Post-stroke deficits in the anticipatory control and bimanual coordination during naturalistic cooperative bimanual action.

BACKGROUND: Unilateral stroke leads to asymmetric deficits in movement performance; yet its effects on naturalistic bimanual actions, a key aspect of everyday functions, are understudied. Particularly, how naturalistic bimanual actions that require the two hands to cooperatively interact with each other while manipulating a single common object are planned, executed, and coordinated after stroke is not known. In the present study, we compared the anticipatory planning, execution, and coordination of force between individuals with left and right hemisphere stroke and neurotypical controls in a naturalistic bimanual common-goal task, lifting a box. METHOD: Thirty-three individuals with chronic stroke (15 LCVA, 18 RCVA) and 8 neurotypical age-matched controls used both hands to lift a box fitted with force transducers under unweighted and weighted conditions. Primary dependent variables included measures of anticipation (peak grip and load force rate), execution (peak grip force, load force), and measures of within-hand (grip-load force coordination) and between-hand coordination (force rate cross-correlations). Primary analyses were performed using linear mixed effects modeling. Exploratory backward stepwise regression examined predictors of individual variability within participants with stroke. RESULTS: Participants with stroke, particularly the RCVA group, showed impaired scaling of grip and load force rates with the addition of weight, indicating deficits in anticipatory control. While there were no group differences in peak grip force, participants with stroke showed significant impairments in peak load force and in grip-load force coordination with specific deficits in the evolution of load force prior to object lift-off. Finally, there were differences in spatial coordination of load force rates for participants with stroke, and especially the RCVA group, as compared to controls. Unimanual motor performance of the paretic arm and hemisphere of lesion (right hemisphere) were the key predictors of impairments in anticipatory planning of grip force and bimanual coordination among participants with stroke. CONCLUSIONS: These results suggest that individuals with stroke, particularly those with right hemisphere damage, have impairments in anticipatory planning and interlimb coordination of symmetric cooperative bimanual tasks.

Linking Pain and Motor Control: Conceptualization of Movement Deficits in Patients With Painful Conditions.

When people experience or expect pain, they move differently. Pain-altered movement strategies, collectively described here as pain-related movement dysfunction (PRMD), may persist well after pain resolves and, ultimately, may result in altered kinematics and kinetics, future reinjury, and disability. Although PRMD may manifest as abnormal movements that are often evident in clinical assessment, the underlying mechanisms are complex, engaging sensory-perceptual, cognitive, psychological, and motor processes. Motor control theories provide a conceptual framework to determine, assess, and target processes that contribute to normal and abnormal movement and thus are important for physical therapy and rehabilitation practice. Contemporary understanding of motor control has evolved from reflex-based understanding to a more complex task-dependent interaction between cognitive and motor systems, each with distinct neuroanatomic substrates. Though experts have recognized the importance of motor control in the management of painful conditions, there is no comprehensive framework that explicates the processes engaged in the control of goal-directed actions, particularly in the presence of pain. This Perspective outlines sensory-perceptual, cognitive, psychological, and motor processes in the contemporary model of motor control, describing the neural substrates underlying each process and highlighting how pain and anticipation of pain influence motor control processes and consequently contribute to PRMD. Finally, potential lines of future inquiry-grounded in the contemporary model of motor control-are outlined to advance understanding and improve the assessment and treatment of PRMD. IMPACT: This Perspective proposes that approaching PRMD from a contemporary motor control perspective will uncover key mechanisms, identify treatment targets, inform assessments, and innovate treatments across sensory-perceptual, cognitive, and motor domains, all of which have the potential to improve movement and functional outcomes in patients with painful conditions.

Complex Skill Training Transfers to Improved Performance and Control of Simpler Tasks After Stroke.

