405
NeuroRehabilitation 35 (2014) 405–414 DOI:10.3233/NRE-141131 IOS Press
Segmental muscle vibration modifies muscle activation during reaching in chronic stroke: A pilot study Marco Paolonia,∗ , Emanuela Taverneseb , Massimo Finic , Patrizio Salec , Marco Franceschinic , Valter Santillia and Massimiliano Mangonea a Department
of Physical Medicine and Rehabilitation, Sapienza – University of Rome, Rome, Italy Neuro-Rehabilitation Division, Bambino Gesu` Children’s Hospital, IRCCS, Rome, Italy c IRCSS San Raffaele Pisana, Rome, Italy b Pediatric
Abstract. BACKGROUND: Segmental muscle vibration (SMV) improves motor performances in neurological conditions, including stroke. OBJECTIVE: To determine if SMV modifies upper limb muscular activity in chronic stroke patients performing a reaching movement. METHODS: We randomized 22 chronic stroke patients to an experimental group (EG; n = 12), receiving 10 sessions of exercise + 120 Hz SMV over the biceps brachii (BB) and the flexor carpi ulnaris (FCU) muscles, or to a control group (CG; n = 10) receiving exercise only. All subjects performed a reaching movement with the affected side before and 4 weeks after therapy ended. We recorded surface EMG activity of the anterior deltoid (AD), posterior deltoid (PD), BB, triceps brachii (TB), FCU and extensor carpi radialis (ECR) muscles. We calculated muscular onset times, modulation ratio, co-contractions and degree of contraction. RESULTS: After SMV, onset times of the PD (p = 0.03), BB (p = 0.02) and ECR (p = 0.04) in the EG were less anticipated than at baseline; the modulation ratio increased in AD (p = 0.003) and BB (p = 0.01); co-contractions decreased in the pairs BB/TB (p = 0.007), PD/BB (p = 0.004) and AD/BB (p = 0.01); and the degree of contraction decreased in BB (p = 0.01). CONCLUSIONS: The modulation of muscular function induced by SMV may aid to explain its action on smoothness and coordination of movements. Keywords: Stroke, rehabilitation, electromyography, reaching movement, vibration therapy
1. Introduction Motor disability following a stroke is often due to poor arm function. Indeed, chronic stroke sufferers may lose their ability to perform motor functions as a result of reduced neural drive from the cortex to motor units (Hara, Masakado, & Chino, 2004) and to a de∗ Address for correspondence: Marco Paoloni, Department of Physical Medicine and Rehabilitation, “Sapienza” – University of Rome, Piazzale Aldo Moro, 5 00185 Rome, Italy. Tel.: +39 6 49975924; E-mail: [email protected].
synchronized firing rate of motor units (Gemperline, Allen, Walk, & Rymer, 1995). This ultimately leads to muscle weakness (Bourbonnais & Vanden Noven, 1989; Chae, Yang, Park, & Labatia, 2002), slowness of movement (Canning, Ada, & O’Dwyer, 1999) and uncoordinated muscular contractions during the performance of a given motor task (Levin, 1996). One of the most important actions performed by the upper limb, which allows the hand to interact with the environment, is reaching (Wu, Trombly, Lin, & TickleDegnen, 2000), a complex multi-joint movement to a
1053-8135/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
406
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
defined point in space (Georgopoulos, 1986). Acute and sub-acute stroke patients are subject to various alterations in the electromyographic (EMG) activities of the upper limb muscles when they perform the reaching movement, including altered muscle onset times, a reduced ability to modulate EMG activity at the beginning of the movement and an increased degree of muscular contraction (Wagner, Dromerick, Sahrmann, & Lang, 2007). Mechanical stimuli, delivered as segmental muscle vibration (SMV), have been successfully used in some neurological conditions, such as chronic stroke (Noma, Matsumoto, Etoh, Shimodozono, & Kawahira, 2009; Noma, Matsumoto, Shimodozono, Etoh, & Kawahira, 2012), multiple sclerosis (Paoloni et al., 2013) and spinal cord injury (Murillo et al., 2011), to improve several features of motor performance. Acting on muscle spindle primary endings (Roll, Vedel, & Ribot, 1989), SMV induces the generation of Ia inputs, which can alter the excitability of the corticospinal pathway (Steyvers, Levin, Van Baelen, & Swinnen, 2003) by modulating intracortical inhibiting and facilitating inputs to the primary motor cortex (Rosenkranz, Pesenti, Paulus, & Tergau, 2003; Rosenkranz & Rothwell, 2003). Recently, SMV, added to general physical therapy, has been shown to improve reaching performances in chronic stroke patients (Tavernese et al., 2013). One intriguing hypothesis is that these motor improvements may be accompanied, or even determined, by changes in muscle activation characteristics during movement. To test this hypothesis, we designed a pilot randomized controlled trial to verify whether SMV in chronic stroke patients performing a reaching movement induces any changes in surface EMG activities of the shoulder, arm and forearm muscles.
2. Materials and methods 2.1. Subjects We considered eligible for the present research hemiparetic patients (right or left hemiparesis of at least 6 months’ duration secondary to ischemic stroke) of both sexes, aged between 40 and 85 years, without any other neurological conditions (e.g. multiple sclerosis, Parkinson’s disease, bilateral brain lesions, ischemic involvement of the cerebellum or basal ganglia or cognitive impairment). Further exclusion criteria were: injections performed to treat spasticity 6 months prior to participation in the study, or rheumatic and orthopedic conditions that may interfere with upper limb
movements. The study protocol was approved by the local ethics committee. The experimental protocol was explained to the participants, all of whom gave their informed consent prior to participation. Participants who fulfilled the inclusion/exclusion criteria were randomly assigned to either the experimental group (EG) or control group (CG) by an independent person who selected a sealed envelope 30 minutes before the intervention was due to start. 2.2. Clinical and instrumental evaluation All the participants underwent a clinical and an instrumental evaluation before the training started (baseline), and an instrumental evaluation 1 month after therapy ended (Fig. 1). To obtain normative data for the variables analyzed, we also recruited ten age-matched healthy subjects (5 males; mean age 60.0 ± 4.9 years; range 50–65), with no neurological and/or orthopedic impairments. Healthy subjects only performed one kinematic evaluation, according to the same modalities as those used for the EG and CG patients. At baseline, we collected all the patients’ demographic and clinical characteristics by means of an interview and a clinical evaluation. We focused, in particular, on: recovery of motor function by determining the patients’ Brunnstrom’s stage; movements, coordination and reflexes of the upper limb as measured by means of the Fugl-Meyer assessment scale of the upper extremity (Gladstone, Danells, & Black, 2002); spasticity at the shoulder, elbow and wrist as assessed by means of the Modified Ashworth (Bohannon & Smith, 1987). The motor task we analyzed consisted of a single reaching movement of the affected limb. The subjects sat on a chair whose height could be adjusted, with the feet resting on the floor and the knees and hips bent at 90◦ . With their hand placed on their thigh, they were asked to move their hand toward the target marker as rapidly and as accurately as possible, without moving their backs away from the backrest. After a warm-up and familiarizing session in which the subjects cyclically performed a series of reaching movements, we acquired five trials and we considered for the data analysis the mean values of the EMG measurements. After the reaching trial data had been collected, we performed an additional EMG recording for each muscle during maximal voluntary isometric contraction (MVC). The kinematic analysis was performed by means of an optoelectronic stereophotogrammetric system (ELITE, BTS, Milan, Italy), with a sampling rate of 100 Hz, to capture the movement of a retro-reflective marker
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
407
Fig. 1. Flow-chart diagram of the study. SMV: segmental muscle vibration.
