Stroke is a leading cause of disability in the United States. While restoring voluntary control of skilled reaching and grasping movements is often a primary goal, 60% of stroke survivors continue to have significant upper extremity (UE) disability after 6 months.1,2 Previous reports have suggested that the potential for recovery of UE function is limited to only the first year post-stroke3 and that only compensatory strategies are possible if the initial paresis is severe.4 Subsequently, traditional rehabilitation interventions are often attempted only during the initial 12-month time period following injury.
However, more recent evidence from studies of neuroplasticity suggest that changes in motor behavior continuously occur across the lifespan with task practice or under different motor learning conditions.5–11 The central nervous system dynamically adapts throughout life in response to ever-changing situations within both the internal and external environment.8,10 Behaviorally-induced structural and functional cortical reorganization after stroke has also been observed initially after the injury.11–14 Thus, perhaps neuroplasticity is also possible at any point following the stroke, if specified conditions or meaningful and relevant environmental contexts are present during practice.15–18
Generally, clinical rehabilitation studies that demonstrate therapeutic benefits for individuals with chronic stroke include only subjects with a moderate degree of wrist and/or finger extensor ability.19–22 Therefore, the potential for improving UE motor performance for chronic stroke survivors with severe hand dysfunction is unclear. Theoretically, neuroplasticity concepts would suggest that some improvement of all functional movements may be possible after stroke, regardless of severity, if extensive learning and consistent practice occurs.23–25 However, to date, this theory has not been systematically tested in humans post-stroke. Alternatively, functional improvement after stroke may be linked to the timing of the intervention, level of disability, and specificity of treatment.26,27
Theoretically, neuromuscular electrical stimulation (NMES) delivered through the skin over motoneuronal innervations activates the Ia muscle afferents, Ib afferents of Golgi tendon organs, and cutaneous afferent nerve fibers.28,29 NMES has long been available as a rehabilitation tool. In healthy subjects, NMES drives both motor and somatosensory cortical reorganization that outlasts a short simulation period.30–32 Although the results are mixed, a meta-analysis of randomized clinical trials by deKroon et al33 could not conclusively determine the benefit of NMES for improving upper extremity function post-stroke. Overall, there is strong evidence that NMES aids in motor performance after stroke injury, although the greatest therapeutic benefit may be confined to the subset of individuals who already possess some volitional wrist and hand movements. For example, mild to moderately impaired stroke survivors significantly benefit from NMES therapy applied to the upper extremity.21,22,30–37 A more recent report indicates that subjects with chronic stroke and minimal to moderate hand dysfunction improved performance speeds of functional tasks from just a single NMES session applied to the wrist extensors and flexors.30 NMES alone or paired with exercise improves volitional range of motion, strength, and reaction times.21,22,38,39 Potentially, applying NMES to the wrist and hand as an aid in relearning how to grasp and release objects may be beneficial to those with severe hand dysfunction, who are unable to initiate voluntary wrist/hand motion.
The first purpose of this investigation was to determine if individuals with chronic stroke and severe hand dysfunction (ie, little or no active movement at the wrist and fingers) would benefit from NMES treatments. Based upon previous evidence, our primary hypothesis was that NMES would significantly improve motor performance speed in this group. The second purpose of this research was to determine if motor performance improvements observed from somatosensory stimulation were further enhanced when utilizing NMES during task practice. Therefore, apriori, we designed our experiment to include 2 different NMES treatments for the wrist and hand musculature: (1) NMES-activated wrist flexion and extension, and (2) NMES-activated grasp and release (ie, ‘task practice’). Our second hypothesis was that motor performance improvements for individuals with chronic stroke would be greater following NMES-activated grasp and release.
Eight subjects (3 Fe, 5 M; 58.3 ± 6.9 y/o) with chronic ischemic stroke of the middle cerebral arterial distribution participated in the study (Table 1). All subjects lived at home with a spouse/caregiver and freely ambulated throughout the community. To control for spontaneous recovery from stroke, subjects had experienced their stroke injuries at least 3 years (or greater) prior to entering the study (See Table 1). All subjects had severe hand dysfunction and reported the inability to functionally use their hand to perform more than 30% of their daily activities. In order to participate in the study, subjects ≥ 18 years old demonstrated at least: (1) 10° of passive wrist extension and (2) 90% of passive extension of the fingers and thumb with the wrist in a neutral position, (3) voluntary shoulder flexion to at least 30°, (4) voluntary elbow extension of ∼10° when the initial position of the elbow was 90° flexed, and (5) Mini-Mental Status Exam of < 24, indicating intact cognition. Subjects did not participate in other rehabilitation therapies while enrolled in this study. Subjects were excluded if they had: (1) cardiac pacemakers, (2) uncontrolled cardiac arrhythmias, (3) seizures within the past 12 months, or (4) other central/peripheral neurological diseases other than stroke. The Human Subjects Committee for the Kansas University Medical Center approved the study protocol and tests. All subjects signed the informed consent.
