque and contraction duration were averaged across repetitions and normalized to baseline. RESULTS: During tonic pain, participants reported lower pain intensity during the contraction than at rest (p < 0.001), whereas pain intensity increased with contraction during movement-evoked pain (p < 0.001). Knee extension torque decreased during both pain conditions (p < 0.001), but a larger reduction was observed during movement-evoked compared to tonic pain (p < 0.001). Participants produced torque for longer during tonic compared to movement-evoked pain (p = 0.005). CONCLUSION: Our results indicate that movement-evoked pain was a more potent stimulus to reduce knee extension torque than tonic pain. The longer contraction time observed during tonic pain may be a result of a lower perceived pain intensity during muscle contraction. Overall, our results suggest different motor adaptation to tonic and movement-evoked pain and support the notion that motor adaptation to pain is a purposeful strategy to limit pain. This mechanistic evidence suggests that individuals experiencing prevalently tonic or movement-evoked pain may exhibit different motor adaptations, which may be important for exercise prescription.

The independence of impairments in proprioception and visuomotor adaptation after stroke.

BACKGROUND: Proprioceptive impairments are common after stroke and are associated with worse motor recovery and poor rehabilitation outcomes. Motor learning may also be an important factor in motor recovery, and some evidence in healthy adults suggests that reduced proprioceptive function is associated with reductions in motor learning. It is unclear how impairments in proprioception and motor learning relate after stroke. Here we used robotics and a traditional clinical assessment to examine the link between impairments in proprioception after stroke and a type of motor learning known as visuomotor adaptation. METHODS: We recruited participants with first-time unilateral stroke and controls matched for overall age and sex. Proprioceptive impairments in the more affected arm were assessed using robotic arm position- (APM) and movement-matching (AMM) tasks. We also assessed proprioceptive impairments using a clinical scale (Thumb Localization Test; TLT). Visuomotor adaptation was assessed using a task that systematically rotated hand cursor feedback during reaching movements (VMR). We quantified how much participants adapted to the disturbance and how many trials they took to adapt to the same levels as controls. Spearman's rho was used to examine the relationship between proprioception, assessed using robotics and the TLT, and visuomotor adaptation. Data from healthy adults were used to identify participants with stroke who were impaired in proprioception and visuomotor adaptation. The independence of impairments in proprioception and adaptation were examined using Fisher's exact tests. RESULTS: Impairments in proprioception (58.3%) and adaptation (52.1%) were common in participants with stroke (n = 48; 2.10% acute, 70.8% subacute, 27.1% chronic stroke). Performance on the APM task, AMM task, and TLT scores correlated weakly with measures of visuomotor adaptation. Fisher's exact tests demonstrated that impairments in proprioception, assessed using robotics and the TLT, were independent from impairments in visuomotor adaptation in our sample. CONCLUSION: Our results suggest impairments in proprioception may be independent from impairments in visuomotor adaptation after stroke. Further studies are needed to understand factors that influence the relationship between motor learning, proprioception and other rehabilitation outcomes throughout stroke recovery.

Propulsive Force Modulation Drives Split-Belt Treadmill Adaptation in People with Multiple Sclerosis.

Most people with multiple sclerosis (PwMS) experience significant gait asymmetries between their legs during walking, leading to an increased risk of falls. Split-belt treadmill training, where the speed of each limb is controlled independently, alters each leg's stepping pattern and can improve gait symmetry in PwMS. However, the biomechanical mechanisms of this adaptation in PwMS remain poorly understood. In this study, 32 PwMS underwent a 10 min split-belt treadmill adaptation paradigm with the more affected (MA) leg moving twice as fast as the less affected (LA) leg. The most noteworthy biomechanical adaptation observed was increased peak propulsion asymmetry between the limbs. A kinematic analysis revealed that peak dorsiflexion asymmetry and the onset of plantarflexion in the MA limb were the primary contributors to the observed increases in peak propulsion. In contrast, the joints in the LA limb underwent only immediate reactive adjustments without subsequent adaptation. These findings demonstrate that modulation during gait adaptation in PwMS occurs primarily via propulsive forces and joint motions that contribute to propulsive forces. Understanding these distinct biomechanical changes during adaptation enhances our grasp of the rehabilitative impact of split-belt treadmill training, providing insights for refining therapeutic interventions aimed at improving gait symmetry.

Hypothalamic Control of Forelimb Motor Adaptation.

The ability to perform skilled arm movements is central to everyday life, as limb impairments in common neurologic disorders such as stroke demonstrate. Skilled arm movements require adaptation of motor commands based on discrepancies between desired and actual movements, called sensory errors. Studies in humans show that this involves predictive and reactive movement adaptations to the errors, and also requires a general motivation to move. How these distinct aspects map onto defined neural signals remains unclear, because of a shortage of equivalent studies in experimental animal models that permit neural-level insights. Therefore, we adapted robotic technology used in human studies to mice, enabling insights into the neural underpinnings of motivational, reactive, and predictive aspects of motor adaptation. Here, we show that forelimb motor adaptation is regulated by neurons previously implicated in motivation and arousal, but not in forelimb motor control: the hypothalamic orexin/hypocretin neurons (HONs). By studying goal-oriented mouse-robot interactions in male mice, we found distinct HON signals occur during forelimb movements and motor adaptation. Temporally-delimited optosilencing of these movement-associated HON signals impaired sensory error-based motor adaptation. Unexpectedly, optosilencing affected neither task reward or execution rates, nor motor performance in tasks that did not require adaptation, indicating that the temporally-defined HON signals studied here were distinct from signals governing general task engagement or sensorimotor control. Collectively, these results reveal a hypothalamic neural substrate regulating forelimb motor adaptation.SIGNIFICANCE STATEMENT The ability to perform skilled, adaptable movements is a fundamental part of daily life, and is impaired in common neurologic diseases such as stroke. Maintaining motor adaptation is thus of great interest, but the necessary brain components remain incompletely identified. We found that impaired motor adaptation results from disruption of cells not previously implicated in this pathology: hypothalamic orexin/hypocretin neurons (HONs). We show that temporally confined HON signals are associated with skilled movements. Without these newly-identified signals, a resistance to movement that is normally rapidly overcome leads to prolonged movement impairment. These results identify natural brain signals that enable rapid and effective motor adaptation.