placed over the base of 2nd metacarpal joint on the analyzed side. We placed a target marker in front of the subject, at shoulder height, at a distance that slightly exceeded the sum of the lengths of the arm and forearm. Given the distance between the hand marker and the target marker, we used the 3-point differentiation method to calculate the mean linear velocity. The mean linear velocity was filtered using a low-pass, secondorder Butterworth filter (cut-off frequency, 5 Hz), and used to determine the start (defined as the instant in which the velocity exceeded 5% of the maximum velocity recorded during the task) and the end (defined as the instant in which the velocity dropped to zero) of the movement. We acquired surface myoelectric signals with a sampling rate of 1000 Hz using a 16-channel telemetric transmission surface electromyography (pocket EMG System; BTS, Milan, Italy). The lower and upper cut-off frequencies of the Hamming filter were 10 and
400 Hz, respectively, whereas the common mode reaction ratio was 100 dB. To record surface EMG we used a pair of Ag/AgCl electrodes, with an inter-electrode space of 2 cm, placed on the skin overlying the muscle belly of the posterior deltoid (PD), anterior deltoid (AD), biceps brachii (BB), triceps brachii (TB), flexor carpi ulnaris (FCU) and extensor carpi radialis (ECR). We rectified, low-pass filtered with an upper cut-off frequency of 5 Hz, and integrated using a mobile window of 125 ms the raw signal, to obtain the envelope. 2.3. Interventions All the participants underwent a 60-minute general physical therapy session, 5 times per week, over a period of 2 weeks. These sessions comprised stretching, muscle strengthening and specific training for reaching and reaching-to-grasp movements. Participants in the EG
408
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
also received 30 minutes of low-amplitude SMV at a fixed frequency of 120 Hz over the target muscles, i.e. the BB and the FCU on the affected side, by means of a commercial device (Horus, Akropolis, Rome, Italy). We set the vibration amplitude at 10 m to drive Ia spindle afferents (Brown, Engberg, & Matthews, 1967) and we delivered the 30-minute stimulation session in trains of 6" divided by 1" pauses (Tavernese et al., 2013), at the end of each general physical therapy session with the patient lying supine. We assessed, the occurrence of muscle pain or skin lesions in patients in the EG at the end of each session.
was demonstrated by MR > 1 (higher values represent greater muscle activation), while a MR = 1 means no modulation. We computed the %MCV as the ratio between the peak envelope value during reaching and the peak envelope value during the MVC trial (Wagner et al., 2007). All EMG data were analyzed off-line by means of a dedicated software (SMART Analyzer, BTS, Milan, Italy) by an assessor who was blinded to the randomization.
2.4. Outcome measures
To perform the statistical analysis we used the MedCalc® 12.2.1.0 (MedCalc Software). Following randomization, we verified normal distribution of all the variables analyzed in both groups by means of a D’Agostino-Pearson test, and we applied parametric or non-parametric tests, as appropriate, to compare means. We used the unpaired t-test or Mann-Whitney test to compare the pre- and post-treatment data in EG and CG and the paired t-test or the Wilcoxon matched pairs test to assess differences between pre- and post-treatment values in the two groups. We set the level of significance at p < 0.05 for all the analyses and we applied a Bonferroni correction to reduce type I error in interpreting the data. We conducted all the analyses according to the intention-to-treat principle.
As outcome measures we assessed the following: muscle onset time, co-contraction index (CCI), modulation ratio (MR) and percentage of activation in relation to the MVC (%MVC). We defined the muscle onset time as the time in which the enveloped EMG signal passed the baseline threshold (defined as the resting mean EMG value plus 2 standard deviation) for > 30 ms (Wagner et al., 2007), with the value 0 ms representing the start of the movement, with negative values representing muscle pre-activation before the movement starts and positive values representing muscle activation after the movement has started. We considered the CCI (Hu et al., 2007) for the following muscle pairs: the agonist/antagonist muscles of the shoulder, arm and forearm (AD/PD, BB/TB, FCU/ECR, respectively); the main synergistic muscles for the reaching movement (AD/TB), and their respective antagonists (PD/BB); the shoulder flexor muscles (AD/BB). We calculated the CCI according to the following formula (Frost, Dowling, Dyson, & Bar-Or, 1997): CCI =
start
end
Aij (t) dt
(1)
where Aij (t) is the overlapping activity of the EMG envelopes for muscles i and j, T is the length of the signal, and start and end represent, respectively, the start and the end of the reaching movement as defined above. Higher CCI values indicate greater co-contraction. The MR expresses the ability to properly increase muscle activation at the start of the reaching movement. We calculated MR as the ratio of integrated EMG activity during the first 100 ms of contraction and the resting mean value (Lang & Bastian, 1999). Modulation
2.5. Statistical analysis
3. Results We considered eligible for the study thirty-five patients, randomly selected from among those referring to our outpatient service between October 2012 and June 2013, and we randomized to either the EG (n = 12) or CG (n = 10) those patients who satisfied the inclusion criteria (Fig. 1). The demographic and clinical baseline characteristics of the two groups were well balanced (Table 1). We did not observe adverse events in either the EG or CG, and all the patients completed the treatment and performed the post-treatment assessment. Muscle onset times are shown in Fig. 2. We observed no differences at baseline between patients in the EG and those in the CG in any of the onset times considered. We found significant differences between pre- and post-treatment in the EG as regards the PD (total of ranks = 6.00; p = 0.03), BB (t = 2.75; p = 0.02) and ECR (t = 2.35; p = 0.04) muscle onset times. We found the muscle onset time to be closer to zero following treatment in all the cases (Fig. 2). We could not find
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
409
Table 1 Demographic and clinical characteristics of patients in both groups at baseline Experimental Group (n = 12) Age (years)1 Gender (Males/Females) Time since acute event (months) 1 Right/left hemiplegia (n) Upper extremity Brunnstrom stage2 Fugl-Meyer Scale (upper extremity) 2 Modified Ashworth Scale2 Shoulder Elbow Wrist 1 Data
Control Group (n = 10)
p
60.3 ± 15.3 7/5 15.5 ± 14.9 4/8 5.5 (5.0 – 6.0) 48/66 (44.25 – 54.5)
60.7 ± 13.2 6/4 13.0 ± 5.0 4/6 5.0 (5.0 – 6.0) 49/66 (44.75 – 55.75)
n.s. n.s. n.s. n.s. n.s. n.s.
1.0 (1.0 – 2.0) 1.0 (0.0 – 2.0) 1.0 (0.0 – 1.0)
1.0 (1.0 – 2.0) 1.0 (1.0 – 2.0) 1.0 (0.0 – 1.125)
n.s. n.s. n.s.
are expressed as means ± SD. 2 Median values (25th–75th interquartiles). n.s.: not significant.
differences between pre- and post-treatment in the CG in any of the muscle onset times. We found the posttreatment PD muscle onset time significantly closer to zero in the EG than in the CG (t = 3.11; p = 0.005), whereas we did not observe any differences for the other variables analyzed. The results of the CCI are shown in Table 2. We did not detect any differences at baseline between the EG and CG in any of the values investigated. We found patients in the EG to have a significantly lower CCI in the post-treatment assessment than at baseline for the pairs BB/TB (t = 3.31; p = 0.007), PD/BB (t = 3.60; p = 0.004) and AD/BB (t = 3.066; p = 0.01). No other significant changes emerged between the pre- and posttreatment CCI values. We did not find any differences in the CCI between pre- and post-treatment in the CG, except for AD/PD (t = 2.92; p = 0.02), which was lower in the post-treatment evaluation. When post-treatment values between groups were compared, we found the CCI to be significantly lower in the EG for PD/BB (t = 2.21; p = 0.04) and AD/BB (t = 2.29; p = 0.04). Table 3 shows the results of MR. No significant differences emerged between groups at baseline. At the post-treatment assessment, patients in the EG modulated the AD (t = 3.782; p = 0.003) and BB (t = 3.044; p = 0.01) significantly better than at baseline. We found no differences between the pre- and post-treatment evaluation in the CG. Patients in the EG modulated the AD (t = 3.235; p = 0.004) and BB (t = 2.923; p = 0.01) significantly better than those in the CG at the posttreatment evaluation. As regards the %MCV, we did not find any significant difference at baseline between groups. In the EG we only pointed out a significant difference only for the BB, whose %MCV value was lower at the post-treatment evaluation than at the baseline (t = 2.995; p = 0.01). We found no differences between baseline and post-treatment values in the CG. The
between-groups comparison at the post-treatment evaluation revealed a significantly lower %MCV value for the BB in the EG than in the CG (t = 2.467; p = 0.03). No differences emerged in any of the other variables analyzed (Table 4).
4. Discussion In the present pilot study, we performed an EMG analysis of reaching in chronic stroke patients to assess the short-term effects of 10 applications of SMV on upper limb muscle activity. We studied various aspects of dynamic muscular function so as to determine the timing of muscular activation, its modulation and the degree of muscular contraction during movement. Our findings demonstrate that SMV modulates muscular activity during the execution of reaching movement. In particular, the target muscle responsible for the majority of the changes we observed is the BB, which modulates its activity most effectively in the milliseconds that immediately follow the movement onset, generally requires less force and induces a lower degree of co-contraction with the others arm muscles following vibration therapy. All the patients recruited in our study demonstrated, at each follow-up, a pre-activation of all the muscles examined, which means that the onset of activation always occurred before the start of reaching movement (considered as time zero). Wagner and colleagues (2007) found that the onset of pre-activation in acute and sub-acute stroke patients is delayed, sometimes even occurring after the movement starts, which is contrast to what is observed in healthy subjects. In our study, the pre-activation pattern in healthy controls was similar to that found by Wagner and colleagues (2007), and differs from the pattern observed in patients. In the pre-treatment sessions, all the patients displayed an
410
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
Fig. 2. Baseline (a) and post-treatment (b) group mean muscle onset times during reaching for the examined muscles for the experimental group (black triangles) and the control group (black circles), compared with healthy subjects (c, black squares). Numeric values are mean ± standard deviation muscle onset times (ms) for each muscle. Error bars represent standard deviations.