A portable electrical stimulator (EMS+2, Rehabilicare, New Brighton, Minn) was used to activate the forearm extensor and flexor muscle groups at the wrist of the affected UE. The gel electrodes (2″ diameter, Rehabilicare, New Brighton, Minn) were attached at the motoneuronal innervation site (ie, ‘motor point’) of the extensor and flexor digitorium communis. A rectangular symmetrical biphasic waveform was applied to activate the muscle groups (300μsec, 45 Hz). Specific contraction times and intensities varied according to the NMES intervention and are described more fully below.
Prior to each intervention, subjects repeated each of the conventional clinical tests over 2 separate testing days in order to stabilize motor performance. Subjects then received both the NMESpassive and NMESactive interventions to the affected wrist and hand. The order of NMES interventions were counterbalanced across subjects so that 3 subjects first received NMESpassive and 4 subjects initially received NMESactive. interventions. For each intervention, NMESpassive and NMESactive, subjects received a total of 10 NMES treatments (30 minute sessions, 5x/wk × 2 wks). After at least 2 weeks following the completion of the first intervention, subjects then entered the second intervention. Despite this 2-week ‘washout period’, apriori, we anticipated that NMES potentially could still affect motor performance. Therefore, baseline measurements were repeated prior to beginning the second intervention for each subject. Clinical tests were performed in a randomized fashion for individual subjects across timepoints. Tests related to performance speed were performed bilaterally at all timepoints.
Upper extremity motor performance speed and function were tested twice at baseline (‘Pre’), then re-tested immediately following intervention (‘Post’) and 10 days post-NMES treatment (‘Retention’) using conventional clinical tests: (1) UE Fugl-Meyer test of Sensorimotor Impairment (FM)40 (66 points possible; high scores indicate greater function), (2) Modified Ashworth Spasticity Scale (MASS) (16 points possible; high scores indicate greater dysfunction), (3) Box to Block (BB)41 which measures the blocks transported within a 1-minute time period, and (4) Jebsen's Hand Function Test (JHFT),42 which is a performance speed test, including 7 tasks such as writing, bean-spooning, card turning, picking up objects (paper clips, heavy cans, lightweight cans), and stacking checkers.
NMESpassive: Subjects rested quietly in a chair during the treatment. The impaired forearm was placed in a mid-position (between pronation and supination) on a table for each treatment. At each session, NMES was sequentially applied to the wrist flexors and extensors in such a way to produce one wrist flexion and extension contraction (flex/ext) per minute (300μsec pulse width @ 40 Hz; 2s ramp up/down with a 6s hold) with ∼20 sec rest between contractions for a total of 30 minutes. Stimulation intensity was adjusted according to subject tolerance at the beginning of each session and was readjusted (up/down) if necessary. Subjects were instructed to not assist the stimulator, but rather ‘passively’ allow the stimulator to perform wrist flexion and extension (Figure 1A). The treatments during the intervention were performed daily × 10 days.
NMESactive: The goal of this intervention was to use NMES to activate specific muscle groups to assist the subject in grasping a 4″ diameter ball and then releasing it into a receptacle (Figure 1B). Subjects sat in a chair during the treatment. Two separate stimulators were used with manual button switches in order to appropriately activate either the flexor or the extensor muscle groups throughout the task. Upon a verbal cue, subjects independently activated shoulder flexion, while the stimulators assisted with wrist and hand movements to reach and grasp the ball. For example, when reaching for the ball, the extensors were activated in order to assist in opening from a fisted posture. Subsequently, the flexors were activated to close the fingers around the ball, followed by extensor activation to release the ball to the receptacle. Therefore, the duration of stimuli was manually controlled based upon the subject's individual speed and accuracy. In total, subjects were required to perform 30 grasp/releases within 30 minutes. The interval between repetitions was 30 seconds. Stimulation intensity was adjusted according to subject tolerance. The treatments during the intervention were performed daily × 10 days.
