Pratik K. Mutha

The effects of brain lateralization on motor control and adaptation.

ABSTRACT 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.

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.

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.

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.

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.

Visual modulation of proprioceptive reflexes during movement

Previous research has demonstrated that feedback circuits such as reflexes can be tuned by setting their gains prior to movement onset during both posture and movement tasks. However, such a control strategy requires that perturbation contingencies be predicted during movement planning and that task goals remain fixed. Here we test the hypothesis that feedforward regulation of reflex circuits also occurs during the course of movement in response to changes in task goals. Participants reached to a visual target that was occasionally jumped on movement initiation, thus changing task goals. Reflex responses were elicited through a mechanical perturbation on the same trial, 100 ms after the target jump. Impedance to the perturbation was tuned to the direction of the preceding jump: reflex responses increased or decreased depending on whether the perturbation opposed or was consistent with the target jump. This modulation, although sensitive to the direction of the jump, was insensitive to jump amplitude, as tested in a follow-up experiment. Our findings thus suggest that modulation of reflex circuits occurs online, and is sensitive to changes in visual target information. In addition, our results suggest a two-level model for visuo-motor control that reflects hierarchical neural organization.

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.

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.

Coordination deficits in ideomotor apraxia during visually targeted reaching reflect impaired visuomotor transformations.

Ideomotor limb apraxia, commonly defined as a disorder of skilled, purposeful movement, is characterized by spatiotemporal deficits during a variety of actions. These deficits have been attributed to damage to, or impaired retrieval of, stored representations of learned actions, especially object-related movements. However, such deficits might also arise from impaired visuomotor transformation mechanisms that operate in parallel to or downstream from mechanisms for storage of action representations. These transformation processes convert extrinsic visual information into intrinsic neural commands appropriate for the desired motion. These processes are a key part of the movement planning process and performance errors due to inadequate transformations have been shown to increase with the dynamic complexity of the movement. This hypothesis predicts that apraxic patients should show planning deficits when reaching to visual targets, especially when the coordination and/or dynamic requirements of the task increase. Three groups (18 healthy controls, 9 non-apraxic and 9 apraxic left hemisphere damaged patients) performed reaching movements to visual targets that varied in the degree of interjoint coordination required. Relative to the other two groups, apraxic patients made larger initial direction errors and showed higher variability during their movements, especially when reaching to the target with the highest intersegmental coordination requirement. These problems were associated with poor coordination of shoulder and elbow torques early in the movement, consistent with poor movement planning. These findings suggest that the requirement to transform extrinsic visual information into intrinsic motor commands impedes the ability to accurately plan a visually targeted movement in ideomotor limb apraxia.

Relationship Between Arm Usage and Instrumental Activities of Daily Living After Unilateral Stroke

OBJECTIVEnTo 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.nnnDESIGNnObservational cohort.nnnSETTINGnResearch laboratory.nnnPARTICIPANTSnStroke patients (n=60; 30 RHD, 30 LHD) and healthy controls (n=52).nnnINTERVENTIONSnNot applicable.nnnMAIN OUTCOME MEASURESnThe Functional Impact Assessment was used to assess performance on instrumental activities of daily living (IADLs).nnnRESULTSnThe 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.nnnCONCLUSIONSnThe 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.