Skip Navigation LinksHome > December 2010 - Volume 34 - Issue 4 > Functional and Corticomotor Changes in Individuals With Tetr...
Journal of Neurologic Physical Therapy:
doi: 10.1097/NPT.0b013e3181fbe692
Articles

Functional and Corticomotor Changes in Individuals With Tetraplegia Following Unimanual or Bimanual Massed Practice Training With Somatosensory Stimulation: A Pilot Study

Hoffman, Larisa R. PT, PhD; Field-Fote, Edelle C. PT, PhD

Free Access
Article Outline
Collapse Box

Author Information

School of Physical Therapy, Regis University, Denver, Colorado (L.R.H.); The Miami Project to Cure Paralysis, University of Miami Miller School of Medicine, Miami, Florida (E.C.F.F.); and Department of Physical Therapy, University of Miami Miller School of Medicine, Coral Gables, Florida (E.C.F.F.).

Correspondence: Larisa R. Hoffman, PT, PhD, Regis University, School of Physical Therapy, Denver, CO 80221 (lhoffman@regis.edu).

Funded by the Miami Project to Cure Paralysis and by a Foundation for Physical Therapy Promotion of Doctoral Studies Award to L.R.H.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.jnpt.org).

Collapse Box

Abstract

Background and Purpose: In individuals with cervical spinal cord injury (SCI), damage to spinal pathways results in deficits of hand function; maladaptive cortical changes further impair function. Unimanual massed practice (MP) training with somatosensory stimulation (SS) has been shown to improve hand function and increase corticomotor excitability after SCI. However, bimanual training may be more beneficial as these individuals have bilateral impairment. We compared clinical and corticomotor changes associated with unimanual versus bimanual MP training, each combined with SS.

Methods: Participants were 13 individuals with chronic tetraplegia who had at least minimal voluntary control of the thenar muscles of 1 hand. The participants were randomly assigned to unimanual MP + SS or bimanual MP + SS. Clinical outcome measures included tests of unimanual (Jebsen Taylor Hand Function Test; JTT) and bimanual hand function (Chedoke Arm and Hand Activity Inventory; CAHAI), sensory function (monofilament test), and pinch grip strength. Neurophysiological outcome measures were corticomotor map area, center of gravity (COG), of the corticomotor map and corticomotor threshold as assessed by transcranial magnetic stimulation.

Results: There were no significant differences in outcomes between the unimanual MP + SS versus bimanual MP + SS groups, both groups showed significant improvements in the JTT, CAHAI, and monofilament test. However, trends suggest that the unimanual MP + SS group had greater improvement in the JTT whereas the bimanual MP + SS group had greater improvement on the CAHAI. Functional changes were accompanied by a strong trend toward increased corticomotor map area.

Discussion and Conclusion: When combined with SS, both unimanual and bimanual MP training improve hand function and sensation in individuals with tetraplegia. Changes in hand function seem to be associated with increased corticomotor map area.

Back to Top | Article Outline

BACKGROUND AND PURPOSE

There are approximately 12 000 spinal cord injuries (SCIs) each year in the United States, with the largest subgroup comprising individuals having incomplete cervical injuries.1 According to 2 different surveys of individuals with tetraplegia due to SCI, recovery of hand function is the single factor that these individuals report would most improve their quality of life.2,3 Therefore, given the importance of hand function, and the difference that even small improvements in hand function can make to activities of daily living, identifying effective approaches for restoration of hand function in individuals with tetraplegia is important.

Deficits in hand function in individuals with cervical SCI are attributable to a variety of factors. Beyond the physical damage caused by the trauma, secondary central nervous system (CNS) reorganization may exacerbate the functional loss.4,5 Maladaptive reorganization includes decreased corticomotor excitability,6,7 decreased size of corticomotor representation,6 and displacement of the corticomotor representation to a more posterior location.79 Many of the changes in corticomotor reorganization that occur after SCI are akin to those that occur following stroke.10 Therefore, interventions that are effective in improving hand function in individuals poststroke may be effective for individuals with SCI. Two interventions shown to be effective in individuals poststroke are massed practice training (MP)11,12 and somatosensory stimulation (SS).13,14

Back to Top | Article Outline
Massed Practice Training

Massed practice training entails repetitive task practice to improve motor performance. Beekhuizen and Field-Fote15,16 showed that individuals with incomplete, cervical SCI who participated in a combination intervention incorporating practice of unimanual MP of upper extremity tasks and SS demonstrate greater improvements in the performance of activities than individuals assigned to either MP or SS alone. In addition, significantly greater corticomotor excitability was found following the combined intervention. Furthermore, Hoffman and Field-Fote9 found evidence suggesting reorganization of the corticomotor map in an individual with SCI who underwent this training.