At each timepoint, measurements were manually recorded for each subject. Motor performance tests were performed on all subjects and data collection personnel were blinded from the group assignment and therapy intervention. The two baseline measures (‘Baseline’) of motor performance measurements were averaged for each subject (2 weeks prior to and immediately before NMES) for statistical analyses. Motor performances measures were also obtained immediately following (‘Post’) and 2 weeks after (‘Retention’) NMES interventions. Group mean scores were determined at each timepoint. Mixed models were used to test the study hypotheses of the effectiveness of NMES and of the benefit of active versus passive NMES. Difference scores (‘Post’ – ‘Baseline’) were used as the response variables, and treatment, treatment order, and the treatment-by-treatment order interaction were included as explanatory variables. Treatment order effects were included in these models to test for a carryover effect from the intervention first received into the second treatment period. Statistics for these tests were compared against F distributions to calculate p-values. Mixed models were estimated separately for each behavioral test using PROC MIXED (SAS ver. 9.1, SAS Institute, Inc., Cary, NC, 2002–2003). A covariance parameter was estimated to adjust for the correlation between repeated measures within subjects due to the crossover design. A compound symmetry covariance structure was used. Linear contrasts were used to estimate and test the effects of NMES (active and passive combined; primary hypothesis) and to estimate and compare the effects of active versus passive NMES (secondary hypothesis). Test statistics derived from these linear contrasts were compared to the t-distribution. To assess retention, similar analyses were performed when NMES was demonstrated to be beneficial (‘Post’ minus ‘Baseline’) by using difference scores (‘Retention’ minus ‘Baseline’). Statistical significance was set at α=0.05. Because the primary purpose of this pilot study is to guide the design of a larger, future intervention trial, no adjustments to statistical tests were made to account for the multiple testing due to having 4 behavioral response variables.
Upon enrollment, all subjects had less than 10° of volitional flexion/extension at the wrist or fingers joints. Each subject tolerated the NMES interventions and completed the protocol, with the exception of one subject who did not complete the NMESactive intervention (S204). For this subject, we were unable to electrically activate the wrist extensors comfortably in order to overcome the flexor spasticity/tone at the hand. Subsequently, the subject was unable to perform the task of grasping or releasing the ball during the active intervention. However, the mixed model analysis using PROC MIXED allowed us to accommodate this imbalance and include data observed from this subject under the NMESpassive intervention.
NMES Effects on Sensorimotor Impairment
Repeated measures analyses revealed significant main effects for improvement in the upper extremity FM scores (66-point scale) (μ = 5.8; p<0.002) across both types of interventions. Linear contrasts within each intervention revealed significant improvement from baseline scores to post-intervention for the NMES (μ = 6.2, p<0.014) and NMESpassive. (μ = 5.4, p<0.018). Treatment effects on FM scores were retained at 10 days following intervenentions (μ = 4.0, p<0.013 for NMES; μ = 4.3, p<0.024 for NMESactive; μ = 3.6, p=0.036 NMESpassive) (Figure 2A). Between intervention comparisons were not significant.
Significant effects were also observed for the improvement in the MASS (μ = −2.1, p<0.03). Although no significant difference was detected between interventions, only NMESpassive demonstrated a significant improvement from baseline (μ = −2.6, p<0.034). No carryover effects were observed for this variable. Intervention effects on MASS were not significant at retention (Figure 2B). Between intervention comparisons were not significant.
Skilled Motor Performance and Dexterity Function
Overall, subjects performed tasks faster following the NMESactive intervention. Significant effects were observed for JHFT (μ = −29.9, p<0.033). No significant difference was detected between NMESactive versus NMESpassive, but NMESactive intervention showed a significant improvement from baseline (μ = −58.9, p<0.033). No carryover effects were observed for this variable. Intervention effects on JHFT were not retained. Although between intervention comparisons were not significantly different, performance speeds for the group increased (−50.94 ± 19.41 sec) for NMESactive immediately following intervention, compared to an increase of only (−1.2 ± 18.41 sec) for the NMESpassive interventions (Figure 3A, Figure 4). These increased performance speeds in the NMESactive intervention were observed within subjects and for the group as a whole (Figure 4C).