BACKGROUND: Given limited therapy time, it is important to practice tasks that optimize transfer to other tasks that cannot be practiced during therapy. However, little is known about how tasks can be selected for practice to optimize generalization. OBJECTIVE: One dimension of task selection is the complexity of the task. The purpose of the current study was to test if learning of a complex motor skill with the paretic arm would transfer to a simpler unpracticed goal-directed reaching task. DESIGN: This is an observational study, repeated measures design. METHODS: Fifteen participants with mild-to-moderate stroke practiced a complex motor skill using their paretic arm for 2 consecutive days. Complex skill learning was quantified using change in the speed-accuracy trade-off from baseline to 1 day and 1 month post-practice. Motor transfer was assessed as the change in goal-directed planar reaching performance and kinematics from 2 baselines to 1 day and 1 month post-practice. Nine additional participants with stroke were recruited as the test-alone group who only participated in the transfer tests to rule out the effects of repeated testing. RESULTS: Practice improved the speed-accuracy trade-off for the practiced complex skill that was retained over a period of 1 month. Importantly, complex skill practice, but not repeated testing alone, improved the long-term performance and kinematics of the unpracticed simpler goal-directed planar reaching task. Improvements in the unpracticed transfer task (reaching) strongly correlated with improvements in the practiced complex motor skill. LIMITATIONS: We did not have a comparison stroke group that practiced task-specific reaching movements. CONCLUSIONS: Given the limited number of tasks that can be practiced during therapy, training complex tasks may have an added advantage of transfer to improved simpler task performance.

Task-Dependent Bimanual Coordination After Stroke: Relationship With Sensorimotor Impairments.

OBJECTIVES: To determine (1) bimanual coordination deficits in patients with stroke using 3-dimensional kinematic analyses as they perform naturalistic tasks requiring collaborative interaction of the 2 arms; and (2) whether bimanual coordination deficits are related to clinical measures of sensorimotor impairments and unimanual performance of the paretic arm. DESIGN: Case-control study. SETTING: Rehabilitation hospital research institute. PARTICIPANTS: Participants (N=24) were patients with unilateral chronic stroke (n=14) and age-matched controls (n=10). INTERVENTIONS: Not applicable. MAIN OUTCOME MEASURES: Temporal coordination between the 2 hands as participants performed (1) a symmetric task: reach to pick up a box using both hands; and (2) an asymmetric task: open a drawer with 1 hand to press a button inside with the other hand. RESULTS: During the symmetric task, patients and controls showed preserved temporal coupling while transporting the hands to the box. However, on reaching the box, patients demonstrated an impaired ability to cooperatively interact their 2 arms for an efficient pickup. This led to significantly longer pickup times compared with controls. Pickup time positively correlated with proprioceptive deficits of the paretic arm. During the asymmetric task, patients had a longer time delay between drawer opening and button pressing movements than controls. The deficits in asymmetric coordination did not significantly correlate with sensorimotor impairments or unimanual paretic arm performance. CONCLUSIONS: Bimanual coordination was impaired in patients poststroke during symmetric and asymmetric bimanual tasks that required cooperative interaction between the 2 arms. While the proprioceptive system contributes to symmetric cooperative coordination, commonly tested measures of paretic arm impairment or performance, or both, do not strongly predict deficits in bimanual coordination.

Reduced asymmetry in motor skill learning in left-handed compared to right-handed individuals.

Hemispheric specialization for motor control influences how individuals perform and adapt to goal-directed movements. In contrast to adaptation, motor skill learning involves a process wherein one learns to synthesize novel movement capabilities in absence of perturbation such that they are performed with greater accuracy, consistency and efficiency. Here, we investigated manual asymmetry in acquisition and retention of a complex motor skill that requires speed and accuracy for optimal performance in right-handed and left-handed individuals. We further determined if degree of handedness influences motor skill learning. Ten right-handed (RH) and 10 left-handed (LH) adults practiced two distinct motor skills with their dominant or nondominant arms during separate sessions two-four weeks apart. Learning was quantified by changes in the speed-accuracy tradeoff function measured at baseline and one-day retention. Manual asymmetry was evident in the RH group but not the LH group. RH group demonstrated significantly greater skill improvement for their dominant-right hand than their nondominant-left hand. In contrast, for the LH group, both dominant and nondominant hands demonstrated comparable learning. Less strongly-LH individuals (lower EHI scores) exhibited more learning of their dominant hand. These results suggest that while hemispheric specialization influences motor skill learning, these effects may be influenced by handedness.

Recurrence quantification analysis of surface electromyogram supports alterations in motor unit recruitment strategies by anodal transcranial direct current stimulation.

