Limb-related sensory prediction errors and task-related performance errors facilitate human sensorimotor learning through separate mechanisms.

The unpredictable nature of our world can introduce a variety of errors in our actions, including sensory prediction errors (SPEs) and task performance errors (TPEs). SPEs arise when our existing internal models of limb-environment properties and interactions become miscalibrated due to changes in the environment, while TPEs occur when environmental perturbations hinder achievement of task goals. The precise mechanisms employed by the sensorimotor system to learn from such limb- and task-related errors and improve future performance are not comprehensively understood. To gain insight into these mechanisms, we performed a series of learning experiments wherein the location and size of a reach target were varied, the visual feedback of the motion was perturbed in different ways, and instructions were carefully manipulated. Our findings indicate that the mechanisms employed to compensate SPEs and TPEs are dissociable. Specifically, our results fail to support theories that suggest that TPEs trigger implicit refinement of reach plans or that their occurrence automatically modulates SPE-mediated learning. Rather, TPEs drive improved action selection, that is, the selection of verbally sensitive, volitional strategies that reduce future errors. Moreover, we find that exposure to SPEs is necessary and sufficient to trigger implicit recalibration. When SPE-mediated implicit learning and TPE-driven improved action selection combine, performance gains are larger. However, when actions are always successful and strategies are not employed, refinement in behavior is smaller. Flexibly weighting strategic action selection and implicit recalibration could thus be a way of controlling how much, and how quickly, we learn from errors.

Mechanistic determinants of effector-independent motor memory encoding.

Coordinated, purposeful movements learned with one effector generalize to another effector, a finding that has important implications for tool use, sports, performing arts, and rehabilitation. This occurs because the motor memory acquired through learning comprises representations that are effector-independent. Despite knowing this for decades, the neural mechanisms and substrates that are causally associated with the encoding of effector-independent motor memories remain poorly understood. Here we exploit intereffector generalization, the behavioral signature of effector-independent representations, to address this crucial gap. We first show in healthy human participants that postlearning generalization across effectors is principally predicted by the level of an implicit mechanism that evolves gradually during learning to produce a temporally stable memory. We then demonstrate that interfering with left but not right posterior parietal cortex (PPC) using high-definition cathodal transcranial direct current stimulation impedes learning mediated by this mechanism, thus potentially preventing the encoding of effector-independent memory components. We confirm this in our final experiment in which we show that disrupting left PPC but not primary motor cortex after learning has been allowed to occur blocks intereffector generalization. Collectively, our results reveal the key mechanism that encodes an effector-independent memory trace and uncover a central role for the PPC in its representation. The encoding of such motor memory components outside primary sensorimotor regions likely underlies a parsimonious neural organization that enables more efficient movement planning in the brain, independent of the effector used to act.

Symmetric interlimb transfer of newly acquired skilled movements.

In this study, we aimed to examine features of interlimb generalization or "transfer" of newly acquired motor skills, with a broader goal of better understanding the mechanisms mediating skill learning. Right-handed participants (n = 36) learned a motor task that required them to make very rapid but accurate reaches to one of eight randomly presented targets, thus bettering the typical speed-accuracy tradeoff. Subjects were divided into an "RL" group that first trained with the right arm and was then tested on the left and an "LR" group that trained with the left arm and was subsequently tested on the right. We found significant interlimb transfer in both groups. Remarkably, we also observed that participants learned faster with their left arm compared with the right. We hypothesized that this could be due to a previously suggested left arm/right hemisphere advantage for movements under variable task conditions. To corroborate this, we recruited two additional groups of participants (n = 22) that practiced the same task under a single target condition. This removal of task level variability eliminated learning rate differences between the arms, yet interlimb transfer remained robust and symmetric, as in the first experiment. Additionally, the strategy used to reduce errors during learning, albeit heterogeneous across subjects particularly in our second experiment, was adopted by the untrained arm. These findings may be best explained as the outcome of the operation of cognitive strategies during the early stages of motor skill learning.NEW & NOTEWORTHY How newly acquired motor skills generalize across effectors is not well understood. Here, we show that newly learned skilled actions transfer symmetrically across the arms and that task-level variability influences learning rate but not transfer magnitude or direction. Interestingly, strategies developed during learning with one arm transfer to the untrained arm. This likely reflects the outcome of learning driven by cognitive mechanisms during the initial stages of motor skill acquisition.