Subjects transported blocks at a faster rate following both NMES interventions (μ = 2.7, p < 0.025) (Figure 3B). As with the JHFT measure, there was no significant difference for BB between interventions, but NMESactive intervention showed a significant improvement from baseline (μ = 3.3, p < 0.045). No carryover effects were observed for this variable, nor were intervention effects retained 10-days following treatment.
Our primary goal was to determine the effectiveness of NMES for the chronic stroke survivor who possessed severe hand dysfunction. Each subject received a short intervention (10 sessions) of NMES that was systematically applied using 2 different methods. In one intervention, we applied NMES in a novel fashion, using multiple stimulators applied to the forearm flexors and extensors to assist subjects while they grasped and released a tennis ball. In the other intervention, the NMES was applied using a traditional method of passively stimulating wrist flexion and extension.
We used clinical tests that encompassed a broad spectrum of motor control aspects including function, performance time, and movement ability. The FM and MASS tests assessed fundamental improvements in sensorimotor impairment. Because finger/wrist extension and forearm supination prove particularly difficult to regain following stroke, we also focused on the JHFT and BB as an indicator of subjects' ability to achieve more complex movements following intervention. The small sample size of this pilot study has obvious limitations in generalizing to a broader stroke population. However, our group as a whole demonstrated that a short duration of NMES intervention applied to the wrist musculature can substantially improve severe hand dysfunction long after the initial stroke occurs. And, generally, it appears as if using NMES while performing a meaningful task such as grasp and release is of greater functional benefit than merely activating passive wrist flexion and extension. Our results indicate that NMESactive specifically improved FM, JHFT, and BB scores, while NMES passive specifically improved MASS.
The NMES-driven effects for either intervention were small in magnitude, which caused us to question the clinical meaningfulness of the change. To understand the between day change in our test scores, we examined the baseline measures for each subject that were collected on 2 separate days prior to each intervention. All scores showed small between-day differences for the group (FM = 0.62 points; MASS = 0.71 points; BB = 0.3 blocks/min; and JHFT = 3.6 sec.), suggesting that the changes due to intervention surpassed random variability or experimental noise. Overall, given that it is difficult to improve severe hand dysfunction in the chronic phase of stroke,1,2 we find these effects from a short bout of NMES intervention optimistic for this population.
At the initial baseline, the FM scores for individual subjects ranged from 4–32 (66 points possible), and subsequently the mean group improvement was <16%, regardless of the type of NMES intervention (Figures 2 and 3). Similarly, 28% to 31% improvement in the mean MASS score for the group was observed immediately following each intervention. Our group could not actively coordinate finger/wrist extension and flexion, yet their sensorimotor improvements reflect other studies of stroke survivors with less severe deficits, ie, those who presumably already possessed the ability to move the wrist and hand prior to receiving NMES.30,32 In these previous studies, subjects with the lowest FM scores tended to show the greatest magnitude of motor improvement. Our results suggest that this same trend is generally present, even though the initial wrist and hand scores from our group for FM (Table 1) and MASS (Figure 4) scores are much lower than those of previous studies.
Our results suggest that NMES may prove useful well beyond the first year of stroke injury, regardless of the level of disability. Early studies2–4,39 indicate that the ability to recover function after stroke is related to initial severity and the time since the onset of injury. However, at least some motor performance improvement was observed in all of our subjects, regardless of the location of the stroke or the size of the lesion. Indeed, while such factors might have impacted our results, improved UE voluntary motion can be expected within 2 weeks of daily treatments using NMES at the wrist after stroke.
Skilled manual dexterity improvements were observed in our group from using NMES while grasping and releasing a tennis ball (Figure 3). While these general trends from task-related electrical stimulation are optimistic, other factors suggest that further in depth study are warranted for those with severe hand dysfunction. Specifically, while improvement occurred, full hand function was not restored after just 10 treatments. Perhaps the magnitude of change relies more on treatment intensity or duration, since skilled manual dexterity requires both somatosensory integrations and descending control proceeding in parallel.43 To understand the effects of NMES in isolation of other treatments, we did not include a home exercise program within our experimental design. It is possible that functional ability may improve with NMESpassive at home while simultaneously receiving NMESactive intervention in a clinical setting; or with extensive task practice within the home exercise program outside of the NMES treatment.