PURPOSE: Recent evidence indicates that anodal transcranial direct current stimulation (tDCS) can selectively alter the EMG/force relationship of agonist arm muscles; however, the mechanisms mediating those changes are less clear. The purpose of this study was to evaluate the effect of anodal tDCS on motor unit synchronization by using a sophisticated non-linear EMG analysis called recurrence quantification analysis (RQA). METHODS: Surface EMG signals were collected from the biceps brachii muscle of eighteen healthy young adults (9 tDCS and 9 control) at various force levels (12.5%, 25%, 37.5%, and 50% maximum) before and after the application of anodal tDCS over the primary motor cortex. RQA was employed to quantify the changes in percentage of determinism (% DET) and laminarity (% LAM) of the surface EMG signals, which are surrogate measures of motor unit synchronization. RESULTS: RQA analyses indicated that the changes in % DET and % LAM scores were significantly higher in the tDCS group than in the control group (p < 0.05) and this effect was particularly pronounced at higher force levels. CONCLUSION: The results of this study provide novel evidence supporting that anodal tDCS significantly alters motor unit firing strategies (i.e., the degree of synchronization) of the biceps brachii muscle.

Timing of motor cortical stimulation during planar robotic training differentially impacts neuroplasticity in older adults.

OBJECTIVE: The objective was to determine how stimulation timing applied during reaching influenced neuroplasticity related to practice. Older adult participants were studied to increase relevance for stroke rehabilitation and aging. METHODS: Sixteen participants completed 3 sessions of a reaching intervention with 480 planar robotic movement trials. Sub-threshold, single-pulse transcranial magnetic stimulations (TMS) were delivered during the late reaction time (LRT) period, when muscle activity exceeded a threshold (EMG-triggered), or randomly. Assessments included motor evoked potentials (MEP), amplitude, and direction of supra-threshold TMS-evoked movements and were calculated as change scores from baseline. RESULTS: The direction of TMS-evoked movements significantly changed after reaching practice (p<0.05), but was not significantly different between conditions. Movement amplitude changes were significantly different between conditions (p<0.05), with significant increases following the LRT and random conditions. MEP for elbow extensors and flexors, and the shoulder muscle that opposed the practice movement were significantly different between conditions with positive changes following LRT, negative changes following EMG-triggered, and no changes following the random condition. Motor performance including movement time and peak velocity significantly improved following the training but did not differ between conditions. CONCLUSIONS: The responsiveness of the motor cortex to stimulation was affected positively by stimulation during the late motor response period and negatively during the early movement period, when stimulation was combined with robotic reach practice. SIGNIFICANCE: The sensitivity of the activated motor cortex to additional stimulation is highly dynamic.

Anodal transcranial direct current stimulation alters elbow flexor muscle recruitment strategies.

BACKGROUND: Transcranial direct current stimulation (tDCS) is known to reliably alter motor cortical excitability in a polarity dependent fashion such that anodal stimulation increases cortical excitability and cathodal stimulation inhibits cortical excitability. However, the effect of tDCS on agonist and antagonist volitional muscle activation is currently not known. OBJECTIVE: This study investigated the effect of motor cortical anodal tDCS on EMG/force relationships of biceps brachii (agonist) and triceps brachii (antagonist) using surface electromyography (EMG). METHODS: Eighteen neurologically intact adults (9 tDCS and 9 controls) participated in this study. EMG/force relationships were established by having subjects perform submaximal isometric contractions at several force levels (12.5%, 25%, 37.5%, and 50% of maximum). RESULTS: Results showed that anodal tDCS significantly affected the EMG/force relationship of the biceps brachii muscle. Specifically, anodal tDCS increased the magnitude of biceps brachii activation at 37.5% and 50% of maximum. Anodal tDCS also resulted in an increase in the peak force and EMG values during maximal contractions as compared to the control condition. EMG analyses of other elbow muscles indicated that the increase in biceps brachii activation after anodal tDCS was not related to alterations in synergistic or antagonistic muscle activity. CONCLUSIONS: Our results indicate that anodal tDCS significantly affects the voluntary EMG/force relationship of the agonist muscles without altering the coactivation of the antagonistic muscles. The most likely explanation for the observed greater EMG per unit force after anodal tDCS appears to be related to alterations in motor unit recruitment strategies.