Laterality of Damage Influences the Relationship Between Impairment and Arm Use After Stroke.

OBJECTIVES: To investigate whether the relationship between arm use and motor impairment post-stroke is influenced by the hemisphere of damage. METHODS: Right-handed patients with unilateral left hemisphere damage (LHD) or right (RHD) (n=58; 28 LHD, 30 RHD) were recruited for this study. The Arm Motor Ability Test and Functional Impact Assessment were used to derive arm use patterns. The Fugl-Meyer motor assessment scale was used to quantify the level of motor impairment. RESULTS: A significant interaction between patient group and impairment level was observed for contralesional, but not ipsilesional arm use. For lower impairment levels, contralesional (right arm for LHD and left arm for RHD) arm use was greater in LHD than RHD patients. In contrast, for greater levels of impairment, there were no arm use differences between the two patient groups. CONCLUSIONS: When motor impairment is significant, it overrides potential effects of stroke laterality on the patterns of arm use. However, a robust influence of hemisphere of damage on the patterns of arm use is evident at lower impairment levels. This may be attributed to previously described arm preference effects. These findings suggest adoption of distinct strategies for rehabilitation following left versus right hemisphere damage in right-handers, at least when the impairment is moderate to low. (JINS, 2019, 25, 470-478).

Interference between competing motor memories developed through learning with different limbs.

Learning from motor errors that occur across different limbs is essential for effective tool use, sports training, and rehabilitation. To probe the neural organization of error-driven learning across limbs, we asked whether learning opposing visuomotor mappings with the two arms would interfere. Young right-handers first adapted to opposite visuomotor rotations A and B with different arms and were then reexposed to A 24 h later. We observed that relearning of A was never faster nor were initial errors smaller than prior A learning, which would be expected if there was no interference from B. Rather, errors were greater than or similar to, and learning rate was slower than or comparable to, previous A learning depending on the order in which the arms learned. This indicated robust interference between the motor memories of A and B when they were learned with different arms in close succession. We then proceeded to uncover that the order-dependent asymmetry in performance upon reexposure resulted from asymmetric transfer of learning from the left arm to the right but not vice versa and that the observed interference was retrograde in nature. Such retrograde interference likely occurs because the two arms require the same neural resources for learning, a suggestion consistent with that of our past work showing impaired learning following left inferior parietal damage regardless of the arm used. These results thus point to a common neural basis for formation of new motor memories with different limbs and hold significant implications for how newly formed motor memories interact. NEW & NOTEWORTHY In a series of experiments, we demonstrate robust retrograde interference between competing motor memories developed through error-based learning with different arms. These results provide evidence for shared neural resources for the acquisition of motor memories across different limbs and also suggest that practice with two effectors in close succession may not be a sound approach in either sports or rehabilitation. Such training may not allow newly acquired motor memories to be stabilized.

Motor Adaptation Deficits in Ideomotor Apraxia.

OBJECTIVES: The cardinal motor deficits seen in ideomotor limb apraxia are thought to arise from damage to internal representations for actions developed through learning and experience. However, whether apraxic patients learn to develop new representations with training is not well understood. We studied the capacity of apraxic patients for motor adaptation, a process associated with the development of a new internal representation of the relationship between movements and their sensory effects. METHODS: Thirteen healthy adults and 23 patients with left hemisphere stroke (12 apraxic, 11 nonapraxic) adapted to a 30-degree visuomotor rotation. RESULTS: While healthy and nonapraxic participants successfully adapted, apraxics did not. Rather, they showed a rapid decrease in error early but no further improvement thereafter, suggesting a deficit in the slow, but not the fast component of a dual-process model of adaptation. The magnitude of this late learning deficit was predicted by the degree of apraxia, and was correlated with the volume of damage in parietal cortex. Apraxics also demonstrated an initial after-effect similar to the other groups likely reflecting the early learning, but this after-effect was not sustained and performance returned to baseline levels more rapidly, consistent with a disrupted slow learning process. CONCLUSIONS: These findings suggest that the early phase of learning may be intact in apraxia, but this leads to the development of a fragile representation that is rapidly forgotten. The association between this deficit and left parietal damage points to a key role for this region in learning to form stable internal representations. (JINS, 2017, 23, 139-149).