Given that unimanual training can induce practice-dependent plasticity in individuals with SCI,15,16 it is possible that bimanual training may induce even greater adaptive plasticity. Neurophysiological evidence suggests that bilateral movements increase bihemispheric cortical excitability1719 and may thereby facilitate movement in individuals with bilateral impairments of hand function. In individuals poststroke, during unimanual hand activities of the less affected side, the nonlesioned cortex sends inhibitory signals to the lesioned cortex.20 Conversely, in bimanual activities, muscle contractions on the less affected side create a facilitatory effect in the cortically evoked response in the affected hand.17,18 Furthermore, there are more corticomotor areas active during bimanual tasks than during unimanual tasks, even when the tasks are similar,21 which maybe related to the coordination of both hands and control of a greater number of degrees of freedom.17,22,23 From a clinical perspective, bimanual training in individuals with bilateral upper extremity deficits provides the opportunity to address deficits in both limbs simultaneously.

Despite the apparent neurophysiologic and functional advantages of bimanual training over unimanual training, it is possible that unimanual training is superior, as it provides a greater intensity of practice for the hand that is being trained. The participant focuses the entire training session on 1 extremity rather than dividing the training session between the 2 limbs. In addition, during unimanual MP sessions, the participant is unable to use the contralateral limb as an assistive hand, which may make the task more challenging. Activities may also be more challenging when a participant is required to perform a bimanual task with 1 hand alone.

Back to Top | Article Outline
Sensory Stimulation

The sensory cortex is a potent source of excitation for the motor cortex.24 Therefore, it seems plausible that increasing sensory input would increase the excitability of the sensory cortex and thereby increase excitability of M1 resulting in increased voluntary drive. Sensory stimulation is a form of electrical stimulation with a long pulse duration. Longer pulse duration is thought to preferentially activate the large type I sensory nerve fibers.25 Beekhuizen and Field-Fote15,16 found that SS alone can improve unimanual hand function and pinch-grip strength in individuals with SCI.

The purpose of this study was to compare changes in hand function associated with participation in unimanual or bimanual MP training, each combined with SS. The secondary aim of the study was to evaluate the changes in corticomotor physiology related to a task-oriented training intervention. We hypothesized that following the intervention, those in the bimanual MP group would demonstrate greater changes on the activity-related outcome measures than in the unimanual MP group.

Back to Top | Article Outline

METHODS

Design

We used a pre-post intervention design (Figure 1). Participants were randomly assigned to 1 of 2 groups: unimanual or bimanual each combined with SS. The randomization was performed by lottery (ie, drawing from a envelope a slip of paper indicating one of the two intervention assignments.)

Figure 1
Figure 1
Image Tools
Back to Top | Article Outline
Participants

Participants met the following inclusion criteria: cervical SCI rostral to neurological level C8, at least 1 year postinjury, and an ability to produce a visible twitch in the thenar muscles of at least 1 hand. Participants were excluded if they had a history of head injury, stroke, or metal implants in the cranial cavity. All participants gave written and verbal informed consent according to the protocol of a study approved by the Human Studies Research Office at the University of Miami Miller School of Medicine.

Back to Top | Article Outline
Outcome Measures

To evaluate across the different domains of the International Classification of Functioning, Disability, and Health, several different outcome measures were selected, but the primary outcome measure was the Jebsen Taylor Hand Function Test (JTT). Participant's limitations in activities were assessed using the JTT26 and the Chedoke Arm and Hand Activity Inventory (CAHAI).27 The clinical tests used to evaluate impairments were the Semmes-Weinstein Monofilament Test (SWMT)28 and pinch-grip strength dynamometry. The JTT, the CAHAI, the SWMT, and dynamometry have been shown to be reliable in individuals with movement disorders and sensitive to changes associated with intervention.26,27,29 For the clinical tests, participants were positioned in their wheelchair with the shoulder in the neutral position, elbow positioned to 90° of flexion, and the forearm resting on a table.

The JTT assesses change in unimanual hand function associated with therapeutic interventions, and individuals with SCI were included in the population for which this test has been shown to be reliable and valid.26 The CAHAI27 was designed to measure the performance of bimanual hand tasks, as they relate to functional ability in individuals poststroke, but has not previously been validated for use in individuals with SCI. As part of the study we sought to validate the use of the CAHAI for use in individuals with SCI by establishing concurrent validity with the JTT. The SWMT28 was used to measure the degree of sensitivity to light touch in the median nerve sensory distribution. A lower score indicates poorer sensory perception, whereas a higher score indicates better sensory perception. Pinch-grip strength was measured with a hand-held dynamometer (Microfet4; Hoggan Health Industries, West Jordan, Utah). The maximum force produced on the 3 trials was recorded, and the mean force was calculated.