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
411
Table 2 Mean ± standard deviations (95% CI) of co-contraction index values for the examined muscle pairs. Significant values are in bold AD/PD Baseline Post-treatment p Value2 BB/TB Baseline Post-treatment p Value2 FCU/ECR Baseline Post-treatment p Value2 AD/TB Baseline Post-treatment p Value2 PD/BB Baseline Post-treatment p Value2 AD/BB Baseline Post-treatment p Value2
Experimental Group
Control Group
p Value1
Healthy subjects
0.20 ± 0.15 (0,11 to 0.30) 0.14 ± 0.14 (0.04 to 0.22) 0.17
0.25 ± 0.12 (0.16 to 0.34) 0.18 ± 0.08 (0.12 to 0.23) 0.02
0.46 0.42
0.02 ± 0.02 (0.01 to 0.04)
0.09 ± 0.05 (0.06 to 0.12) 0.07 ± 0.03 (0.05 to 0.09) 0.007
0.10 ± 0.04 (0.07 to 0.13) 0.11 ± 0.07 (0.06 to 0.16) 0.71
0.72 0.11
0.02 ± 0.01 (0.01 to 0.03)
0.10 ± 0.11 (0.03 to 0.17) 0.11 ± 0.07 (0.06 to 0.15) 0.34
0.09 ± 0.10 (0.02 to 0.16) 0.07 ± 0.05 (0.04 to 0.11) 0.55
0.79 0.26
0.02 ± 0.02 (0.01 to 0.04)
0.12 ± 0.07 (0.08 to 0.16) 0.12 ± 0.11 (0.05 to 0.19) 0.94
0.12 ± 0.05 (0.09 to 0.16) 0.14 ± 0.09 (0.07 to 0.20) 0.68
0.89 0.75
0.04 ± 0.02 (0.02 to 0.05)
0.09 ± 0.05 (0.06 to 0.12) 0.07 ± 0.05 (0.04 to 0.10) 0.004
0.12 ± 0.04 (0.09 to 0.14) 0.12 ± 0.07 (0.07 to 0.17) 0.90
0.14 0.04
0.02 ± 0.01 (0.01 to 0.02)
0.13 ± 0.06 (0.09 to 0.16) 0.10 ± 0.03 (0.08 to 0.12) 0.01
0.16 ± 0.06 (0.12 to 0.21) 0.16 ± 0.08 (0.10 to 0.22) 0.88
0.20 0.04
0.03 ± 0.01 (0.02 to 0.03)
AD: anterior deltoid; PD: posterior deltoid; BB: biceps brachii; TB: triceps brachii; FCU: flexor carpi ulnaris; ECR: extensor carpi radialis. 1 : within group comparison at each follow-up; 2 : between group comparison.
Table 3 Mean ± standard deviations (95% CI) of modulation ratio values. Significant values are in bold AD Baseline Post-treatment p Value2 PD Baseline Post-treatment p Value2 BB Baseline Post-treatment p Value2 TB Baseline Post-treatment p Value2 FCU Baseline Post-treatment p Value2 ECR Baseline Post-treatment p Value2
Experimental Group
Control Group
p Value1
Healthy subjects
1.98 ± 0.50 (1.67 to 2.30) 2.65 ± 0.68 (2.22 to 3.08) 0.003
1.98 ± 0.72 (1.47 to 2.49) 1.77 ± 0.56 (1.37 to 2.18) 0.32
0.99 0.004
3.18 ± 1.85 (1.67 to 4.32)
1.83 ± 0.31 (1.63 to 2.02) 1.82 ± 0.62 (1.42 to 2.21) 0.52
1.82 ± 0.32 (1.59 to 2.05) 1.81 ± 0.66 (1.34 to 2.29) 0.99
0.93 0.51
2.09 ± 1.00 (1.39 to 2.75)
1.61 ± 0.40 (1.35 to 1.86) 2.55 ± 1.23 (1.77 to 3.34) 0.01
1.48 ± 0.35 (1.23 to 1.73) 1.48 ± 0.30 (1.26 to 1.69) 0.96
0.44 0.01
3.39 ± 2.70 (1.85 to 4.75)
1.49 ± 0.21 (1.35 to 1.62) 1.46 ± 0.17 (1.35 to 1.57) 0.91
1.43 ± 0.25 (1.25 to 1.61) 1.46 ± 0.25 (1.28 to 1.63) 0.64
0.55 0.79
2.11 ± 1.05 (1.49 to 2.11)
1.56 ± 0.30 (1.37 to 1.75) 1.67 ± 0.67 (1.24 to 2.10) 0.91
1.42 ± 0.27 (1.22 to 1.61) 1.43 ± 0.32 (1.20 to 1.65) 0.84
0.35 0.51
1.72 ± 0.38 (1.47 to 1.95)
1.62 ± 0.32 (1.41 to 1.82) 1.68 ± 0.65 (1.27 to 2.10) 0.73
1.64 ± 0.47 (1.31 to 1.98) 1.61 ± 0.39 (1.33 to 1.89) 0.81
0.88 0.89
1.97 ± 0.72 (1.46 to 2.12)
AD: anterior deltoid; PD: posterior deltoid; BB: biceps brachii; TB: triceps brachii; FCU: flexor carpi ulnaris; ECR: extensor carpi radialis. 1 : within group comparison at each follow-up; 2 : between group comparison.
412
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke Table 4 Mean ± standard deviations (95% CI) of percentage of muscle activation with respect to isometric maximum voluntary contraction values. Significant values are in bold AD Baseline Post-treatment p Value2 PD Baseline Post-treatment p Value2 BB Baseline Post-treatment p Value2 TB Baseline Post-treatment p Value2 FCU Baseline Post-treatment p Value2 ECR Baseline Post-treatment p Value2
Experimental Group
Control Group
p Value1
66.0 ± 19.9 (53.4 to 78.7) 73.5 ± 24.9 (57.7 to 89.4) 0.50
78.1 ± 11.8 (69.6 to 86.5) 72.9 ± 22.9 (56.4 to 89.3) 0.50
0.11 0.95
25.1 ± 23.6 (10.1 to 40.1) 23.2 ± 27.4 (5.8 to 40.6) 0.73
33.1 ± 31.8 (10.4 to 55.9) 47.0 ± 32.6 (23.6 to 70.3) 0.30
0.50 0.08
3.4 ± 2.4 (1.7 to 4.8)
22.2 ± 9.4 (16.2 to 28.2) 17.2 ± 7.0 (12.7 to 21.7) 0.01
29.8 ± 13.7 (20.0 to 39.6) 31.8 ± 17.5 (19.2 to 44.3) 0.75
0.14 0.03
4.7 ± 2.6 (2.3 to 7.6)
27.3 ± 12.9 (19.1 to 35.5) 21.6 ± 19.0 (9.5 to 33.7) 0.08
29.1 ± 12.2 (20.4 to 37.9) 32.7 ± 22.5 (16.6 to 48.8) 0.53
0.73 0.22
8.4 ± 4.8 (4.4 to 13.7)
31.3 ± 33.4 (10.1 to 52.5) 19.9 ± 11.8 (12.4 to 27.4) 0.13
30.7 ± 29.3 (9.7 to 51.6) 22.9 ± 23.1(6.4 to 39.5) 0.13
0.96 0.71
7.6 ± 7.5 (1.2 to 15.9)
29.2 ± 11.5 (21.8 to 36.5) 26.8 ± 11.6 (19.4 to 34.2) 0.23
27.7 ± 15.2 (16.8 to 38.5) 21.3 ± 15.9 (9.9 to 32.7) 0.12
0.79 0.88
10.0 ± 5.3 (6.0 to 15.4)
Healthy subjects 50.4 ± 27.5 (34.0 to 76.7)
AD: anterior deltoid; PD: posterior deltoid; BB: biceps brachii; TB: triceps brachii; FCU: flexor carpi ulnaris; ECR: extensor carpi radialis. 1 : within group comparison at each follow-up, 2 : between group comparison.