Our experimental design prevented our understanding the NMES-related impact on motor learning post-stroke. Overall, performance speeds (JHFT) for skilled dexterity tasks improved to a greater degree following the NMESactive (Figures 3 and 4) compared to the NMESactive intervention. These results suggest that specific changes in motor performance can be driven with the activity that is performed during stimulation. We find this result compelling. Theoretically, NMES during meaningful task practice may have improved neural transmission efficiency across the entire upper extremity, despite that the electrodes were applied only to the forearm musculature. NMES-evoked muscle force is produced by initiating movement at the periphery, while simultaneously producing ascending somatosensory signals.44 Alternatively, the final motor command for skilled grasping on the uninvolved limb uses descending control, that originates directly from the primary motor cortex and proceeds along the corticospinal tract to the hand/wrist complex to produce the accurate muscle force required for the task.45 How the central nervous system resolves this apparent conflict of muscle activation proceeding differently at the involved limb compared to the uninvolved limb when performing grasp and release is unclear. These, and other related questions are of significant interest for rehabilitation.
To our surprise, despite that individual subjects had relatively low function in the hand subtests of the FM test (Table 1), they were able to perform fairly well on the JHFT tests at baseline. Moderate functional ability was observed in our group for the tasks that accommodated movements performed within their available range of motion. For example, S200 and S201 required less than 4 seconds/block to transport the block across the divider to complete the BB test at baseline by using whole-hand grasping to accomplish the movement. This observation is in accordance with previous theories suggesting chronic stroke survivors exhibit ‘functional disuse syndrome’ which can benefit from ‘forced use.’46
In contrast to previous reports of individuals who had recent strokes or possessed greater UE ability,21,22,32,34,35,37 our group demonstrated a generalized decline in performance within 2 weeks after completing either intervention. The reasons for this decline are unclear and cannot be answered with our small group of subjects, but these results suggest that increasing therapy duration is useful for retention, regardless of the type of NMES application. Theoretically, while improvements are possible after all types of strokes, retaining therapeutic benefit from NMES may indeed be related to severity, the time interval from the initial injury until voluntary muscle activation occurs, or other factors. Thus, those with severe hand dysfunction may require longer durations of NMES in order to continue improving functional abilities with task practice once the intervention is discontinued.
Our NMESactive task required subjects to grasp, transport, and subsequently aim the ball so that it was released into the receptacle. Subjects improved their ability to reach, grasp, and release large objects following this task-related NMES treatment compared to the NMESactive intervention. However, JHFT tasks which required the greatest complexity of precision grip, such as grasping/releasing paperclips, demonstrated little improvement beyond the baseline scores, regardless of the intervention. This finding underscores the difficulty of fully restoring the neuromuscular coordination necessary for all aspects related to skilled dexterity.47,48 Somatosensory input is required for skilled movements in order for the central controller to monitor the spatial position of the body relative to the environment, task accuracy, and other important factors.49,50 Recent evidence30,51,52 of increased corticomotoneuronal excitability51 and an expanded body-related representations within the primary somatosensory cortex30 have been reported immediately following peripheral nerve stimulation in humans. Relevant context of the somatosensory signals processed by the central controller is also necessary for fast and accurate movements. The mechanism of how complex somatosensory processing proceeds after stroke injury is not fully understood,53–55 but rapid, well-coordinated UE movements will likely require persistent practice50,56–58 that mandate extending treatments well into the chronic phase of stroke.
In conclusion, we find the data from this pilot study compelling for several reasons. Short bouts of NMES can produce significant changes in wrist and hand function for the chronic stroke survivor. We observed improvement for all subjects, despite that they may have had severe hand disability upon entering the study or that many years had passed since the occurrence of stroke. Also, using NMES to assist during task practice appears more beneficial than activating the wrist flexors and extensors in a passive mode. Finally, of interest, is gaining knowledge of the effects produced within the nervous system after using NMES. Overall, additional investigations of UE dysfunction in chronic stroke are merited in order to more fully understand the potential for functional recovery.
We would like to thank Dr. Randolph Nudo, Dr. Patricia Kluding, and Brenda Wessel, MS, PT for their helpful comments on this project. The NMES equipment for this study was provided through the generosity of Rehabilicare, Inc. Support for this project was provided through the Landon Center on Aging Endowment Grant (G558075) and NIH K01 HD047148-02.