The Neuropsychology of Movement and Movement Disorders: Neuroanatomical and Cognitive Considerations.

This paper highlights major developments over the past two to three decades in the neuropsychology of movement and its disorders. We focus on studies in healthy individuals and patients, which have identified cognitive contributions to movement control and animal work that has delineated the neural circuitry that makes these interactions possible. We cover advances in three major areas: (1) the neuroanatomical aspects of the "motor" system with an emphasis on multiple parallel circuits that include cortical, corticostriate, and corticocerebellar connections; (2) behavioral paradigms that have enabled an appreciation of the cognitive influences on the preparation and execution of movement; and (3) hemispheric differences (exemplified by limb praxis, motor sequencing, and motor learning). Finally, we discuss the clinical implications of this work, and make suggestions for future research in this area. (JINS, 2017, 23, 768-777).

Adaptive reliance on the most stable sensory predictions enhances perceptual feature extraction of moving stimuli.

The prediction of the sensory outcomes of action is thought to be useful for distinguishing self- vs. externally generated sensations, correcting movements when sensory feedback is delayed, and learning predictive models for motor behavior. Here, we show that aspects of another fundamental function-perception-are enhanced when they entail the contribution of predicted sensory outcomes and that this enhancement relies on the adaptive use of the most stable predictions available. We combined a motor-learning paradigm that imposes new sensory predictions with a dynamic visual search task to first show that perceptual feature extraction of a moving stimulus is poorer when it is based on sensory feedback that is misaligned with those predictions. This was possible because our novel experimental design allowed us to override the "natural" sensory predictions present when any action is performed and separately examine the influence of these two sources on perceptual feature extraction. We then show that if the new predictions induced via motor learning are unreliable, rather than just relying on sensory information for perceptual judgments, as is conventionally thought, then subjects adaptively transition to using other stable sensory predictions to maintain greater accuracy in their perceptual judgments. Finally, we show that when sensory predictions are not modified at all, these judgments are sharper when subjects combine their natural predictions with sensory feedback. Collectively, our results highlight the crucial contribution of sensory predictions to perception and also suggest that the brain intelligently integrates the most stable predictions available with sensory information to maintain high fidelity in perceptual decisions.

Contralesional motor deficits after unilateral stroke reflect hemisphere-specific control mechanisms.

We have proposed a model of motor lateralization, in which the left and right hemispheres are specialized for different aspects of motor control: the left hemisphere for predicting and accounting for limb dynamics and the right hemisphere for stabilizing limb position through impedance control mechanisms. Our previous studies, demonstrating different motor deficits in the ipsilesional arm of stroke patients with left or right hemisphere damage, provided a critical test of our model. However, motor deficits after stroke are most prominent on the contralesional side. Post-stroke rehabilitation has also, naturally, focused on improving contralesional arm impairment and function. Understanding whether contralesional motor deficits differ depending on the hemisphere of damage is, therefore, of vital importance for assessing the impact of brain damage on function and also for designing rehabilitation interventions specific to laterality of damage. We, therefore, asked whether motor deficits in the contralesional arm of unilateral stroke patients reflect hemisphere-dependent control mechanisms. Because our model of lateralization predicts that contralesional deficits will differ depending on the hemisphere of damage, this study also served as an essential assessment of our model. Stroke patients with mild to moderate hemiparesis in either the left or right arm because of contralateral stroke and healthy control subjects performed targeted multi-joint reaching movements in different directions. As predicted, our results indicated a double dissociation; although left hemisphere damage was associated with greater errors in trajectory curvature and movement direction, errors in movement extent were greatest after right hemisphere damage. Thus, our results provide the first demonstration of hemisphere specific motor control deficits in the contralesional arm of stroke patients. Our results also suggest that it is critical to consider the differential deficits induced by right or left hemisphere lesions to enhance post-stroke rehabilitation interventions.

A lateralized motor network in order to understand adaptation to visuomotor rotation.