overly anticipated pre-activation of the PD, BB, FCU and ECR, and a delayed pre-activation of the TB. The changes observed following SMV in the EG demonstrate a trend to normalization for the BB, PD and ECR onset times, which displayed a significantly less anticipated pre-activation (Fig. 2). According to our results, SMV influences the MR, an index used to calculate a person’s ability to rapidly activate muscles. In particular, we observed an increased MR for the AD and BB muscles following SMV. In our healthy subjects, the AD and BB, the prime reaching effectors, are the muscles displaying the greatest degree of modulation, thereby confirming data in the literature (Wagner et al., 2007). We may therefore interpret the increase in the MR following SMV as an improvement in muscular function, particularly with regard to a person’s ability to produce movement when required. We calculated the %MVC to quantify the degree of muscular contraction used to perform the movement. According to our results, the %MVC for the BB in patients in our EG dropped after SMV, whereas values for the other muscles remained unchanged. While healthy subjects require a low degree of force to reach a target, chronic stroke patients require a greater activation force owing to the impaired voluntary activity of
the arm. SMV applied over the BB may have resulted in an increased cortical representation of this muscle (Forner-Cordero, Steyvers, Levin, Alaerts, & Swinnen, 2008; Rosenkranz et al., 2003; Rosenkranz & Rothwell, 2003), which in turn led to its activation being facilitated. Likewise, the other muscle that was vibrated in our experiment, i.e. the FCU, exhibited a reduction in the %MVC following SMV, which did not however reach significance. The preliminary results that emerge from our study indicate that the BB/TB, AD/BB and PD/BB muscle pairs reduce their co-contraction levels following SMV. The function of antagonist muscles, such as the BB and TB, should not be coupled during a fluid movement. From this point of view, the reduction in their CCI might facilitate performance of the movement. The same applies to the AD and BB, both of which are shoulder flexor muscles; however, their respective activations occur in different moments of reaching, with BB being activated first. As regards the pair PD/BB, we presume, according to our CCI calculation method designed to investigate the minimal activity of the muscle pairs during reaching, that the reduction in the CCI indicates that the minimal contraction values in both muscles were reduced, particularly in those phases of the movement in
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
which their activation was not required. Numerous transcranial magnetic stimulation studies (Forner-Cordero et al., 2008; Rosenkranz et al., 2003; Rosenkranz & Rothwell, 2003; Siggelkow et al., 1999) have demonstrated that SMV exerts its effects at the central nervous system level, modifying patterns of intra-cortical inhibition and facilitation and increasing representation, as well as motor output, of a vibrated muscle. Reports of increased smoothness and enhanced performances of reaching movements (Tavernese et al., 2013), as well as of improved walking ability (Paoloni et al., 2010), in chronic stroke patients following SMV, may reflect the clinical effects corresponding to these central plastic changes. The poor reaching movement performances in stroke patients may be the result of impaired coordination between the shoulder flexor and elbow extensor muscles (McCrea, Eng, & Hodgson, 2005). When Kisiel-Sajewicz et al. (2011) found reduced functional coupling between the AD and TB, i.e. the two synergists, during a reaching movement in 11 stroke patients, they speculated that this might be due to a loss of common drive following an interruption in the information flow in the cortico-spinal pathway. Although we did not estimate either motor output or neural common drive, we may hypothesize that the vibratory stimulus improved the cortical organization and execution of the motor task through remodeling. This would also explain the finding in a previous study (Tavernese et al., 2013) of an increase in mean linear velocity, which is a parameter of extrinsic workspace because it is controlled above all by the Cartesian coordinate system in which the movement is actuated (Moran & Schwartz, 1999), as well as an increase in shoulder angular velocity, which is a parameter of intrinsic space because it is measured relative to adjacent arm/body segments (Reina, Moran, & Schwartz, 2001), after SMV. It is noteworthy that we observed changes in EMG activity 4 weeks after SMV therapy ended. This not only lends further support to the hypothesis that vibration therapy acts through plastic changes that are determined at the central nervous system level, but also suggests that long-lasting results may be achieved by means of longer stimulation periods (Marconi et al., 2011).
5. Study limitations The main limitation of the present pilot study was the small sample size. Moreover, the study was not doubleblinded. However, the use of an instrumented measure for outcomes evaluation and of an independent assessor
413
blinded to the group assignment partially limited this bias. 6. Conclusions Results from this pilot study show that the application of SMV modulates EMG activity in chronic stoke patients performing a reaching movement. This is probably due to the plastic remodeling action that vibratory stimuli exert at the central nervous system level. This finding highlights the potential use of SMV for motor impairment rehabilitation purposes in stroke patients, but needs to be confirmed by larger, controlled, prospective trials of SMV in motor rehabilitation following stroke. Declaration of interest All the authors are able to declare that there are no relationships of a financial nature, or other issues, that might lead to a conflict of interests. Funding This research received no specific grant from any funding agency in the public, commercial, or not-forprofit sectors. References Bohannon, R.W., & Smith, M.B. (1987). Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther, 67(2), 206-207. Bourbonnais, D., & Vanden Noven, S. (1989). Weakness in patients with hemiparesis. Am J Occup Ther, 43(5), 313-319. Brown, M.C., Engberg, I., & Matthews, P.B. (1967). The relative sensitivity to vibration of muscle receptors of the cat. J Physiol, 192(3), 773-800. Canning, C.G., Ada, L., & O’Dwyer, N. (1999). Slowness to develop force contributes to weakness after stroke. Arch Phys Med Rehabil, 80(1), 66-70. Chae, J., Yang, G., Park, B.K., & Labatia, I. (2002). Muscle weakness and cocontraction in upper limb hemiparesis: Relationship to motor impairment and physical disability. Neurorehabil Neural Repair, 16(3), 241-248. Forner-Cordero, A., Steyvers, M., Levin, O., Alaerts, K., & Swinnen, S.P. (2008). Changes in corticomotor excitability following prolonged muscle tendon vibration. Behav Brain Res, 190(1), 41-49. doi: 10.1016/j.bbr.2008.02.019 Frost, G., Dowling, J., Dyson, K., & Bar-Or, O. (1997). Cocontraction in three age groups of children during treadmill locomotion. J Electromyogr Kinesiol, 7(3), 179-186.