1 Broeks JG, Lankhorst GJ, Rumping K, Prevo AJ. The long-term outcome of arm function after stroke
: results of a follow-up study. Disabil Rehabil
2 Duncan PW, Goldstein LB, Horner RD, Landsman PB, Samsa GP, Matchar DB. Similar motor recovery of upper and lower extremities after stroke
3 Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS. Recovery of upper extremity
function in stroke
patients: the Copenhagen Stroke
Study. Arch Phys Med Rehabil
4 Nakayama H, Jorgensen HS, H.O. R, Olsen TS. Compensation in recovery of upper extremity
function after stroke
: The Copenhagen Stroke
Study. Arch Phys Med Rehabil
5 Classen J, Liepert J, Wise S, Hallett M, Cohen L. Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol
6 Hallett M. Plasticity of the human motor cortex and recovery from stroke
. Brain Res Rev
7 Cotman CW, Berchtold NC. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci
8 Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Ann Rev Neurosci
9 Jones TA, Chu CJ, Grande LA, Gregory AD. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J Neurosci
Sanes J, Donoghue J. Plasticity and primary motor cortex. Annu Rev Neurosci
11 Singh K, Scott SH. A motor learning strategy reflects neural circuitry for limb control. Nat Neurosci
12 Xerri C, Merzenich MM, Peterson BE, Jenkins W. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke
in adult monkeys. J Neurophysiol
13 Nudo R, Wise B, SiFuentes F, Milliken G. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science
14 Heddings AA, Friel KM, Plautz EJ, Barbay S, Nudo R. Factors contributing to motor impairment and recovery after stroke
. Neurorehabil Neural Repair
15 Nudo R, Barbay S, Kleim J. Role of neuroplasticity in functional recovery after stroke
. In: Levin HS, Grafman J, eds. Cerebral Reorganization of Function after Brain Damage
. Vol 1. USA: Oxford University Press; 2000:168–197.
16 Kleim J, Jones T, Schallert T. Motor enrichment and the induction of plasticity before or after brain injury. Neurochem Research
17 Kolb B. Overview of cortical plasticity and recovery from brain injury. Phys Med Rehabil Clin N Am
. 2003;14:S7-25, viii.
18 Kolb B, Brown R, Witt-Lajeunesse A, Gibb R. Neural compensations after lesion of the cerebral cortex. Neural Plast
19 Alberts JL, Butler AJ, Wolf SL. The effects of constraint-induced therapy on precision grip: a preliminary study. Neurorehabil Neural Repair
. 2004; 18:250–258.
20 Wolf SL, Thompson PA, Morris DM, et al. The EXCITE trial: attributes of the Wolf Motor Function Test in patients with subacute stroke
. Neurorehabil Neural Repair
21 Cauraugh J, Light K, Sangbum K, Thigpen M, Behrman A. Chronic motor dysfunction after stroke
: Recovering wrist and finger extension by electromyography-triggered neuromuscular stimulation. Stroke
22 Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey LL, Lojovich JM, Carey JR. Electrical stimulation
driving functional improvements and cortical changes in subjects with stroke
. Exp Brain Res
. 2004; 154:450–460.
23 Kleim JA, Barbay S, Cooper NR, et al. Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem
24 Friel KM, Barbay S, Frost SB, et al. Dissociation of sensorimotor deficits after rostral versus caudal lesions in the primary motor cortex hand representation. J Neurophysiol
25 Nudo RJ. Functional and structural plasticity in motor cortex: implications for stroke
recovery. Phys Med Rehabil Clin N Am
26 Patel AT, Duncan PW, Lai SM, Studenski S. The relation between impairments and functional outcomes poststroke. Arch Phys Med Rehabil
27 Studenski SA, Wallace D, Duncan PW, Rymer M, Lai SM. Predicting stroke
recovery: three- and six-month rates of patient-centered functional outcomes based on the orpington prognostic scale. J Am Geriatr Soc
28 Trimble MH, Enoka RM. Mechanisms underlying the training effects associated with neuromuscular electrical stimulation
. Phys Ther
. 1991;71:273–280; discussion 280–272.
29 Kimura J. Electrodiagnosis in Diseases of Nerve and Muscle
. 3rd ed. New York, NY: Oxford University Press; 2001:91–117.
