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).

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.

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.

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.

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.

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).

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).

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.

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.

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.

Learning of bimanual motor sequences in normal aging.

While it is well accepted that motor performance declines with age, the ability to learn simple procedural motor tasks appears to remain intact to some extent in normal aging. Here we examined the impact of aging on the acquisition of a simple sequence of bimanual actions. We further asked whether such learning results from an overall decrease in response time or is also associated with improved coordination between the hands. Healthy young and old individuals performed a bimanual version of the classic serial reaction time task. We found no learning deficit in older adults and noted that older subjects were able to learn as much as young participants. We also observed that learning in both groups was associated with an overall decrease in response time, but switch cost, the increase in response time when a switch in hands was required during sequence execution, did not decrease with learning. Surprisingly however, overall switch cost was lower in the older group compared to the younger subjects. These findings are discussed in the context of interactions between procedural and declarative memory, reduced interhemispheric inhibition and more symmetric cortical activation during motor performance in normal aging.

The influence of visual target information on the online control of movements.

The continuously changing properties of our environment require constant monitoring of our actions and updating of our motor commands based on the task goals. Such updating relies upon our predictions about the sensory consequences of our movement commands, as well as sensory feedback received during movement execution. Here we focus on how visual information about target location is used to update and guide ongoing actions so that the task goal is successfully achieved. We review several studies that have manipulated vision of the target in a variety of ways, ranging from complete removal of visual target information to changes in visual target properties after movement onset to examine how such changes are accounted for during motor execution. We also examined the specific role of a critical neural structure, the parietal cortex, and argue that a fundamental challenge for the future is to understand how visual information about target location is integrated with other streams of information, during movement execution, to estimate the state of the body and the environment in order to ensure optimal motor performance.

Frontal and parietal cortex contributions to action modification.

Successful achievement of task goals depends critically on the ability to adjust ongoing actions in response to environmental changes. The neural substrates underlying action modification have been a topic of great controversy: both, posterior parietal cortex and frontal regions, particularly prefrontal cortex have been previously identified as crucial in this regard, with most studies arguing in favor of one or the other. We aimed to address this controversy and understand whether frontal and parietal regions might play distinct roles during action modification. We tested ipsilesional arm performance of 27 stroke patients with focal lesions to frontal or parietal regions of the left or right cerebral hemisphere, and left or right arm performance of 18 healthy subjects on the classic double-step task in which a target is unpredictably displaced to a new location, requiring modification of the ongoing action. Only right hemisphere frontal lesions adversely impacted the timing of initiation of the modified response, while only left hemisphere parietal lesions impaired the accuracy of the modified action. Patients with right frontal lesions tended to complete the ongoing action to the initially displayed baseline target and initiated the new movement after a significant delay. In contrast, patients with left parietal damage did not accurately reach the new target location, but compared to the other groups, initiated the new action during an earlier phase of motion, before their baseline action was complete. Our findings thus suggest distinct, hemisphere specific contributions of frontal and parietal regions to action modification, and bring together, for the first time, disparate sets of prior findings about its underlying neural substrates.

Rethinking motor lateralization: specialized but complementary mechanisms for motor control of each arm.

Motor lateralization in humans has primarily been characterized as "handedness", resulting in the view that one arm-hemisphere system is specialized for all aspects of movement while the other is simply a weaker analogue. We have proposed an alternative view that motor lateralization reflects proficiency of each arm for complementary functions that arises from a specialization of each hemisphere for distinct movement control mechanisms. However, before this idea of hemispheric specialization can be accepted, it is necessary to precisely identify these distinct, lateralized mechanisms. Here we show in right-handers that dominant arm movements rely on predictive mechanisms that anticipate and account for the dynamic properties of the arm, while the non-dominant arm optimizes positional stability by specifying impedance around equilibrium positions. In a targeted-reaching paradigm, we covertly and occasionally shifted the hand starting location either orthogonal to or collinear with a particular direction of movement. On trials on which the start positions were shifted orthogonally, we did not notice any strong interlimb differences. However, on trials on which start positions were shifted orthogonally, the dominant arm largely maintained the direction and straightness of its trajectory, while the non-dominant arm deviated towards the previously learned goal position, consistent with the hypothesized control specialization of each arm-hemisphere system. These results bring together two competing theories about mechanisms of movement control, and suggest that they coexist in the brain in different hemispheres. These findings also question the traditional view of handedness, because specialized mechanisms for each arm-hemisphere system were identified within a group of right-handers. It is likely that such hemispheric specialization emerged to accommodate increasing motor complexity during evolution.

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.

The effects of brain lateralization on motor control and adaptation.

Lateralization of mechanisms mediating functions such as language and perception is widely accepted as a fundamental feature of neural organization. Recent research has revealed that a similar organization exists for the control of motor actions, in that each brain hemisphere contributes unique control mechanisms to the movements of each arm. The authors review present research that addresses the nature of the control mechanisms that are lateralized to each hemisphere and how they impact motor adaptation and learning. In general, the studies suggest an enhanced role for the left hemisphere during adaptation, and the learning of new sequences and skills. The authors suggest that this specialization emerges from a left hemisphere specialization for predictive control-the ability to effectively plan and coordinate motor actions, possibly by optimizing certain cost functions. In contrast, right hemisphere circuits appear to be important for updating ongoing actions and stopping at a goal position, through modulation of sensorimotor stabilization mechanisms such as reflexes. The authors also propose that each brain hemisphere contributes its mechanism to the control of both arms. They also discuss the potential advantages of such a lateralized control system.

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.

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.