As neurophysiologic outcome measures, training-related changes in corticomotor areas were assessed via transcranial magnetic stimulation (TMS)-evoked potentials elicited at rest. Monophasic TMS was delivered by a Magstim 200 stimulator (The Magstim Co Ltd, Wales, UK), with maximum magnetic field strength = 2 Tesla, using a figure-of-eight coil. Measures included: corticomotor map area, location of the center of gravity (COG) of the corticomotor map,30 and (cortico)motor threshold (MT) associated with the thenar muscles, all of which have been shown to be reliable outcome measures.31 Changes in map area and MT are sensitive to change following either SS in isolation32 or a combination intervention of MP and SS.15,16

The thenar muscles were chosen for several reasons: thumb control is critical to many manual task, it was hypothesized that these muscles might illustrate the greatest change related to the stimulation,15,16 and these muscles have been previously studied in other published work of TMS-evoked potentials in individuals with SCI.6,7 The weaker limb was tested unless the individual had no voluntary control of the thenar muscles in the weaker hand, in which case the stronger limb was tested. Approximately half (7/13) of the participants were tested using their stronger limb (Table 1).

Table 1
Table 1
Image Tools

During the TMS testing, the participants sat reclined on a padded treatment table, with the head and arm supported. Participants wore a tight-fitting, silicone cap (The Bobby Co, San Diego, California), with an imprinted grid demarking 1-cm squares. To ensure reliable placement of the cap, the location of the nasion, inion, ears, and the vertex (Cz; the point at which the interaural line and the line connecting nasion and inion intersect) was marked on the cap. The opponens pollicis muscle was palpated, and the overlying skin was abraded with an alcohol swab. Two surface Ag/AgCl electrodes (3.2 × 2.2 cm2) were placed 2 cm apart over the muscle and tendon, with a ground electrode over the olecranon. To ensure the muscle was at rest, 200- and 300-ms epochs were recorded, respectively, before and after the stimulus was applied. The electromyography signals were amplified (×1000) and band pass filtered (10-2 kHz) (Grass P511 AC; Grass-Telefactor, West Warwick, Rhode Island). The signals were digitized (CED model 1401; Cambridge Electronic Design Ltd, Cambridge, UK) at a sampling rate of 2 kHz. Data were stored using a digital acquisition program (Signal 2.15; Cambridge Electronic Design Ltd) and analyzed off-line.

The TMS coil was placed directly on the cap over the hemisphere contralateral to the test hand, with the handle directed 45° posteriorly and laterally.33 The upper extremity region was estimated to be approximately 5 cm lateral on the interaural line. The stimulator was initially set to approximately 70% to 90% maximal stimulator output (MSO), and the coil was moved in 1-cm increments until the “hot spot” (site at which the amplitude of the MEP is the greatest and latency is shortest) was identified.34 To determine resting MT at the hotspot, stimulus intensity was reduced to a level that did not evoke an MEP and then increased in increments of 5%. The MT was defined as minimum stimulus intensity at which 5 of 10 responses achieved amplitude of at least 50 μV.34

To create the map, the stimulator intensity was increased to 120% of MT.30 Each site on the grid was stimulated 3 times and the responses were recorded; the coil was then moved to the contiguous site until reaching a site at which no MEP could be evoked. The map area35 was defined by the region encompassing sites from which an MEP of at least 50 μV could be evoked. The average amplitude of the 3 MEPs recorded from each site was calculated and normalized to the maximum MEP of the corticomotor map. The COG35 was determined by creating a map representing the amplitude-weighted sites of the excitable area, according to the distance from Cz (x = 0, y = 0). The formula1 for the longitudinal value of the YCOG calculation is as follows:

Equation 1
Equation 1
Image Tools

where ai is the mean amplitude at a specific scalp site whose coordinate is yi cm from Cz and mi is the mean maximum MEP. Following this convention, the latitude value of the COG is calculated1 in a similar manner:

Equation (Uncited)
Equation (Uncited)
Image Tools

Therefore, sites medial and anterior to Cz had positive values, whereas sites lateral and posterior to Cz had negative values.

Back to Top | Article Outline
Interventions

The intervention protocol consisted of either unimanual or bimanual MP in conjunction with SS, for 2 hours a day, 5 days a week, for 3 weeks. The protocol was modeled after the unimanual MP described in previously published studies.15,16 Training sessions were divided into 5 intervals, each with 5 movement categories that were practiced for 20 to 25 minutes each (see Table, Supplemental Digital Content 1, which describes sample unimanual and bimanual tasks practiced during the intervention, http://links.lww.com/JNPT/A6). Participants chose the tasks to practice to ensure the task had relevance for them.36 During the 3-week intervention period, most participants chose to practice a variety of tasks.

