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Motor Learning in Stroke: Trained Patients Are Not Equal to Untrained Patients With Less Impairment

ABSTRACT: Stroke rehabilitation assumes motor learning contributes to motor recovery, yet motor learning in stroke has received little systematic investigation. Here we aimed to illustrate that despite matching levels of performance on a task, a trained patient should not be considered equal to an untrained patient with less impairment.We examined motor learning in healthy control participants and groups of stroke survivors with mild-to-moderate or moderate-to-severe motor impairment. Participants performed a series of isometric contractions of the elbow flexors to navigate an on-screen cursor to different targets, and trained to perform this task over a 4-day period. The speed-accuracy trade-off function (SAF) was assessed for each group, controlling for differences in self-selected movement speeds between individuals.The initial SAF for each group was proportional to their impairment. All groups were able to improve their performance through skill acquisition. Interestingly, training led the moderate-to-severe group to match the untrained (baseline) performance of the mild-to-moderate group, while the trained mild-to-moderate group matched the untrained (baseline) performance of the controls. Critically, this did not make the two groups equivalent; they differed in their capacity to improve beyond this matched performance level. Specifically, the trained groups had reached a plateau, while the untrained groups had not.Despite matching levels of performance on a task, a trained patient is not equal to an untrained patient with less impairment. This has important implications for decisions both on the focus of rehabilitation efforts for chronic stroke, as well as for returning to work and other activities.

SUBMITTER: Hardwick RM

PROVIDER: S-EPMC5292612 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Motor Learning in Stroke: Trained Patients Are Not Equal to Untrained Patients With Less Impairment

Hardwick Robert M RM Rajan Vikram A VA Bastian Amy J AJ Krakauer John W JW Celnik Pablo A PA

Neurorehabilitation and neural repair 20161028 2

<h4>Background and objective</h4>Stroke rehabilitation assumes motor learning contributes to motor recovery, yet motor learning in stroke has received little systematic investigation. Here we aimed to illustrate that despite matching levels of performance on a task, a trained patient should not be considered equal to an untrained patient with less impairment.<h4>Methods</h4>We examined motor learning in healthy control participants and groups of stroke survivors with mild-to-moderate or moderate ...[more]

PMID: 27789762

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Project description:Previous motor learning studies based on adapting movements of the hemiparetic arm in stroke subjects have not accounted for spasticity occurring in specific joint ranges (spasticity zones), resulting in equivocal conclusions about learning capacity. We compared the ability of participants with stroke to rapidly adapt elbow extension movements to changing external load conditions outside and inside spasticity zones. Participants with stroke ( n = 12, aged 57.8 ± 9.6 yr) and healthy age-matched controls ( n = 8, 63.5 ± 9.1 yr) made rapid 40°-50° horizontal elbow extension movements from an initial (3°) to a final (6°) target. Sixteen blocks (6-10 trials/block) consisting of alternating loaded (30% maximal voluntary contraction) and nonloaded trials were made in one (controls) or two sessions (stroke; 1 wk apart). For the stroke group, the tonic stretch reflex threshold angle at which elbow flexors began to be activated during passive elbow extension was used to identify the beginning of the spasticity zone. The task was repeated in joint ranges that did or did not include the spasticity zone. Error correction strategies were identified by the angular positions before correction and compared between groups and sessions. Changes in load condition from no load to load and vice versa resulted in undershoot and overshoot errors, respectively. Stroke subjects corrected errors in 1-4 trials compared with 1-2 trials in controls. When movements did not include the spasticity zone, there was an immediate decrease in the number of trials needed to restore accuracy, suggesting that the capacity to learn may be preserved after stroke but masked by the presence of spasticity. NEW & NOTEWORTHY When arm movements were made outside, instead of inside, the range affected by spasticity, there was an immediate decrease in the number of trials needed to restore accuracy in response to a change in the external load. This suggests that motor learning processes may be preserved in patients with stroke but masked by the presence of spasticity in specific joint ranges. This has important implications for designing rehabilitation interventions predicated on motor learning principles.

Project description:Motor skill learning is critical in post-stroke motor recovery, but little is known about its underlying neural substrates. Recently, using a new visuomotor skill learning paradigm involving a speed/accuracy trade-off in healthy individuals we identified three subpopulations based on their behavioral trajectories: fitters (in whom improvement in speed or accuracy coincided with deterioration in the other parameter), shifters (in whom speed and/or accuracy improved without degradation of the other parameter), and non-learners. We aimed to identify the neural substrates underlying the first stages of motor skill learning in chronic hemiparetic stroke patients and to determine whether specific neural substrates were recruited in shifters versus fitters. During functional magnetic resonance imaging (fMRI), 23 patients learned the visuomotor skill with their paretic upper limb. In the whole-group analysis, correlation between activation and motor skill learning was restricted to the dorsal prefrontal cortex of the damaged hemisphere (DLPFCdamh: r = -0.82) and the dorsal premotor cortex (PMddamh: r = 0.70); the correlations was much lesser (-0.16 < r > 0.25) in the other regions of interest. In a subgroup analysis, significant activation was restricted to bilateral posterior parietal cortices of the fitters and did not correlate with motor skill learning. Conversely, in shifters significant activation occurred in the primary sensorimotor cortexdamh and supplementary motor areadamh and in bilateral PMd where activation changes correlated significantly with motor skill learning (r = 0.91). Finally, resting-state activity acquired before learning showed a higher functional connectivity in the salience network of shifters compared with fitters (qFDR < 0.05). These data suggest a neuroplastic compensatory reorganization of brain activity underlying the first stages of motor skill learning with the paretic upper limb in chronic hemiparetic stroke patients, with a key role of bilateral PMd.

Project description:BackgroundCognitive difficulties are the most common neurological complications in neurofibromatosis type 1 (NF1) patients. Recent animal models proposed increased GABA-mediated inhibition as one underlying mechanism directly affecting the induction of long-term potentiation (LTP) and learning. In most adult NF1 patients, apparent cognitive and attentional deficits, tumors affecting the nervous system and other confounding factors for neuroscientific studies are difficult to control for. Here we used a highly specific group of adult NF1 patients without cognitive or nervous system impairments. Such selected NF1 patients allowed us to address the following open questions: Is the learning process of acquiring a challenging motor skill impaired in NF1 patients? And is such an impairment in relation to differences in intracortical inhibition?MethodsWe used an established non-invasive, double-pulse transcranial magnetic stimulation (dp-TMS) paradigm to assess practice-related modulation of intracortical inhibition, possibly mediated by gamma-minobutyric acid (GABA)ergic-neurotransmission. This was done during an extended learning paradigm in a group of NF1 patients without any neuropsychological deficits, functioning normally in daily life and compared them to healthy age-matched controls.FindingsNF1 patients experienced substantial decline in motor skill acquisition (F = 9.2, p = 0.008) over five-consecutives training days mediated through a selective reduction in the early acquisition (online) and the consolidation (offline) phase. Furthermore, there was a consistent decrease in task-related intracortical inhibition as a function of the magnitude of learning (T = 2.8, p = 0.014), especially evident after the early acquisition phase.InterpretationsCollectively, the present results provide evidence that learning of a motor skill is impaired even in clinically intact NF1 patients based, at least partially, on a GABAergic-cortical dysfunctioning as suggested in previous animal work.

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Motor Learning in Stroke: Trained Patients Are Not Equal to Untrained Patients With Less Impairment

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Motor Learning in Stroke: Trained Patients Are Not Equal to Untrained Patients With Less Impairment

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