414
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
Gemperline, J.J., Allen, S., Walk, D., & Rymer, W.Z. (1995). Characteristics of motor unit discharge in subjects with hemiparesis. Muscle Nerve, 18(10), 1101-1114. doi: 10.1002/mus.880181006 Georgopoulos, A.P. (1986). On reaching. Annu Rev Neurosci, 9, 147170. doi: 10.1146/annurev.ne.09.030186.001051 Gladstone, D.J., Danells, C.J., & Black, S.E. (2002). The fugl-meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil Neural Repair, 16(3), 232-240. Hara, Y., Masakado, Y., & Chino, N. (2004). The physiological functional loss of single thenar motor units in the stroke patients: When does it occur? Does it progress? Clin Neurophysiol, 115(1), 97-103. Hu, X., Tong, K.Y., Song, R., Tsang, V.S., Leung, P.O., & Li, L. (2007). Variation of muscle coactivation patterns in chronic stroke during robot-assisted elbow training. Arch Phys Med Rehabil, 88(8), 1022-1029. doi: 10.1016/j.apmr.2007.05.006 Kisiel-Sajewicz, K., Fang, Y., Hrovat, K., Yue, G.H., Siemionow, V., Sun, C.K., Daly, J.J., et al. (2011). Weakening of synergist muscle coupling during reaching movement in stroke patients. Neurorehabil Neural Repair, 25(4), 359-368. doi: 10.1177/1545968310388665 Lang, C.E., & Bastian, A.J. (1999). Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol, 82(5), 2108-2119. Levin, M.F. (1996). It Interjoint coordination during pointing movements is disrupted in spastic hemiparesis. Brain, 119(Pt 1), 281-293. Marconi, B., Filippi, G.M., Koch, G., Giacobbe, V., Pecchioli, C., Versace, V., Caltagirone, C., et al. (2011). Long-term effects on cortical excitability and motor recovery induced by repeated muscle vibration in chronic stroke patients. Neurorehabil Neural Repair, 25(1), 48-60. doi: 10.1177/1545968310376757 McCrea, P.H., Eng, J.J., & Hodgson, A.J. (2005). Saturated muscle activation contributes to compensatory reaching strategies after stroke. J Neurophysiol, 94(5), 2999-3008. doi: 10.1152/jn.00732.2004 Moran, D.W., & Schwartz, A.B. (1999). Motor cortical representation of speed and direction during reaching. J Neurophysiol, 82(5), 2676-2692. Murillo, N., Kumru, H., Vidal-Samso, J., Benito, J., Medina, J., Navarro, X., & Valls-Sole, J. (2011). Decrease of spasticity with muscle vibration in patients with spinal cord injury. Clin Neurophysiol, 122(6), 1183-1189. doi: 10.1016/j.clinph.2010.11.012 Noma, T., Matsumoto, S., Etoh, S., Shimodozono, M., & Kawahira, K. (2009). Anti-spastic effects of the direct application of vibratory stimuli to the spastic muscles of hemiplegic limbs in post-stroke patients. Brain Inj, 23(7), 623-631. doi: 10.1080/02699050902997896 Noma, T., Matsumoto, S., Shimodozono, M., Etoh, S., & Kawahira, K. (2012). Anti-spastic effects of the direct application of vibratory stimuli to the spastic muscles of hemiplegic limbs in post-stroke patients: A proof-of-principle study. J Rehabil Med, 44(4), 325-330. doi: 10.2340/16501977-0946
Paoloni, M., Giovannelli, M., Mangone, M., Leonardi, L., Tavernese, E., Di Pangrazio, E., Pozzilli, C., et al. (2013). Does giving segmental muscle vibration alter the response to botulinum toxin injections in the treatment of spasticity in people with multiple sclerosis? A single-blind randomized controlled trial. Clin Rehabil, 27(9), 803-812. doi: 10.1177/0269215513480956 Paoloni, M., Mangone, M., Scettri, P., Procaccianti, R., Cometa, A., & Santilli, V. (2010). Segmental muscle vibration improves walking in chronic stroke patients with foot drop: A randomized controlled trial. Neurorehabil Neural Repair, 24(3), 254-262. doi: 10.1177/1545968309349940 Reina, G.A., Moran, D.W., & Schwartz, A.B. (2001). On the relationship between joint angular velocity and motor cortical discharge during reaching. J Neurophysiol, 85(6), 2576-2589. Roll, J.P., Vedel, J.P., & Ribot, E. (1989). Alteration of proprioceptive messages induced by tendon vibration in man: A microneurographic study. Exp Brain Res, 76(1), 213-222. Rosenkranz, K., Pesenti, A., Paulus, W., & Tergau, F. (2003). Focal reduction of intracortical inhibition in the motor cortex by selective proprioceptive stimulation. Exp Brain Res, 149(1), 9-16. doi: 10.1007/s00221-002-1330-3 Rosenkranz, K., & Rothwell, J.C. (2003). Differential effect of muscle vibration on intracortical inhibitory circuits in humans. J Physiol, 551(Pt 2), 649-660. doi: 10.1113/jphysiol.2003.043752 Siggelkow, S., Kossev, A., Schubert, M., Kappels, H.H., Wolf, W., & Dengler, R. (1999). Modulation of motor evoked potentials by muscle vibration: The role of vibration frequency. Muscle Nerve, 22(11), 1544-1548. Steyvers, M., Levin, O., Van Baelen, M., & Swinnen, S.P. (2003). Corticospinal excitability changes following prolonged muscle tendon vibration. Neuroreport, 14(15), 1901-1905. doi: 10.1097/01.wnr.0000093296.63079.fa Tavernese, E., Paoloni, M., Mangone, M., Mandic, V., Sale, P., Franceschini, M., & Santilli, V. (2013). Segmental muscle vibration improves reaching movement in patients with chronic stroke. A randomized controlled trial. NeuroRehabilitation, 32(3), 591599. doi: 10.3233/NRE-130881 Wagner, J.M., Dromerick, A.W., Sahrmann, S.A., & Lang, C.E. (2007). Upper extremity muscle activation during recovery of reaching in subjects with post-stroke hemiparesis. Clin Neurophysiol, 118(1), 164-176. doi: 10.1016/j.clinph.2006.09.022 Wu, C., Trombly, C.A., Lin, K., & Tickle-Degnen, L. (2000). A kinematic study of contextual effects on reaching performance in persons with and without stroke: Influences of object availability. Arch Phys Med Rehabil, 81(1), 95-101.
Copyright of NeuroRehabilitation is the property of IOS Press and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
NeuroRehabilitation 35 (2014) 405–414 DOI:10.3233/NRE-141131 IOS Press
Segmental muscle vibration modifies muscle activation during reaching in chronic stroke: A pilot study Marco Paolonia,∗ , Emanuela Taverneseb , Massimo Finic , Patrizio Salec , Marco Franceschinic , Valter Santillia and Massimiliano Mangonea a Department
of Physical Medicine and Rehabilitation, Sapienza – University of Rome, Rome, Italy Neuro-Rehabilitation Division, Bambino Gesu` Children’s Hospital, IRCCS, Rome, Italy c IRCSS San Raffaele Pisana, Rome, Italy b Pediatric
Abstract. BACKGROUND: Segmental muscle vibration (SMV) improves motor performances in neurological conditions, including stroke. OBJECTIVE: To determine if SMV modifies upper limb muscular activity in chronic stroke patients performing a reaching movement. METHODS: We randomized 22 chronic stroke patients to an experimental group (EG; n = 12), receiving 10 sessions of exercise + 120 Hz SMV over the biceps brachii (BB) and the flexor carpi ulnaris (FCU) muscles, or to a control group (CG; n = 10) receiving exercise only. All subjects performed a reaching movement with the affected side before and 4 weeks after therapy ended. We recorded surface EMG activity of the anterior deltoid (AD), posterior deltoid (PD), BB, triceps brachii (TB), FCU and extensor carpi radialis (ECR) muscles. We calculated muscular onset times, modulation ratio, co-contractions and degree of contraction. RESULTS: After SMV, onset times of the PD (p = 0.03), BB (p = 0.02) and ECR (p = 0.04) in the EG were less anticipated than at baseline; the modulation ratio increased in AD (p = 0.003) and BB (p = 0.01); co-contractions decreased in the pairs BB/TB (p = 0.007), PD/BB (p = 0.004) and AD/BB (p = 0.01); and the degree of contraction decreased in BB (p = 0.01). CONCLUSIONS: The modulation of muscular function induced by SMV may aid to explain its action on smoothness and coordination of movements. Keywords: Stroke, rehabilitation, electromyography, reaching movement, vibration therapy
1. Introduction Motor disability following a stroke is often due to poor arm function. Indeed, chronic stroke sufferers may lose their ability to perform motor functions as a result of reduced neural drive from the cortex to motor units (Hara, Masakado, & Chino, 2004) and to a de∗ Address for correspondence: Marco Paoloni, Department of Physical Medicine and Rehabilitation, “Sapienza” – University of Rome, Piazzale Aldo Moro, 5 00185 Rome, Italy. Tel.: +39 6 49975924; E-mail: [email protected].
synchronized firing rate of motor units (Gemperline, Allen, Walk, & Rymer, 1995). This ultimately leads to muscle weakness (Bourbonnais & Vanden Noven, 1989; Chae, Yang, Park, & Labatia, 2002), slowness of movement (Canning, Ada, & O’Dwyer, 1999) and uncoordinated muscular contractions during the performance of a given motor task (Levin, 1996). One of the most important actions performed by the upper limb, which allows the hand to interact with the environment, is reaching (Wu, Trombly, Lin, & TickleDegnen, 2000), a complex multi-joint movement to a
1053-8135/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
406
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
defined point in space (Georgopoulos, 1986). Acute and sub-acute stroke patients are subject to various alterations in the electromyographic (EMG) activities of the upper limb muscles when they perform the reaching movement, including altered muscle onset times, a reduced ability to modulate EMG activity at the beginning of the movement and an increased degree of muscular contraction (Wagner, Dromerick, Sahrmann, & Lang, 2007). Mechanical stimuli, delivered as segmental muscle vibration (SMV), have been successfully used in some neurological conditions, such as chronic stroke (Noma, Matsumoto, Etoh, Shimodozono, & Kawahira, 2009; Noma, Matsumoto, Shimodozono, Etoh, & Kawahira, 2012), multiple sclerosis (Paoloni et al., 2013) and spinal cord injury (Murillo et al., 2011), to improve several features of motor performance. Acting on muscle spindle primary endings (Roll, Vedel, & Ribot, 1989), SMV induces the generation of Ia inputs, which can alter the excitability of the corticospinal pathway (Steyvers, Levin, Van Baelen, & Swinnen, 2003) by modulating intracortical inhibiting and facilitating inputs to the primary motor cortex (Rosenkranz, Pesenti, Paulus, & Tergau, 2003; Rosenkranz & Rothwell, 2003). Recently, SMV, added to general physical therapy, has been shown to improve reaching performances in chronic stroke patients (Tavernese et al., 2013). One intriguing hypothesis is that these motor improvements may be accompanied, or even determined, by changes in muscle activation characteristics during movement. To test this hypothesis, we designed a pilot randomized controlled trial to verify whether SMV in chronic stroke patients performing a reaching movement induces any changes in surface EMG activities of the shoulder, arm and forearm muscles.