The 2 interventions were designed to be as similar as possible in order to ensure that the primary difference between the interventions was the practice of unimanual or bimanual tasks. In the unimanual group, participants performed the tasks with their weaker extremity (regardless of hand dominance); however, as with testing, if the participant lacked voluntary control of the thenar muscles, the opposite side was trained. When necessary, to allow tasks to be accomplished with 1 hand, the object was stabilized by glue, putty, or a clamp. For example, in the container-opening task, jars were glued onto a large board and participants practiced removing the lids. Likewise, in the nuts and bolts tasks, participants practiced removing nuts from a bolt while the bolt was stabilized in a block of wood. The bimanual tasks were as similar as possible to the unimanual tasks with slight modifications so that the tasks could be performed bimanually. Using the previous example, participants in the bimanual group opened containers by using one hand to stabilize the container and the other hand to remove the lid. Similarly, in the nuts and bolts task, one hand stabilized the bolt whereas the other hand removed the nut.

For the bimanual MP, some tasks required that both hands perform a similar movement pattern (symmetrical tasks), whereas other tasks required that each hand perform a different movement pattern (asymmetrical tasks). In tasks that were symmetrical, the participants were encouraged to perform similar movement patterns with both hands simultaneously. For example, in the piano keyboard task, the participants were instructed to press the keys by using the same digit on both hands concurrently. In asymmetrical movement tasks, one hand functioned as an assistive or stabilizing hand and the other hand performed the manipulative portions of the task, for example, stabilizing the calculator with one hand and pressing the buttons with the other hands. In these types of tasks, the weaker hand performed the manipulative portion of the task for half of the training time (while the stronger hand stabilized), and for the other half of the training time the weaker hand performed the stabilization portion of the task (while the stronger hand performed the manipulation). The alternation ensured that both the weaker hand and the stronger hand practiced both elements of the task.

The focus of the intervention was to restore movement patterns typical of individuals with no disability. Some tasks were more challenging than others, as indicated by an inability to complete the task in the manner demonstrated by the trainer. If the individual was unable to complete a task, then hand-over-hand assistance was provided over the individual's hands to ensure successful completion of the task. The assistance was gradually reduced throughout the training. Alternatively, at times the task chosen was insufficiently challenging for the participant. The task was determined to be insufficiently challenging if the participant performed the task as demonstrated by the trainer and rated the difficulty of the task as less than 3 on a 10-point scale, where 10 represented great effort to complete the task and 1 represented minimal effort to complete the task. If the task was not challenging, the demands of the task were increased by altering the setup. For example, to increase the difficulty for the writing task, the writing utensil was progressed from a felt-tip pen to a pencil and finally to a crayon. Using this progression, the subject was required to progressively produce greater force on the writing utensil to mark on the paper.

All subjects received SS concurrently with MP training; surface Ag/AgCl electrodes were placed on the volar surface of the wrist overlying the median nerve. The SS was delivered using a constant current stimulator (Digitimer model DS7A; Digitimer Ltd, Welwyn Garden City, UK). Trains of electrical stimulation (frequency: 10 Hz; on/off duty cycle: 500/500 ms; pulse duration: 1 ms) were delivered at an intensity level just below that which evoked an observable twitch. In both the unimanual and bimanual groups, only the weaker hand was stimulated. However, if a subject in the unimanual group had no voluntary control of the thenar muscles in the weaker hand, then both the training and the stimulation were applied to the opposite hand.

Back to Top | Article Outline
Statistics

Two-way repeated-measures analysis of variance was used to compare between-group differences in the pre- and postintervention (time) clinical measures. To determine the concurrent validity of the CAHAI in individuals with SCI, a Pearson correlation coefficient was used to assess its correlation with the JTT. The level of significance was accepted as α < 0.05 for all tests. For the TMS data, consistent thenar MEPs were obtained from 6 of the 13 participants (3 in each group). For this reason, overall effects of training with data pooled across groups were tested using a 2-tailed, paired t test to compare the pre- and postintervention changes. Descriptive statistics were used to characterize data obtained from each group (Table 1).

Back to Top | Article Outline

RESULTS

Of the 13 individuals who were enrolled in the study, 2 participants were unable to complete the study (1 in each group). One of these participants developed an infection (unrelated to the study) and another participant had difficulty with transportation. The groups were similar in terms of baseline demographics (American Spinal Injury Association (ASIA) Impairment Scale classification, level of injury, duration of injury, cause of injury, gender, age, and ability to activate thenar muscles) and preintervention outcome measures (Table 1).