Motor learning in children with hemiplegic cerebral palsy: feedback effects on skill acquisition.

AIM: Motor learning is enhanced with practice and feedback. This cohort control study investigated the effect of different relative feedback frequencies during skill acquisition in children with cerebral palsy (CP) and children with typical development. METHOD: Nineteen children with spastic hemiplegic CP (nine males, 10 females; mean age 11 y 7 mo; range 8-16 y) and 20 children with typical development (12 males, eight females; mean age 10 y 8 mo; range 8-14 y) were assigned to 100% or reduced (62%) feedback subgroups as they practised 200 trials of a discrete arm movement with specific spatiotemporal parameters. Children with CP used their less involved hand. Learning was inferred by delayed (24 h) retention and reacquisition tests. RESULTS: All children improved in accuracy and consistency. Children with typical development demonstrated significantly greater accuracy than children with CP during acquisition (p=0.001), retention (p=0.031), and reacquisition (p=0.001), and greater consistency during retention (p=0.038). The typically developing group who received 100% feedback performed with significantly less error than the 62% feedback group during acquisition (p=0.001), and with greater retention (p=0.017). No statistically significant difference was found between feedback subgroups of children with CP, although the 100% feedback group consistently demonstrated less error. INTERPRETATION: Children with CP use feedback in a manner similar to children with typical development when learning new skills with their less involved hand, but demonstrate less accuracy and consistency.

Posture-related modulations in motor cortical excitability of the proximal and distal arm muscles.

The effect of postural orientation on the motor corticospinal excitability (MCE) of proximal and distal upper extremity (UE) muscles was investigated. In a crossover design, recruitment curves (RCs), short interval cortical inhibition (SICI) and intracortical facilitation (ICF) of resting anterior deltoid (AD) and first dorsal interosseus (FDI) was assessed in two postures: sitting and standing. Six healthy adults without contraindications to transcranial magnetic stimulation (TMS) participated in the study. TMS was applied over the motor cortical representation of FDI and AD at intensities ranging from 90% to 200% of resting motor threshold (RMT) in increments of 10%. SICI and ICF were assessed for each muscle using a conditioning stimulus (80% RMT) preceding a test stimulus (120% RMT) with an interstimulus interval of 2 ms and 15 ms, respectively. For AD, but not FDI, there was a significant and consistent increase in RC slope during standing compared to sitting. For FDI, there was no difference in ICF and SICI between sitting and standing. However, for AD, while there was no difference in ICF between the two postures, there was a clear trend for SICI to decrease (p=0.06) in standing compared to sitting. These results indicate that postural change from sitting to standing, affects the MCE of proximal but not distal muscles. While this indicates the role of proximal UE muscles in postural control, it also implies that rehabilitation protocols for enhancing proximal arm motor function may be advantaged if administered in a standing posture.

Active robotic training improves locomotor function in a stroke survivor.

BACKGROUND: Clinical outcomes after robotic training are often not superior to conventional therapy. One key factor responsible for this is the use of control strategies that provide substantial guidance. This strategy not only leads to a reduction in volitional physical effort, but also interferes with motor relearning. METHODS: We tested the feasibility of a novel training approach (active robotic training) using a powered gait orthosis (Lokomat) in mitigating post-stroke gait impairments of a 52-year-old male stroke survivor. This gait training paradigm combined patient-cooperative robot-aided walking with a target-tracking task. The training lasted for 4-weeks (12 visits, 3 × per week). The subject's neuromotor performance and recovery were evaluated using biomechanical, neuromuscular and clinical measures recorded at various time-points (pre-training, post-training, and 6-weeks after training). RESULTS: Active robotic training resulted in considerable increase in target-tracking accuracy and reduction in the kinematic variability of ankle trajectory during robot-aided treadmill walking. These improvements also transferred to overground walking as characterized by larger propulsive forces and more symmetric ground reaction forces (GRFs). Training also resulted in improvements in muscle coordination, which resembled patterns observed in healthy controls. These changes were accompanied by a reduction in motor cortical excitability (MCE) of the vastus medialis, medial hamstrings, and gluteus medius muscles during treadmill walking. Importantly, active robotic training resulted in substantial improvements in several standard clinical and functional parameters. These improvements persisted during the follow-up evaluation at 6 weeks. CONCLUSIONS: The results indicate that active robotic training appears to be a promising way of facilitating gait and physical function in moderately impaired stroke survivors.