Objective.The functional asymmetry between the two brain hemispheres in language and spatial processing is well documented. However, a description of difference in control between the two hemispheres in motor function is not well established. Our primary objective in this study was to examine the distribution of control in the motor hierarchy and its variation across hemispheres.Approach.We developed a computation model termed the bilateral control network and implemented the same in a neural network framework to be used to replicate certain experimental results. The network consists of a simple arm model capable of making movements in 2D space and a motor hierarchy with separate elements coding target location, estimated position of arm, direction, and distance to be moved by the arm, and the motor command sent to the arm. The main assumption made here is the division of direction and distance coding between the two hemispheres with distance coded in the non-dominant and direction coded in the dominant hemisphere.Main results.With this assumption, the network was able to show main results observed in visuomotor adaptation studies. Importantly it showed decrease in error exhibited by the untrained arm while the other arm underwent training compared to the corresponding naïve arm's performance-transfer of motor learning from trained to the untrained arm. It also showed how this varied depending on the performance variable used-with distance as the measure, the non-dominant arm showed transfer and with direction, dominant arm showed transfer.Significance.Our results indicate the possibility of shared control between the two hemispheres. If indeed found true, this result could have major significance in motor rehabilitation as treatment strategies will need to be designed in order to account for this and can no longer be confined to the arm contralateral to the affected hemisphere.

Hemispheric specialization for movement control produces dissociable differences in online corrections after stroke.

In this study, we examine whether corrections made during an ongoing movement are differentially affected by left hemisphere damage (LHD) and right hemisphere damage (RHD). Our hypothesis of motor lateralization proposes that control mechanisms specialized to the right hemisphere rely largely on online processes, while the left hemisphere primarily utilizes predictive mechanisms to specify optimal coordination patterns. We therefore predict that RHD, but not LHD, should impair online correction when task goals are unexpectedly changed. Fourteen stroke subjects (7 LHD, 7 RHD) and 14 healthy controls reached to 1 of the 3 targets that unexpectedly "jumped" during movement onset. RHD subjects showed a considerable delay in initiating the corrective response relative to controls and LHD subjects. However, both stroke groups made large final position errors on the target jump trials. Position deficits following LHD were associated with poor intersegmental coordination, while RHD subjects had difficulty terminating their movements appropriately. These findings confirm that RHD, but not LHD, produces a deficit in the timing of online corrections and also indicate that both stroke groups show position deficits that are related to the specialization of their damaged hemisphere. Further research is needed to identify specific neural circuits within each hemisphere critical for these processes.

Spontaneous recovery in an untrained arm as an assay of interlimb transfer of motor learning.

Motor skills learned with one effector are known to transfer to an untrained effector. However, which of the many mechanisms that drive learning principally predict interlimb transfer, is less clear. Recent studies of motor adaptation suggest that transfer is tied to the state of an implicit mechanism that evolves gradually during learning. Interestingly, this "slow" process also promotes spontaneous recovery, or adaptation rebound, when error feedback is clamped to zero following adaptation-extinction training. If this mechanism also drives transfer, then recovery must occur in an arm performing zero-error-clamp movements after adaptation-extinction training with the opposite arm. Here we show this to be the case in participants who undergo visuomotor learning with their left arm and perform error-clamp movements with the right, but not vice versa. The performance of control participants reveals that the absence of a rebound in this latter group is not due to an inability to recover past learning when using the left arm. Our findings firstly advance the view that interlimb transfer following visuomotor adaptation is asymmetric. Secondly, since spontaneous recovery is a hallmark of the slow process, they lend strong support to the idea that it is this specific mechanism that provides a gateway for post-learning transfer to occur. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Left parietal regions are critical for adaptive visuomotor control.

The question addressed in this study is whether parietal brain circuits involved in adaptation to novel visuomotor conditions are lateralized. This information is critical for characterizing the neural mechanisms mediating adaptive behavior in humans, as well as for assessing the effects of unilateral brain damage on function. Moreover, previous research has been controversial in this regard. We compared visuomotor adaptation in 10 patients with focal, unilateral, left or right parietal lesions and healthy control participants. All subjects reached to each of eight targets over three experimental sessions: a baseline session, where the visually displayed and actual hand motion were matched; an adaptation session, where the visual feedback deviated from the actual movement direction by 30°; and an after-effect session, where visual feedback was again matched to hand motion. Adaptation was primarily quantified as a change in initial movement direction throughout the adaptation session and the presence of after-effects when the rotation was removed. Patients with right parietal damage demonstrated normal adaptation and large after-effects, which was comparable to the performance of healthy controls. In contrast, patients with left parietal damage showed a clear deficit in adaptation and showed no after-effects. Thus, our results show that left but not right parietal regions are critical for visuomotor adaptation. These findings are discussed in the context that left parietal regions are critical for the modification of stored representations of the relationship between movement commands and limb and environmental state, as is thought to occur during visuomotor adaptation.