Distinct adaptation processes underlie multidigit force coordination for dexterous manipulation.

The human sensorimotor system can adapt to various changes in the environmental dynamics by updating motor commands to improve performance after repeated exposure to the same task. However, the characteristics and mechanisms of the adaptation process remain unknown for dexterous manipulation, a unique motor task in which the body physically interacts with the environment with multiple effectors, i.e., digits, in parallel. We addressed this gap by using robotic manipulanda to investigate the changes in the digit force coordination following mechanical perturbation of an object held by tripod grasps. As the participants gradually adapted to lifting the object under perturbations, we quantified two components of digit force coordination. One is the direction-specific manipulation moment that directly counteracts the perturbation, whereas the other one is the direction-independent internal moment that supports the stability and stiffness of the grasp. We found that trial-to-trial improvement of task performance was associated with increased manipulation moment and a gradual decrease of the internal moment. These two moments were characterized by different rates of adaptation. We also examined how these two force coordination components respond to changes in perturbation directions. Importantly, we found that the manipulation moment was sensitive to the extent of repetitive exposure to the previous context that has an opposite perturbation direction, whereas the internal moment did not. However, the internal moment was sensitive to whether the postchange perturbation direction was previously experienced. Our results reveal, for the first time, that two distinct processes underlie the adaptation of multidigit force coordination for dexterous manipulation.NEW & NOTEWORTHY Changes in digit force coordination in multidigit object manipulation were quantified with a novel experimental design in which human participants adapted to mechanical perturbations applied to the object. Our results show that the adaptation of digit force coordination can be characterized by two distinct components that operate at different timescales. We further show that these two components respond to changes in perturbation direction differently.

Minimum effort simulations of split-belt treadmill walking exploit asymmetry to reduce metabolic energy expenditure.

Walking on a split-belt treadmill elicits an adaptation response that changes baseline step length asymmetry. The underlying causes of this adaptation, however, are difficult to determine. It has been proposed that effort minimization may drive this adaptation, based on the idea that adopting longer steps on the fast belt, or positive step length asymmetry (SLA), can cause the treadmill to exert net-positive mechanical work on a bipedal walker. However, humans walking on split-belt treadmills have not been observed to reproduce this behavior when allowed to freely adapt. To determine if an effort-minimization motor control strategy would result in experimentally observed adaptation patterns, we conducted simulations of walking on different combinations of belt speeds with a human musculoskeletal model that minimized muscle excitations and metabolic rate. The model adopted increasing amounts of positive SLA and decreased its net metabolic rate with increasing belt speed difference, reaching +42.4% SLA and -5.7% metabolic rate relative to tied-belt walking at our maximum belt speed ratio of 3:1. These gains were primarily enabled by an increase in braking work and a reduction in propulsion work on the fast belt. The results suggest that a purely effort minimization driven split-belt walking strategy would involve substantial positive SLA, and that the lack of this characteristic in human behavior points to additional factors influencing the motor control strategy, such as aversion to excessive joint loads, asymmetry, or instability.NEW & NOTEWORTHY Behavioral observations of split-belt treadmill adaptation have been inconclusive toward its underlying causes. To estimate gait patterns when driven exclusively by one of these possible underlying causes, we simulated split-belt treadmill walking with a musculoskeletal model that minimized its summed muscle excitations. Our model took significantly longer steps on the fast belt and reduced its metabolic rate below tied-belt walking, unlike experimental observations. This suggests that asymmetry is energetically optimal, but human adaptation involves additional factors.

Interaction of dynamic error signals in saccade adaptation.

Motor adaptation maintains movement accuracy. To evaluate movement accuracy, motor adaptation relies on an error signal, generated by the movement target, while suppressing error signals from irrelevant objects in the vicinity. Previous work used static testing environments, where all information required to evaluate movement accuracy was available simultaneously. Using saccadic eye movements as a model for motor adaptation, we tested how movement accuracy is maintained in dynamic environments, where the availability of conflicting error signals varied over time. Participants made a vertical saccade toward a target (either a small square or a large ring). Upon saccade detection, two candidate stimuli were shown left and right of the target, and participants were instructed to discriminate a feature on one of the candidates. Critically, candidate stimuli were presented sequentially, and saccade adaptation, thus, had to resolve a conflict between a task-relevant and a task-irrelevant error signal that were separated in space and time. We found that the saccade target influenced several aspects of oculomotor learning. In presence of a small target, saccade adaptation evaluated movement accuracy based on the first available error signal after the saccade, irrespective of its task relevance. However, a large target not only allowed for greater flexibility when evaluating movement accuracy, but it also promoted a stronger contribution of strategic behavior when compensating inaccurate saccades. Our results demonstrate how motor adaptation maintains movement accuracy in dynamic environments, and how properties of the visual environment modulate the relative contribution of different learning processes.NEW & NOTEWORTHY Motor adaptation is typically studied in static environments, where all information that is required to evaluate movement accuracy is available simultaneously. Here, using saccadic eye movements as a model, we studied motor adaptation in a dynamic environment, where the availability of conflicting information about movement accuracy varied over time. We demonstrate that properties of the visual environment determine how dynamic movement errors are corrected.