Movement pattern and parameter learning in children: effects of feedback frequency.

Reduced feedback during practice has been shown to be detrimental to movement accuracy in children but not in young adults. We hypothesized that the reduced accuracy is attributable to reduced movement parameter learning but not pattern learning in children. A rapid arm movement task that required the acquisition of a motorpattern scaled to specific spatial and temporal parameters was used to investigate the effects of feedback (FB) frequency (100% vs. 62% faded) on motor learning differences between 19 school-age children and 19 young adults. Adults and children practiced the task for 200 trials under the 100% or faded FB condition on day 1 and returned on day 2 for a no-FB retention test. On the retention test, children who practiced with reduced feedback performed with greater temporal parameter errors, but not pattern error than children who received frequent feedback. Motor skill learning in children is influenced byfeedback frequency during practice that affects parameter learning but not pattern learning.

Primary motor and premotor cortex in implicit sequence learning--evidence for competition between implicit and explicit human motor memory systems.

Implicit and explicit memory systems for motor skills compete with each other during and after motor practice. Primary motor cortex (M1) is known to be engaged during implicit motor learning, while dorsal premotor cortex (PMd) is critical for explicit learning. To elucidate the neural substrates underlying the interaction between implicit and explicit memory systems, adults underwent a randomized crossover experiment of anodal transcranial direct current stimulation (AtDCS) applied over M1, PMd or sham stimulation during implicit motor sequence (serial reaction time task, SRTT) practice. We hypothesized that M1-AtDCS during practice will enhance online performance and offline learning of the implicit motor sequence. In contrast, we also hypothesized that PMd-AtDCS will attenuate performance and retention of the implicit motor sequence. Implicit sequence performance was assessed at baseline, at the end of acquisition (EoA), and 24 h after practice (retention test, RET). M1-AtDCS during practice significantly improved practice performance and supported offline stabilization compared with Sham tDCS. Performance change from EoA to RET revealed that PMd-AtDCS during practice attenuated offline stabilization compared with M1-AtDCS and sham stimulation. The results support the role of M1 in implementing online performance gains and offline stabilization for implicit motor sequence learning. In contrast, enhancing the activity within explicit motor memory network nodes such as the PMd during practice may be detrimental to offline stabilization of the learned implicit motor sequence. These results support the notion of competition between implicit and explicit motor memory systems and identify underlying neural substrates that are engaged in this competition.

Learning-performance distinction and memory processes for motor skills: a focused review and perspective.

Behavioral research in cognitive psychology provides evidence for an important distinction between immediate performance that accompanies practice and long-term performance that reflects the relative permanence in the capability for the practiced skill (i.e. learning). This learning-performance distinction is strikingly evident when challenging practice conditions may impair practice performance, but enhance long-term retention of motor skills. A review of motor learning studies with a specific focus on comparing differences in performance between that at the end of practice and at delayed retention suggests that the delayed retention or transfer performance is a better indicator of motor learning than the performance at (or end of) practice. This provides objective evidence for the learning-performance distinction. This behavioral evidence coupled with an understanding of the motor memory processes of encoding, consolidation and retrieval may provide insight into the putative mechanism that implements the learning-performance distinction. Here, we propose a simplistic empirically-based framework--motor behavior-memory framework--that integrates the temporal evolution of motor memory processes with the time course of practice and delayed retention frequently used in behavioral motor learning paradigms. In the context of the proposed framework, recent research has used noninvasive brain stimulation to decipher the role of each motor memory process, and specific cortical brain regions engaged in motor performance and learning. Such findings provide beginning insights into the relationship between the time course of practice-induced performance changes and motor memory processes. This in turn has promising implications for future research and practical applications.

Rewiring the brain: potential role of the premotor cortex in motor control, learning, and recovery of function following brain injury.