30 Wu CW, Seo HJ, Cohen LG. Influence of electric somatosensory stimulation on paretic-hand function in chronic stroke
. Arch Phys Med Rehabil
31 Wu CW, van Gelderen P, Hanakawa T, Yaseen Z, Cohen LG. Enduring representational plasticity after somatosensory stimulation. Neuroimage
32 Conforto AB, Kaelin-Lang A, Cohen LG. Increase in hand muscle strength of stroke
patients after somatosensory stimulation. Ann Neurol
33 de Kroon JR, van der Lee JH, MJ IJ, Lankhorst GJ. Therapeutic electrical stimulation
to improve motor control and functional abilities of the upper extremity
: a systematic review. Clin Rehabil
34 Chae J, Yu D. A critical review of neuromuscular electrical stimulation
for treatment of motor dysfunction in hemiplegia. Assist Technol
35 de Kroon JR, MJ IJ, Lankhorst GJ, Zilvold G. Electrical stimulation
of the upper limb in stroke
: stimulation of the extensors of the hand vs. alternate stimulation of flexors and extensors. Am J Phys Med Rehabil
36 Hainaut K, Duchateau J. Neuromuscular electrical stimulation
and voluntary exercise. Sports Med
37 Powell J, Pandyan AD, Granat M, Cameron M, Stott DJ. Electrical stimulation
of wrist extensors in poststroke hemiplegia. Stroke
38 Bolton DA, Cauraugh JH, Hausenblas HA. Electromyogram-triggered neuromuscular stimulation and stroke
motor recovery of arm/hand functions: a meta-analysis. J Neurol Sci
. 30 2004;223:121–127.
39 Chae J, Bethoux F, Bohine T, Dobos L, Davis T, Friedl A. Neuromuscular stimulation for upper extremity
motor and functional recovery in acute hemiplegia. Stroke
40 Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke
hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med
41 Mathiowetz V, Volland G, Kashman N, Weber K. Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther
42 Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA. An objective and standardized test of hand function. Arch Phys Med Rehabil
43 Johansson R. Sensory input and control of grip. In: Bock G, Good J, eds. Sensory guidance of movement
. Vol 218. West Sussex: John Wiley & Sons Ltd.; 1998:45–63.
44 Kanda K, Burke RE, Walmsley B. Differential control of fast and slow twitch motor units in the decerebrate cat. Exp Brain Res
45 Porter R. The corticomotoneuronal component of the pyramidal tract: Corticomotoneuronal connections and functions in primates. Brain Res
46 Taub E, Uswatte G, Pidikiti R. Constraint-induced movement therapy: a new family of techniques with broad application to physical rehabilitation–a clinical review. J Rehabil Res Dev
47 Johansson RS, Cole KJ. Grasp stability during manipulative actions. Can J Physiol Pharmacol
48 Johansson RS, Westling G. Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp Brain Res
49 Ghez C, Favilla M, Ghilardi MF, Gordon J, Bermejo R, Pullman S. Discrete and continuous planning of hand movements and isometric force trajectories. Exp Brain Res
50 Ghez C, Hening W, Gordon J. Organization of voluntary movement. Curr Opin Neurobio
51 Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG. Modulation of human corticomotor excitability by somatosensory input. J Physiol
52 Kaelin-Lang A, Sawaki L, Cohen LG. Role of voluntary drive in encoding an elementary motor memory. J Neurophysiol
53 Quaney B, Perera S, Maletsky R, Luchies CW, Nudo RJ. Impaired grip force modulation in the ipsilesional hand after unilateral middle cerebral artery stroke
. Neurorehabil Neural Repair
54 Hermsdorfer J, Hagl E, Nowak DA. Deficits of anticipatory grip force control after damage to peripheral and central sensorimotor systems. Human Movement Science
55 Nowak DA, Hermsdorfer J. Sensorimotor memory and grip force control: does grip force anticipate a self-produced weight change when drinking with a straw from a cup? Eur J Neurosci
56 Witney AG, Vetter P, Wolpert DM. The influence of previous experience on predictive motor control. Neuroreport
57 Wolpert D, Goodbody S, Husain M. Maintaining internal representations: The roles of the human superior parietal lobe. Nature Neurosci
58 Wolpert DM, Ghahramani Z, Jordon MI. An internal model for sensorimotor integration. Science
Keywords:© 2006 Neurology Section, APTA
upper extremity; stroke; electrical stimulation