2. Materials and methods 2.1. Subjects We considered eligible for the present research hemiparetic patients (right or left hemiparesis of at least 6 months’ duration secondary to ischemic stroke) of both sexes, aged between 40 and 85 years, without any other neurological conditions (e.g. multiple sclerosis, Parkinson’s disease, bilateral brain lesions, ischemic involvement of the cerebellum or basal ganglia or cognitive impairment). Further exclusion criteria were: injections performed to treat spasticity 6 months prior to participation in the study, or rheumatic and orthopedic conditions that may interfere with upper limb
movements. The study protocol was approved by the local ethics committee. The experimental protocol was explained to the participants, all of whom gave their informed consent prior to participation. Participants who fulfilled the inclusion/exclusion criteria were randomly assigned to either the experimental group (EG) or control group (CG) by an independent person who selected a sealed envelope 30 minutes before the intervention was due to start. 2.2. Clinical and instrumental evaluation All the participants underwent a clinical and an instrumental evaluation before the training started (baseline), and an instrumental evaluation 1 month after therapy ended (Fig. 1). To obtain normative data for the variables analyzed, we also recruited ten age-matched healthy subjects (5 males; mean age 60.0 ± 4.9 years; range 50–65), with no neurological and/or orthopedic impairments. Healthy subjects only performed one kinematic evaluation, according to the same modalities as those used for the EG and CG patients. At baseline, we collected all the patients’ demographic and clinical characteristics by means of an interview and a clinical evaluation. We focused, in particular, on: recovery of motor function by determining the patients’ Brunnstrom’s stage; movements, coordination and reflexes of the upper limb as measured by means of the Fugl-Meyer assessment scale of the upper extremity (Gladstone, Danells, & Black, 2002); spasticity at the shoulder, elbow and wrist as assessed by means of the Modified Ashworth (Bohannon & Smith, 1987). The motor task we analyzed consisted of a single reaching movement of the affected limb. The subjects sat on a chair whose height could be adjusted, with the feet resting on the floor and the knees and hips bent at 90◦ . With their hand placed on their thigh, they were asked to move their hand toward the target marker as rapidly and as accurately as possible, without moving their backs away from the backrest. After a warm-up and familiarizing session in which the subjects cyclically performed a series of reaching movements, we acquired five trials and we considered for the data analysis the mean values of the EMG measurements. After the reaching trial data had been collected, we performed an additional EMG recording for each muscle during maximal voluntary isometric contraction (MVC). The kinematic analysis was performed by means of an optoelectronic stereophotogrammetric system (ELITE, BTS, Milan, Italy), with a sampling rate of 100 Hz, to capture the movement of a retro-reflective marker
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
407
Fig. 1. Flow-chart diagram of the study. SMV: segmental muscle vibration.
placed over the base of 2nd metacarpal joint on the analyzed side. We placed a target marker in front of the subject, at shoulder height, at a distance that slightly exceeded the sum of the lengths of the arm and forearm. Given the distance between the hand marker and the target marker, we used the 3-point differentiation method to calculate the mean linear velocity. The mean linear velocity was filtered using a low-pass, secondorder Butterworth filter (cut-off frequency, 5 Hz), and used to determine the start (defined as the instant in which the velocity exceeded 5% of the maximum velocity recorded during the task) and the end (defined as the instant in which the velocity dropped to zero) of the movement. We acquired surface myoelectric signals with a sampling rate of 1000 Hz using a 16-channel telemetric transmission surface electromyography (pocket EMG System; BTS, Milan, Italy). The lower and upper cut-off frequencies of the Hamming filter were 10 and
400 Hz, respectively, whereas the common mode reaction ratio was 100 dB. To record surface EMG we used a pair of Ag/AgCl electrodes, with an inter-electrode space of 2 cm, placed on the skin overlying the muscle belly of the posterior deltoid (PD), anterior deltoid (AD), biceps brachii (BB), triceps brachii (TB), flexor carpi ulnaris (FCU) and extensor carpi radialis (ECR). We rectified, low-pass filtered with an upper cut-off frequency of 5 Hz, and integrated using a mobile window of 125 ms the raw signal, to obtain the envelope. 2.3. Interventions All the participants underwent a 60-minute general physical therapy session, 5 times per week, over a period of 2 weeks. These sessions comprised stretching, muscle strengthening and specific training for reaching and reaching-to-grasp movements. Participants in the EG
408
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
also received 30 minutes of low-amplitude SMV at a fixed frequency of 120 Hz over the target muscles, i.e. the BB and the FCU on the affected side, by means of a commercial device (Horus, Akropolis, Rome, Italy). We set the vibration amplitude at 10 m to drive Ia spindle afferents (Brown, Engberg, & Matthews, 1967) and we delivered the 30-minute stimulation session in trains of 6" divided by 1" pauses (Tavernese et al., 2013), at the end of each general physical therapy session with the patient lying supine. We assessed, the occurrence of muscle pain or skin lesions in patients in the EG at the end of each session.
was demonstrated by MR > 1 (higher values represent greater muscle activation), while a MR = 1 means no modulation. We computed the %MCV as the ratio between the peak envelope value during reaching and the peak envelope value during the MVC trial (Wagner et al., 2007). All EMG data were analyzed off-line by means of a dedicated software (SMART Analyzer, BTS, Milan, Italy) by an assessor who was blinded to the randomization.
2.4. Outcome measures
To perform the statistical analysis we used the MedCalc® 12.2.1.0 (MedCalc Software). Following randomization, we verified normal distribution of all the variables analyzed in both groups by means of a D’Agostino-Pearson test, and we applied parametric or non-parametric tests, as appropriate, to compare means. We used the unpaired t-test or Mann-Whitney test to compare the pre- and post-treatment data in EG and CG and the paired t-test or the Wilcoxon matched pairs test to assess differences between pre- and post-treatment values in the two groups. We set the level of significance at p < 0.05 for all the analyses and we applied a Bonferroni correction to reduce type I error in interpreting the data. We conducted all the analyses according to the intention-to-treat principle.
As outcome measures we assessed the following: muscle onset time, co-contraction index (CCI), modulation ratio (MR) and percentage of activation in relation to the MVC (%MVC). We defined the muscle onset time as the time in which the enveloped EMG signal passed the baseline threshold (defined as the resting mean EMG value plus 2 standard deviation) for > 30 ms (Wagner et al., 2007), with the value 0 ms representing the start of the movement, with negative values representing muscle pre-activation before the movement starts and positive values representing muscle activation after the movement has started. We considered the CCI (Hu et al., 2007) for the following muscle pairs: the agonist/antagonist muscles of the shoulder, arm and forearm (AD/PD, BB/TB, FCU/ECR, respectively); the main synergistic muscles for the reaching movement (AD/TB), and their respective antagonists (PD/BB); the shoulder flexor muscles (AD/BB). We calculated the CCI according to the following formula (Frost, Dowling, Dyson, & Bar-Or, 1997): CCI =
start
end
Aij (t) dt
(1)
where Aij (t) is the overlapping activity of the EMG envelopes for muscles i and j, T is the length of the signal, and start and end represent, respectively, the start and the end of the reaching movement as defined above. Higher CCI values indicate greater co-contraction. The MR expresses the ability to properly increase muscle activation at the start of the reaching movement. We calculated MR as the ratio of integrated EMG activity during the first 100 ms of contraction and the resting mean value (Lang & Bastian, 1999). Modulation
2.5. Statistical analysis
3. Results We considered eligible for the study thirty-five patients, randomly selected from among those referring to our outpatient service between October 2012 and June 2013, and we randomized to either the EG (n = 12) or CG (n = 10) those patients who satisfied the inclusion criteria (Fig. 1). The demographic and clinical baseline characteristics of the two groups were well balanced (Table 1). We did not observe adverse events in either the EG or CG, and all the patients completed the treatment and performed the post-treatment assessment. Muscle onset times are shown in Fig. 2. We observed no differences at baseline between patients in the EG and those in the CG in any of the onset times considered. We found significant differences between pre- and post-treatment in the EG as regards the PD (total of ranks = 6.00; p = 0.03), BB (t = 2.75; p = 0.02) and ECR (t = 2.35; p = 0.04) muscle onset times. We found the muscle onset time to be closer to zero following treatment in all the cases (Fig. 2). We could not find
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
409
Table 1 Demographic and clinical characteristics of patients in both groups at baseline Experimental Group (n = 12) Age (years)1 Gender (Males/Females) Time since acute event (months) 1 Right/left hemiplegia (n) Upper extremity Brunnstrom stage2 Fugl-Meyer Scale (upper extremity) 2 Modified Ashworth Scale2 Shoulder Elbow Wrist 1 Data
Control Group (n = 10)
p
60.3 ± 15.3 7/5 15.5 ± 14.9 4/8 5.5 (5.0 – 6.0) 48/66 (44.25 – 54.5)
60.7 ± 13.2 6/4 13.0 ± 5.0 4/6 5.0 (5.0 – 6.0) 49/66 (44.75 – 55.75)
n.s. n.s. n.s. n.s. n.s. n.s.