Critical neural substrates for correcting unexpected trajectory errors and learning from them.

Our proficiency at any skill is critically dependent on the ability to monitor our performance, correct errors and adapt subsequent movements so that errors are avoided in the future. In this study, we aimed to dissociate the neural substrates critical for correcting unexpected trajectory errors and learning to adapt future movements based on those errors. Twenty stroke patients with focal damage to frontal or parietal regions in the left or right brain hemispheres and 20 healthy controls performed a task in which a novel mapping between actual hand motion and its visual feedback was introduced. Only patients with frontal damage in the right hemisphere failed to correct for this discrepancy during the ongoing movement. However, these patients were able to adapt to the distortion such that their movement direction on subsequent trials improved. In contrast, only patients with parietal damage in the left hemisphere showed a clear deficit in movement adaptation, but not in online correction. Left frontal or right parietal damage did not adversely impact upon either process. Our findings thus identify, for the first time, distinct and lateralized neural substrates critical for correcting unexpected errors during ongoing movements and error-based movement adaptation.

Relationship between arm usage and instrumental activities of daily living after unilateral stroke.

OBJECTIVE: To determine whether the preferred pattern of arm use after unilateral hemispheric damage was associated with better everyday functioning. Our previous work showed that right-handed stroke patients with right hemisphere damage (RHD) used their right, ipsilesional arm most frequently, while those with left hemisphere damage (LHD) used both arms together most frequently. This effect was explained by right-hand preference, but its relationship to functional performance is not known. DESIGN: Observational cohort. SETTING: Research laboratory. PARTICIPANTS: Stroke patients (n=60; 30 RHD, 30 LHD) and healthy controls (n=52). INTERVENTIONS: Not applicable. MAIN OUTCOME MEASURES: The Functional Impact Assessment was used to assess performance on instrumental activities of daily living (IADLs). RESULTS: The preferred patterns of arm use were similar to those in our previous report. However, it was the greater use of both arms together that was associated with better IADL performance in both stroke groups. Ipsilesional arm use alone was not significantly associated with IADL performance in the RHD group and was associated with poorer performance in the LHD group. CONCLUSIONS: The modal arm use pattern did not always optimize IADL functioning. Better IADL functioning in both stroke groups was associated with the use of both arms together, which is the most common arm use pattern of healthy individuals doing these same IADLs. An important practical question that arises from these findings is whether bilateral arm rehabilitation should be emphasized, because using both arms together is the best predictor of better performance on everyday tasks.

Sensorimotor Learning in Response to Errors in Task Performance.

The human sensorimotor system is sensitive to both limb-related prediction errors and task-related performance errors. Prediction error signals are believed to drive implicit refinements to motor plans. However, an understanding of the mechanisms that performance errors stimulate has remained unclear largely because their effects have not been probed in isolation from prediction errors. Diverging from past work, we induced performance errors independent of prediction errors by shifting the location of a reach target but keeping the intended and actual kinematic consequences of the motion matched. Our first two experiments revealed that rather than implicit learning, motor adjustments in response to performance errors reflect the use of deliberative, volitional strategies. Our third experiment revealed a potential dissociation of performance-error-driven strategies based on error size. Specifically, behavioral changes following large errors were consistent with goal-directed or model-based control, known to be supported by connections between prefrontal cortex and associative striatum. In contrast, motor changes following smaller performance errors carried signatures of model-free stimulus-response learning, of the kind underpinned by pathways between motor cortical areas and sensorimotor striatum. Across all experiments, we also found remarkably faster re-learning, advocating that such "savings" is associated with retrieval of previously learned strategic error compensation and may not require a history of exposure to limb-related errors.

Shared bimanual tasks elicit bimanual reflexes during movement.