Back to Top | Article Outline
Clinical Outcome Measures

The mean and median pre- and postintervention scores for the clinical outcome measures are summarized in Table 2. For the JTT, the primary outcome measure for this study, the scores of both groups improved significantly as indicated by a significant main effect of time (F = 10.00, P = 0.01; Table 2). Both groups completed the tasks more quickly following training, with a mean decrease in completion time of −91.67 ± 15.51 and −47.27 ± 36.65 seconds for the unimanual and bimanual groups, respectively. Despite the appearance (based on mean change) of greater improvement in the unimanual group, the between-groups difference was not statistically significant as indicated by a nonsignificant interaction effect (Group × Time; F = 1.02, P = 0.34), suggesting that the extent of change was equivalent in both groups. The effect size for this comparison was d = 0.61, and power analysis indicated that it would require 12 subjects per group to detect a difference between these 2 interventions in the JTT, our primary outcome measure. There were some items of the JTT in which no improvement in task performance time was observed in some participants; no particular item demonstrated a lack of improvement across participants.

Table 2
Table 2
Image Tools

To evaluate the validity of the CAHAI individuals with SCI, we assessed the relationship between the preintervention values of the JTT and the CAHAI. The scores on the CAHAI were inversely correlated with scores on the JTT (r = −0.59, P = 0.02), indicating that higher scores (ie, improved function) on the CAHAI were correlated with decreased time to complete the tasks on the JTT. This finding establishes the concurrent validity of the CAHAI for use in individuals with SCI. In terms of the effect of unimanual or bimanual training on the CAHAI, the scores of both groups improved significantly as indicated by a significant main effect of time (F = 6.63, P = 0.02; Table 2). The mean change for the bimanual group (3.50 ± 1.84) was similar to that of the unimanual group (2.17 ± 0.79). The between-groups difference was not statistically significant as indicated by a nonsignificant interaction effect (F = 1.02, P = 0.34), suggesting the extent of change due to training was equivalent in both groups.

For the SWMT, the scores of both groups improved significantly as indicated by a significant main effect of time (F = 14.44, P = 0.004; Table 2). The between-groups difference in the extent of change was not statistically significant as indicated by a nonsignificant interaction effect (F = 0.07, P = 0.80). Both intervention groups showed improvement in sensation by 1 to 2 monofilaments. For pinch-grip strength, there was a trend toward improvement; however, across groups there was no significant difference between pre- and postintervention values (F = 1.94, P = 0.20; Table 2). The unimanual group had a mean change of 0.24 (±0.17) pounds, and the bimanual group had a mean change of 1.24 (±1.02) pounds in pinch-grip force. The interaction between time and group was not significant (F = 0.62, P = 0.45). It is likely that the larger intersubject variability combined with the small sample size limited our ability to identify differences.

Back to Top | Article Outline
Corticomotor Outcome Measures

Consistent resting MEPs were obtained from 6 of the 14 participants. For 3 participants, we were unable to evoke resting MEPs in the thenar muscles even at 100% of stimulator output. Two participants had spontaneous potentials that were independent of the stimulation, and when the latency of the spontaneous potentials was similar to the expected latency for the MEPs (between 20 and 30 milliseconds), the 2 potentials could be easily confused. Therefore, these 2 participants did not complete the TMS portion of the protocol. Of those who had resting MEPs, 7 had stable baseline responses of consistent latency and amplitude (3 in the unimanual group and 4 in the bimanual group). However, 1 of the 7 individuals did not complete the study, leaving 6 individuals (3 per group) who completed pre- and postintervention TMS testing. The TMS-related outcome measures comparing pre- and postintervention values are summarized in Table 3.

Table 3
Table 3
Image Tools

Following the intervention, there was a mean increase in cortical map area of 3.84 cm2. This change bordered on statistical significance (t = 2.56, P = 0.05), indicating a strong trend toward enlargement of the cortical map. The change in map area was 3.16 and 3.52 cm2 for those in the unimanual and bimanual intervention groups, respectively. The mean COG of the corticomotor map was 0.94 cm anterior to Cz prior to the intervention and 1.70 cm anterior to Cz following the intervention (Figure 2). However, this mean shift of 0.76 cm (±1.00 cm) in the anterior direction following training was not statistically significant. There was a mean reduction in resting MT of 4.67% (±9.91%) MSO following intervention; this change was not statistically significant (t = 1.10, P = 0.30). The MT decreased by 11% (±11%) MSO and 2% (±2%) MSO for those in the unimanual and bimanual intervention groups, respectively.