1.0 (1.0 – 2.0) 1.0 (0.0 – 2.0) 1.0 (0.0 – 1.0)
1.0 (1.0 – 2.0) 1.0 (1.0 – 2.0) 1.0 (0.0 – 1.125)
n.s. n.s. n.s.
are expressed as means ± SD. 2 Median values (25th–75th interquartiles). n.s.: not significant.
differences between pre- and post-treatment in the CG in any of the muscle onset times. We found the posttreatment PD muscle onset time significantly closer to zero in the EG than in the CG (t = 3.11; p = 0.005), whereas we did not observe any differences for the other variables analyzed. The results of the CCI are shown in Table 2. We did not detect any differences at baseline between the EG and CG in any of the values investigated. We found patients in the EG to have a significantly lower CCI in the post-treatment assessment than at baseline for the pairs BB/TB (t = 3.31; p = 0.007), PD/BB (t = 3.60; p = 0.004) and AD/BB (t = 3.066; p = 0.01). No other significant changes emerged between the pre- and posttreatment CCI values. We did not find any differences in the CCI between pre- and post-treatment in the CG, except for AD/PD (t = 2.92; p = 0.02), which was lower in the post-treatment evaluation. When post-treatment values between groups were compared, we found the CCI to be significantly lower in the EG for PD/BB (t = 2.21; p = 0.04) and AD/BB (t = 2.29; p = 0.04). Table 3 shows the results of MR. No significant differences emerged between groups at baseline. At the post-treatment assessment, patients in the EG modulated the AD (t = 3.782; p = 0.003) and BB (t = 3.044; p = 0.01) significantly better than at baseline. We found no differences between the pre- and post-treatment evaluation in the CG. Patients in the EG modulated the AD (t = 3.235; p = 0.004) and BB (t = 2.923; p = 0.01) significantly better than those in the CG at the posttreatment evaluation. As regards the %MCV, we did not find any significant difference at baseline between groups. In the EG we only pointed out a significant difference only for the BB, whose %MCV value was lower at the post-treatment evaluation than at the baseline (t = 2.995; p = 0.01). We found no differences between baseline and post-treatment values in the CG. The
between-groups comparison at the post-treatment evaluation revealed a significantly lower %MCV value for the BB in the EG than in the CG (t = 2.467; p = 0.03). No differences emerged in any of the other variables analyzed (Table 4).
4. Discussion In the present pilot study, we performed an EMG analysis of reaching in chronic stroke patients to assess the short-term effects of 10 applications of SMV on upper limb muscle activity. We studied various aspects of dynamic muscular function so as to determine the timing of muscular activation, its modulation and the degree of muscular contraction during movement. Our findings demonstrate that SMV modulates muscular activity during the execution of reaching movement. In particular, the target muscle responsible for the majority of the changes we observed is the BB, which modulates its activity most effectively in the milliseconds that immediately follow the movement onset, generally requires less force and induces a lower degree of co-contraction with the others arm muscles following vibration therapy. All the patients recruited in our study demonstrated, at each follow-up, a pre-activation of all the muscles examined, which means that the onset of activation always occurred before the start of reaching movement (considered as time zero). Wagner and colleagues (2007) found that the onset of pre-activation in acute and sub-acute stroke patients is delayed, sometimes even occurring after the movement starts, which is contrast to what is observed in healthy subjects. In our study, the pre-activation pattern in healthy controls was similar to that found by Wagner and colleagues (2007), and differs from the pattern observed in patients. In the pre-treatment sessions, all the patients displayed an
410
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
Fig. 2. Baseline (a) and post-treatment (b) group mean muscle onset times during reaching for the examined muscles for the experimental group (black triangles) and the control group (black circles), compared with healthy subjects (c, black squares). Numeric values are mean ± standard deviation muscle onset times (ms) for each muscle. Error bars represent standard deviations.
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
411
Table 2 Mean ± standard deviations (95% CI) of co-contraction index values for the examined muscle pairs. Significant values are in bold AD/PD Baseline Post-treatment p Value2 BB/TB Baseline Post-treatment p Value2 FCU/ECR Baseline Post-treatment p Value2 AD/TB Baseline Post-treatment p Value2 PD/BB Baseline Post-treatment p Value2 AD/BB Baseline Post-treatment p Value2
Experimental Group
Control Group
p Value1
Healthy subjects
0.20 ± 0.15 (0,11 to 0.30) 0.14 ± 0.14 (0.04 to 0.22) 0.17
0.25 ± 0.12 (0.16 to 0.34) 0.18 ± 0.08 (0.12 to 0.23) 0.02
0.46 0.42
0.02 ± 0.02 (0.01 to 0.04)
0.09 ± 0.05 (0.06 to 0.12) 0.07 ± 0.03 (0.05 to 0.09) 0.007
0.10 ± 0.04 (0.07 to 0.13) 0.11 ± 0.07 (0.06 to 0.16) 0.71
0.72 0.11
0.02 ± 0.01 (0.01 to 0.03)
0.10 ± 0.11 (0.03 to 0.17) 0.11 ± 0.07 (0.06 to 0.15) 0.34
0.09 ± 0.10 (0.02 to 0.16) 0.07 ± 0.05 (0.04 to 0.11) 0.55
0.79 0.26
0.02 ± 0.02 (0.01 to 0.04)
0.12 ± 0.07 (0.08 to 0.16) 0.12 ± 0.11 (0.05 to 0.19) 0.94
0.12 ± 0.05 (0.09 to 0.16) 0.14 ± 0.09 (0.07 to 0.20) 0.68
0.89 0.75
0.04 ± 0.02 (0.02 to 0.05)
0.09 ± 0.05 (0.06 to 0.12) 0.07 ± 0.05 (0.04 to 0.10) 0.004
0.12 ± 0.04 (0.09 to 0.14) 0.12 ± 0.07 (0.07 to 0.17) 0.90
0.14 0.04
0.02 ± 0.01 (0.01 to 0.02)
0.13 ± 0.06 (0.09 to 0.16) 0.10 ± 0.03 (0.08 to 0.12) 0.01
0.16 ± 0.06 (0.12 to 0.21) 0.16 ± 0.08 (0.10 to 0.22) 0.88
0.20 0.04
0.03 ± 0.01 (0.02 to 0.03)
AD: anterior deltoid; PD: posterior deltoid; BB: biceps brachii; TB: triceps brachii; FCU: flexor carpi ulnaris; ECR: extensor carpi radialis. 1 : within group comparison at each follow-up; 2 : between group comparison.