The brain is a plastic organ with a capability to reorganize in response to behavior and/or injury. Following injury to the motor cortex or emergent corticospinal pathways, recovery of function depends on the capacity of surviving anatomical resources to recover and repair in response to task-specific training. One such area implicated in poststroke reorganization to promote recovery of upper extremity recovery is the premotor cortex (PMC). This study reviews the role of distinct subdivisions of PMC: dorsal (PMd) and ventral (PMv) premotor cortices as critical anatomical and physiological nodes within the neural networks for the control and learning of goal-oriented reach and grasp actions in healthy individuals and individuals with stroke. Based on evidence emerging from studies of intrinsic and extrinsic connectivity, transcranial magnetic stimulation, functional neuroimaging, and experimental studies in animals and humans, the authors propose 2 distinct patterns of reorganization that differentially engage ipsilesional and contralesional PMC. Research directions that may offer further insights into the role of PMC in motor control, learning, and poststroke recovery are also proposed. This research may facilitate neuroplasticity for maximal recovery of function following brain injury.

Transfer of motor learning engages specific neural substrates during motor memory consolidation dependent on the practice structure.

The authors investigated how brain activity during motor-memory consolidation contributes to transfer of learning to novel versions of a motor skill following distinct practice structures. They used 1 Hz repetitive Transcranial Magnetic Stimulation (rTMS) immediately after constant or variable practice of an arm movement skill to interfere with primary motor cortex (M1) or dorsolateral prefrontal cortex (DLPFC). The effect of interference was assessed through skill performance on two transfer targets: one within and one outside the range of practiced movement parameters for the variable practice group. For the control (no rTMS) group, variable practice benefited delayed transfer performance more than constant practice. The rTMS effect on delayed transfer performance differed for the two transfer targets. For the within-range target, rTMS interference had no significant affect on the delayed transfer after either practice structure. However, for the outside-range target, rTMS interference to DLPFC but not M1 attenuated delayed transfer benefit following variable practice. Additionally, for the outside-range target, rTMS interference to M1 but not DLPFC attenuated delayed transfer following constant practice. This suggests that variable practice may promote reliance on DLPFC for memory consolidation associated with outside-range transfer of learning, whereas constant practice may promote reliance on M1 for consolidation and long-term transfer.

Neural substrates of motor memory consolidation depend on practice structure.

Motor-skill practice drives subsequent offline activity in functionally related resting human brain networks. We investigated the manner in which offline neural networks are modulated by practice structures that affect motor-skill retention. Interference to dorsolateral-prefrontal cortex (DLPFC), but not to primary motor cortex (M1), after variable practice attenuated motor-skill retention, whereas interference to M1, but not to DLPFC, after constant practice attenuated motor-skill retention. We conclude that neural substrates of motor-memory consolidation are modulated by practice structure.

Motor learning in children: feedback effects on skill acquisition.

BACKGROUND AND PURPOSE: Reduced feedback during motor skill practice benefits motor learning. However, it is unknown whether these findings can be applied to motor learning in children, given that children have different information-processing capabilities than adults. The purpose of this study was to determine the effect of different relative frequencies of feedback on skill acquisition in children compared with young adults. SUBJECTS: The participants were 20 young adults and 20 children. METHODS: All participants practiced 200 trials of a discrete arm movement with specific spatiotemporal parameters. Participants from each group (adults and children) were randomly assigned to either a 100% feedback group or a reduced (62% faded) feedback group. Learning was inferred from the performance on the delayed (24-hour) retention and reacquisition tests. RESULTS: All participants improved accuracy and consistency across practice trials. During practice, the adults performed with significantly less error than the children. Adults who practiced with reduced feedback performed with increased consistency during the retention test compared with those who practiced with 100% feedback. In contrast, children who received reduced feedback during practice performed with less accuracy and consistency during the retention test than those who received 100% feedback. However, when feedback was reintroduced during the reacquisition test, the children in the reduced feedback group were able to improve their performance comparable to those in the 100% feedback group. DISCUSSION AND CONCLUSION: During motor learning, children use feedback in a manner different from that of adults. To optimize motor learning, children may require longer periods of practice, with feedback reduced more gradually, compared with young adults.