Previous research has suggested distinct predictive and reactive control mechanisms for bimanual movements compared with unimanual motion. Recent studies have extended these findings by demonstrating that movement corrections during bimanual movements might differ depending on whether or not the task is shared between the arms. We hypothesized that corrective responses during shared bimanual tasks recruit bilateral rapid feedback mechanisms such as reflexes. We tested this hypothesis by perturbing one arm as subjects performed uni- and bimanual movements. Movements were made in a virtual-reality environment in which hand position was displayed as a cursor on a screen. During bimanual motion, we provided cursor feedback either independently for each arm (independent-cursor) or such that one cursor was placed at the average location between the arms (shared-cursor). On random trials, we applied a 40 N force pulse to the right arm 100 ms after movement onset. Our results show that while reflex responses were rapidly elicited in the perturbed arm, electromyographic activity remained close to baseline levels in the unperturbed arm during the independent-cursor trials. In contrast, when the cursor was shared between the arms, reflex responses were reduced in the perturbed arm and were rapidly elicited in the unperturbed arm. Our results thus suggest that when both arms contribute to achieving the task goal, reflex responses are bilaterally elicited in response to unilateral perturbations. These results agree with and extend recent suggestions that bimanual feedback control might be modified depending on task context.

Control of velocity and position in single joint movements.

Previous research on single joint movements has lead to the development of models of control that propose that movement speed and distance are controlled through an initial pulsatile signal that can be modified in both amplitude and duration. However, the manner in which the amplitude and duration are modulated during the control of movement remains controversial. We now report two studies that were designed to differentiate the mechanisms used to control movement speed from those employed to control final position accuracy. In our first study, participants move at a series of speeds to a single spatial target. In this task, acceleration duration (pulse-width) varied substantially across speeds, and was negatively correlated with peak acceleration (pulse-height). In a second experiment, we removed the spatial target, but required movements at the three speeds similar to those used in the first study. In this task, acceleration amplitude varied extensively across the speed targets, while acceleration duration remained constant. Taken together, our current findings demonstrate that pulse-width measures can be modulated independently from pulse-height measures, and that a positive correlation between such measures is not obligatory, even when sampled across a range of movement speeds. In addition, our findings suggest that pulse-height modulation plays a primary role in controlling movement speed and specifying target distance, whereas pulse-width mechanisms are employed to correct errors in pulse-height control, as required to achieve spatial precision in final limb position.

Error Detection is Critical for Visual-Motor Corrections.

The target article (Smeets, Oostwoud Wijdenes, & Brenner, 2016) proposes that short latency responses to changes in target location during reaching reflect an unconscious, continuous, and incremental minimization of the distance between the hand and the target, which does not require detection of the change in target location. We, instead, propose that short-latency visuomotor responses invoke reflex- or startle-like mechanisms, an idea supported by evidence that such responses are both automatic and resistant to cognitive influences. In addition, the target article fails to address the biological underpinnings for the range of response latencies reported across the literature, including the circuits that might underlie the proposed sensorimotor loops. When considering the range of latencies reported in the literature, we propose that mechanisms grounded in neurophysiology should be more informative than the simple information processing perspective adopted by the target article.

Deep Breathing Practice Facilitates Retention of Newly Learned Motor Skills.

Paced deep breathing practices, a core component of a number of meditation programs, have been shown to enhance a variety of cognitive functions. However, their effects on complex processes such as memory, and in particular, formation and retention of motor memories, remain unknown. Here we show that a 30-minute session of deep, alternate-nostril breathing remarkably enhances retention of a newly learned motor skill. Healthy humans learned to accurately trace a given path within a fixed time duration. Following learning, one group of subjects (n = 16) underwent the 30-minute breathing practice while another control group (n = 14) rested for the same duration. The breathing-practice group retained the motor skill strikingly better than controls, both immediately after the breathing session and also at 24 hours. These effects were confirmed in another group (n = 10) that rested for 30 minutes post-learning, but practiced breathing after their first retention test; these subjects showed significantly better retention at 24 hours but not 30 minutes. Our results thus uncover for the first time the remarkable facilitatory effects of simple breathing practices on complex functions such as motor memory, and have important implications for sports training and neuromotor rehabilitation in which better retention of learned motor skills is highly desirable.