Figure 2
Figure 2
Image Tools
Back to Top | Article Outline

DISCUSSION

The purpose of this study was to compare changes in hand function associated with participation in unimanual or bimanual MP, each combined with SS. The findings from this study indicate that the 2 interventions are equivalent in terms of efficacy. Regardless of whether training involves one or both hands, the intervention combining training and stimulation improved both hand motor and sensory functions. It is likely that the small sample size limited our ability to detect between-groups differences in these measures. It is noteworthy that our primary outcome measure, the JTT, is a time-based performance test and does not capture changes in motor strategy that may be functionally important. For example, we noted that in some subjects, while there was little change in performance time between the pre- and postintervention tests, the participant used a different strategy after training, reflecting movement patterns more typical of individuals with no disability (see Video, Supplemental Digital Content 2, pre- and postintervention performance on the card flip component of the JTT in an example participant, http://links.lww.com/JNPT/A7). Compared with the former compensatory strategies that may have been used for many years prior to the training, this emergent strategy is new to the participant. Since the new strategy is more efficient, it is likely that with repeated application and practice the participant will be able to perform tasks more quickly with the new strategy than with the old compensatory strategy.

The finding that participating in a program of combined MP and SS is associated with improved function is consistent with our prior reports of unimanual hand training in individuals with SCI.15,16 In individuals with SCI, sensory stimulation alone can improve sensory function, pinch-grip strength, and unimanual hand function, and unimanual MP can improve unimanual hand function.16 However, the combination of the 2 interventions is associated with significantly greater improvements in hand function than either of the 2 interventions in isolation and only the combined intervention is associated with an improvement in sensory scores.15,16

In the present study, the overall effect of the combined intervention on change in sensory function was significant and was reflected in a change of 1 or 2 monofilaments. This change is equal to the effect size (d = 1.5) reported in the literature for the clinically meaningful changes in sensory function associated with recovery from peripheral nerve damage.29 However, while prior studies have identified improved pinch-grip strength following the combined intervention, and we identified a trend toward greater strength in our sample, the change in grip strength was not significant. There was great intersubject variability in this measure, which might have resulted in the group sizes being underpowered to identify a difference. It is also plausible that a floor effect may account for the lack of significant change in this measure. Only 6 of 11 subjects were able to generate sufficient force to register the lowest value (0.1 lb or 45.36 g) on the dynamometer. No change in grip strength was observed in individuals who were initially unable to generate force on the dynamometer.

On average, training was associated with an increase in the size of the corticomotor area associated with the thenar muscles and a shift in the COG of the corticomotor map to a more anterior location. The strong trend (P = 0.05) toward enlargement in cortical representation of the thenar muscles following the intervention is consistent with results following unimanual training in individuals poststroke,37 in whom the size of the corticomotor map of the abductor pollicis brevis increased following intervention. Results related to bimanual training after stroke are equivocal. Luft et al38 used functional magnetic resonance imaging to investigate the size of the map following a bimanual program and found an increase in the size of the map following the intervention. Other investigators have not identified an enlargement of the map but rather more symmetrical levels of excitability. Lewis and Byblow39 investigated the map changes in both hemispheres following a rhythmic bilateral movement program in individuals poststroke. While there was no change in the map of the affected hemisphere, there was a reduction in the map volume on the nonaffected side. The authors suggested the balancing of interhemispheric inhibition and excitation could be an explanation for their findings.

Maladaptive cortical reorganization in individuals with SCI includes displacement of the corticomotor representation to a more posterior location.9,40,41 Therefore, an anterior shift in the COG may suggest that the corticomotor representation has shifted to a position characteristic of individuals who have demonstrated recovery.41 Anterior shifts in COG may be one of the mechanisms that explain the improvements in function demonstrated by these participants. It is possible that the COG of the map shifted to a more anterior position in 4 of the 6 individuals (Figure 2); however, this finding was not significantly different following the intervention. While the variability of the COG in individuals with SCI is not known, we hypothesize that it is similar to that in individuals with other movement disorders. The variability of the COG in the affected hemisphere in individuals with chronic stroke is 1.13 cm (in the absence of intervention); 42 therefore, the magnitude of change in the present study is within the range of the hypothesized variability of this measure.

The MT was not significantly different following training. This was somewhat surprising, as SS alone has been shown to increase excitability in individuals with no disability.32 Furthermore, Beekhuizen and Field-Fote15,16 identified a decrease in MT in individuals with SCI following unimanual MP and SS. While the mean resting MT was not different following intervention, the mean change in MT was greater for those in the unimanual intervention than in the bimanual intervention. Perhaps, those individuals who focused on a single upper extremity have greater changes in excitability of the associated cortex. As noted previously, the intensity of training of the weaker hand is likely to have been greater in the group receiving unimanual training. It is possible that the present study was underpowered to identify changes in excitability, as only 6 individuals completed the TMS testing and training. Alternatively, it is possible that improvements in hand function in individuals with SCI are more related to increases in corticomotor representation rather than changes in excitability. The SS may induce a short-term increase in excitability that provides an opportunity for corticomotor reorganization.

Back to Top | Article Outline
Limitations of this Study

The small sample size of this study prohibits definitive conclusions regarding the comparative efficacy of bimanual compared with unimanual MP training. In addition, there was significant variability among the participants in terms of impairments and ability to perform activities. There may also have been important differences in pathology, as both individuals with upper and lower motor neuron injuries were included as long as they could demonstrates some active thumb opposition. While baseline statistics were similar between groups, future studies should consider stratification to ensure baseline equality between measures. Postintervention testing was performed soon after the completion of the intervention. This might have provided insufficient time for consolidation of the new movement strategies that emerged as part of training; future studies should include follow-up assessment. Less than half of the participants were able to be included in the TMS data primarily because of either a lack of an MEP at rest or the presence of spontaneous potentials that could not be distinguished from MEPs. To increase the sample size for measures of corticomotor activity, future investigations should evaluate changes in TMS outcomes under normalized conditions of minimal muscle contraction.

Back to Top | Article Outline

CONCLUSION

Individuals with chronic tetraplegia due to SCI can improve hand function with a simple, intensive hand training program combined with SS. Our data suggest that when combined with SS, both unimanual training and bimanual training are associated with improved ability to perform tasks with the upper extremities. In individuals with chronic cervical SCI, training-related changes in motor and sensory functions of the hand appear to be accompanied by changes in cortical organization and excitability.

The authors appreciate the technical contributions of Lanitia Ness, PhD, and Mohd Khan.

Back to Top | Article Outline

REFERENCES

1. National Spinal Cord Injury Information Network. Spinal cord injury facts and figures at a glance: 2009. https://www.nscisc.uab.edu/public_content/pdf/FactsApr09.pdf. Accessed March 26, 2010.

2. Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2004; 21(10):1371–1383.

3. Snoek GJ, Ijzerman MJ, Hermens HJ, Maxwell D, Biering-Sorensen F. Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics. Spinal Cord. 2004; 42(9):526–532.

4. Bruehlmeier M, Dietz V, Leenders KL, et al. How does the human brain deal with a spinal cord injury? Eur J Neurosci. 1998; 10(12):3918–3922.

5. Curt A, Keck ME, Dietz V. Functional outcome following spinal cord injury: significance of motor-evoked potentials and ASIA scores. Arch Phys Med Rehabil. 1998; 79(1):81–86.

6. Davey NJ, Smith HC, Wells E, et al. Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury. J Neurol Neurosurg Psychiatry. 1998; 65(1):80–87.

7. Davey NJ, Smith HC, Savic G, et al. Comparison of input-output patterns in the corticospinal system of normal subjects and incomplete spinal cord injured patients. Exp Brain Res. 1999; 127(4):382–390.

8. Brouwer B, Hopkins-Rosseel DH. Motor cortical mapping of proximal upper extremity muscles following spinal cord injury. Spinal Cord. 1997; 35(4):205–212.

9. Hoffman LR, Field-Fote EC. Cortical reorganization following bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys Ther. 2007; 87(2):208–223.

10. Chen R, Cohen LG, Hallett M. Nervous system reorganization following injury. Neuroscience. 2002; 111(4):761–773.

11. Wolf SL, Blanton S, Baer H, Breshears J, Butler AJ. Repetitive task practice: a critical review of constraint-induced movement therapy in stroke. Neurologist. 2002; 8(6):325–338.

12. Taub E, Uswatte G. Constraint-induced movement therapy: bridging from the primate laboratory to the stroke rehabilitation laboratory. J Rehabil Med. 2003;(41)(suppl):34–40.

13. Conforto AB, Cohen LG, dos Santos RL, Scaff M, Marie SK. Effects of somatosensory stimulation on motor function in chronic cortico-subcortical strokes. J Neurol. 2007; 254(3):333–339.

14. Conforto AB, Kaelin-Lang A, Cohen LG. Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol. 2002; 51(1):122–125.

15. Beekhuizen KS, Field-Fote EC. Massed practice versus massed practice with stimulation: effects on upper extremity function and cortical plasticity in individuals with incomplete cervical spinal cord injury. Neurorehabil Neural Repair. 2005; 19(1):33–45.

16. Beekhuizen KS, Field-Fote EC. Sensory stimulation augments the effects of massed practice training in persons with tetraplegia. Arch Phys Med Rehabil. 2008; 89:602–608.

17. Hess CW, Mills KR, Murray NM. Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol. 1987; 388:397–419.

18. Stinear CM, Walker KS, Byblow WD. Symmetric facilitation between motor cortices during contraction of ipsilateral hand muscles. Exp Brain Res. 2001; 139(1):101–105.

19. Renner CI, Woldag H, Atanasova R, Hummelsheim H. Change of facilitation during voluntary bilateral hand activation after stroke. J Neurol Sci. 2005; 239:25–30.

20. Vercauteren K, Pleysier T, Van Belle L, Swinnen SP, Wenderoth N. Unimanual muscle activation increases interhemispheric inhibition from the active to the resting hemisphere. Neurosci Lett. 2008; 445(3):209–213.

21. De Weerd P, Reinke K, Ryan L, et al. Cortical mechanisms for acquisition and performance of bimanual motor sequences. Neuroimage. 2003; 19(4):1405–1416.

22. Sadato N, Yonekura Y, Waki A, Yamada H, Ishii Y. Role of the supplementary motor area and the right premotor cortex in the coordination of bimanual finger movements. J Neurosci. 1997; 17(24):9667–9674.

23. Toyokura M, Muro I, Komiya T, Obara M. Activation of pre-supplementary motor area (SMA) and SMA proper during unimanual and bimanual complex sequences: an analysis using functional magnetic resonance imaging. J Neuroimaging. 2002; 12(2):172–178.

24. Zarzecki P, Shinoda Y, Asanuma H. Projection from area 3a to the motor cortex by neurons activated from group I muscle afferents. Exp Brain Res. 1978; 33: 269–282.

25. Panizza M, Nilsson J, Roth BJ, Basser PJ, Hallett M. Relevance of stimulus duration for activation of motor and sensory fibers: implications for the study of H-reflexes and magnetic stimulation. Electroencephalogr Clin Neurophysiol. 1992; 85(1):22–29.

26. van Tuijl JH, Janssen-Potten YJ, Seele HA. Evaluation of upper extremity motor function tests in tetraplegics. Spinal Cord. 2002; 40(2):51–64.

27. Barreca SR, Stratford PW, Lambert CL, Masters LM, Streiner DL. Test-retest reliability, validity, and sensitivity of the Chedoke arm and hand activity inventory: a new measure of upper-limb function for survivors of stroke. Arch Phys Med Rehabil. 2005; 86(8):1616–1622.

28. Weinstein S. Fifty years of somatosensory research: from the Semmes-Weinstein monofilaments to the Weinstein Enhanced Sensory Test. J Hand Ther. 1993; 6(1):11–22.

29. Jerosch-Herold C. Assessment of sensibility after nerve injury and repair: a systematic review of evidence for validity, reliability and responsiveness of tests. J Hand Surg [Br]. 2005; 30(3):252–264.

30. Wassermann EM, McShane LM, Hallett M, Cohen LG. Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol. 1992; 85(1):1–8.

31. Malcolm MP, Triggs WJ, Light KE, et al. Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clin Neurophysiol. 2006; 117:1037–1046

32. Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res. 2000; 131(1):135–143.

33. Mills KR, Boniface SJ, Schubert M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol. 1992; 85(1):17–21.

34. Rossini PM, Barker AT, Berardelli A, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 1994; 91(2):79–92.

35. Thickbroom GW, Byrnes ML, Mastaglia FL. Methodology and application of TMS mapping. Electroencephalogr Clin Neurophysiol Suppl. 1999; 51:48–54.

36. Kleim JA. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res. 2008; 51(1):S225–239.

37. Liepert J, Miltner WH, Bauder H, et al. Motor cortex plasticity during constraint-induced movement therapy in stroke patients. Neurosci Lett. 1998; 250(1):5–8.

38. Luft AR, McCombe-Waller S, Whitall J, et al. Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. JAMA. 2004; 292(15):1853–1861.

39. Lewis GN, Byblow WD. Neurophysiological and behavioural adaptations to a bilateral training intervention in individuals following stroke. Clin Rehabil. 2004; 18(1):48–59.

40. Green JB, Sora E, Bialy Y, Ricamato A, Thatcher RW. Cortical sensorimotor reorganization after spinal cord injury: an electroencephalographic study. Neurology. 1998; 50(4):1115–1121.

41. Green JB, Sora E, Bialy Y, Ricamato A, Thatcher RW. Cortical motor reorganization after paraplegia: an EEG study. Neurology. 1999; 53(4):736–743.

42. Butler AJ, Kahn S, Wolf SL, Weiss P. Finger extensor variability in TMS parameters among chronic stroke patients. J Neuroeng Rehabil. 2005; 2:10. http://www.jneuroengrehab.com/content/2/1/10. Accessed April 22, 2010.

Supplemental Digital Content

Back to Top | Article Outline

© 2010 Neurology Section, APTA

Login

Article Tools

Images

Share

Follow JNPT on Twitter