Table 3 Mean ± standard deviations (95% CI) of modulation ratio values. Significant values are in bold AD Baseline Post-treatment p Value2 PD Baseline Post-treatment p Value2 BB Baseline Post-treatment p Value2 TB Baseline Post-treatment p Value2 FCU Baseline Post-treatment p Value2 ECR Baseline Post-treatment p Value2
Experimental Group
Control Group
p Value1
Healthy subjects
1.98 ± 0.50 (1.67 to 2.30) 2.65 ± 0.68 (2.22 to 3.08) 0.003
1.98 ± 0.72 (1.47 to 2.49) 1.77 ± 0.56 (1.37 to 2.18) 0.32
0.99 0.004
3.18 ± 1.85 (1.67 to 4.32)
1.83 ± 0.31 (1.63 to 2.02) 1.82 ± 0.62 (1.42 to 2.21) 0.52
1.82 ± 0.32 (1.59 to 2.05) 1.81 ± 0.66 (1.34 to 2.29) 0.99
0.93 0.51
2.09 ± 1.00 (1.39 to 2.75)
1.61 ± 0.40 (1.35 to 1.86) 2.55 ± 1.23 (1.77 to 3.34) 0.01
1.48 ± 0.35 (1.23 to 1.73) 1.48 ± 0.30 (1.26 to 1.69) 0.96
0.44 0.01
3.39 ± 2.70 (1.85 to 4.75)
1.49 ± 0.21 (1.35 to 1.62) 1.46 ± 0.17 (1.35 to 1.57) 0.91
1.43 ± 0.25 (1.25 to 1.61) 1.46 ± 0.25 (1.28 to 1.63) 0.64
0.55 0.79
2.11 ± 1.05 (1.49 to 2.11)
1.56 ± 0.30 (1.37 to 1.75) 1.67 ± 0.67 (1.24 to 2.10) 0.91
1.42 ± 0.27 (1.22 to 1.61) 1.43 ± 0.32 (1.20 to 1.65) 0.84
0.35 0.51
1.72 ± 0.38 (1.47 to 1.95)
1.62 ± 0.32 (1.41 to 1.82) 1.68 ± 0.65 (1.27 to 2.10) 0.73
1.64 ± 0.47 (1.31 to 1.98) 1.61 ± 0.39 (1.33 to 1.89) 0.81
0.88 0.89
1.97 ± 0.72 (1.46 to 2.12)
AD: anterior deltoid; PD: posterior deltoid; BB: biceps brachii; TB: triceps brachii; FCU: flexor carpi ulnaris; ECR: extensor carpi radialis. 1 : within group comparison at each follow-up; 2 : between group comparison.
412
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke Table 4 Mean ± standard deviations (95% CI) of percentage of muscle activation with respect to isometric maximum voluntary contraction values. Significant values are in bold AD Baseline Post-treatment p Value2 PD Baseline Post-treatment p Value2 BB Baseline Post-treatment p Value2 TB Baseline Post-treatment p Value2 FCU Baseline Post-treatment p Value2 ECR Baseline Post-treatment p Value2
Experimental Group
Control Group
p Value1
66.0 ± 19.9 (53.4 to 78.7) 73.5 ± 24.9 (57.7 to 89.4) 0.50
78.1 ± 11.8 (69.6 to 86.5) 72.9 ± 22.9 (56.4 to 89.3) 0.50
0.11 0.95
25.1 ± 23.6 (10.1 to 40.1) 23.2 ± 27.4 (5.8 to 40.6) 0.73
33.1 ± 31.8 (10.4 to 55.9) 47.0 ± 32.6 (23.6 to 70.3) 0.30
0.50 0.08
3.4 ± 2.4 (1.7 to 4.8)
22.2 ± 9.4 (16.2 to 28.2) 17.2 ± 7.0 (12.7 to 21.7) 0.01
29.8 ± 13.7 (20.0 to 39.6) 31.8 ± 17.5 (19.2 to 44.3) 0.75
0.14 0.03
4.7 ± 2.6 (2.3 to 7.6)
27.3 ± 12.9 (19.1 to 35.5) 21.6 ± 19.0 (9.5 to 33.7) 0.08
29.1 ± 12.2 (20.4 to 37.9) 32.7 ± 22.5 (16.6 to 48.8) 0.53
0.73 0.22
8.4 ± 4.8 (4.4 to 13.7)
31.3 ± 33.4 (10.1 to 52.5) 19.9 ± 11.8 (12.4 to 27.4) 0.13
30.7 ± 29.3 (9.7 to 51.6) 22.9 ± 23.1(6.4 to 39.5) 0.13
0.96 0.71
7.6 ± 7.5 (1.2 to 15.9)
29.2 ± 11.5 (21.8 to 36.5) 26.8 ± 11.6 (19.4 to 34.2) 0.23
27.7 ± 15.2 (16.8 to 38.5) 21.3 ± 15.9 (9.9 to 32.7) 0.12
0.79 0.88
10.0 ± 5.3 (6.0 to 15.4)
Healthy subjects 50.4 ± 27.5 (34.0 to 76.7)
AD: anterior deltoid; PD: posterior deltoid; BB: biceps brachii; TB: triceps brachii; FCU: flexor carpi ulnaris; ECR: extensor carpi radialis. 1 : within group comparison at each follow-up, 2 : between group comparison.
overly anticipated pre-activation of the PD, BB, FCU and ECR, and a delayed pre-activation of the TB. The changes observed following SMV in the EG demonstrate a trend to normalization for the BB, PD and ECR onset times, which displayed a significantly less anticipated pre-activation (Fig. 2). According to our results, SMV influences the MR, an index used to calculate a person’s ability to rapidly activate muscles. In particular, we observed an increased MR for the AD and BB muscles following SMV. In our healthy subjects, the AD and BB, the prime reaching effectors, are the muscles displaying the greatest degree of modulation, thereby confirming data in the literature (Wagner et al., 2007). We may therefore interpret the increase in the MR following SMV as an improvement in muscular function, particularly with regard to a person’s ability to produce movement when required. We calculated the %MVC to quantify the degree of muscular contraction used to perform the movement. According to our results, the %MVC for the BB in patients in our EG dropped after SMV, whereas values for the other muscles remained unchanged. While healthy subjects require a low degree of force to reach a target, chronic stroke patients require a greater activation force owing to the impaired voluntary activity of
the arm. SMV applied over the BB may have resulted in an increased cortical representation of this muscle (Forner-Cordero, Steyvers, Levin, Alaerts, & Swinnen, 2008; Rosenkranz et al., 2003; Rosenkranz & Rothwell, 2003), which in turn led to its activation being facilitated. Likewise, the other muscle that was vibrated in our experiment, i.e. the FCU, exhibited a reduction in the %MVC following SMV, which did not however reach significance. The preliminary results that emerge from our study indicate that the BB/TB, AD/BB and PD/BB muscle pairs reduce their co-contraction levels following SMV. The function of antagonist muscles, such as the BB and TB, should not be coupled during a fluid movement. From this point of view, the reduction in their CCI might facilitate performance of the movement. The same applies to the AD and BB, both of which are shoulder flexor muscles; however, their respective activations occur in different moments of reaching, with BB being activated first. As regards the pair PD/BB, we presume, according to our CCI calculation method designed to investigate the minimal activity of the muscle pairs during reaching, that the reduction in the CCI indicates that the minimal contraction values in both muscles were reduced, particularly in those phases of the movement in
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
which their activation was not required. Numerous transcranial magnetic stimulation studies (Forner-Cordero et al., 2008; Rosenkranz et al., 2003; Rosenkranz & Rothwell, 2003; Siggelkow et al., 1999) have demonstrated that SMV exerts its effects at the central nervous system level, modifying patterns of intra-cortical inhibition and facilitation and increasing representation, as well as motor output, of a vibrated muscle. Reports of increased smoothness and enhanced performances of reaching movements (Tavernese et al., 2013), as well as of improved walking ability (Paoloni et al., 2010), in chronic stroke patients following SMV, may reflect the clinical effects corresponding to these central plastic changes. The poor reaching movement performances in stroke patients may be the result of impaired coordination between the shoulder flexor and elbow extensor muscles (McCrea, Eng, & Hodgson, 2005). When Kisiel-Sajewicz et al. (2011) found reduced functional coupling between the AD and TB, i.e. the two synergists, during a reaching movement in 11 stroke patients, they speculated that this might be due to a loss of common drive following an interruption in the information flow in the cortico-spinal pathway. Although we did not estimate either motor output or neural common drive, we may hypothesize that the vibratory stimulus improved the cortical organization and execution of the motor task through remodeling. This would also explain the finding in a previous study (Tavernese et al., 2013) of an increase in mean linear velocity, which is a parameter of extrinsic workspace because it is controlled above all by the Cartesian coordinate system in which the movement is actuated (Moran & Schwartz, 1999), as well as an increase in shoulder angular velocity, which is a parameter of intrinsic space because it is measured relative to adjacent arm/body segments (Reina, Moran, & Schwartz, 2001), after SMV. It is noteworthy that we observed changes in EMG activity 4 weeks after SMV therapy ended. This not only lends further support to the hypothesis that vibration therapy acts through plastic changes that are determined at the central nervous system level, but also suggests that long-lasting results may be achieved by means of longer stimulation periods (Marconi et al., 2011).
5. Study limitations The main limitation of the present pilot study was the small sample size. Moreover, the study was not doubleblinded. However, the use of an instrumented measure for outcomes evaluation and of an independent assessor
413
blinded to the group assignment partially limited this bias. 6. Conclusions Results from this pilot study show that the application of SMV modulates EMG activity in chronic stoke patients performing a reaching movement. This is probably due to the plastic remodeling action that vibratory stimuli exert at the central nervous system level. This finding highlights the potential use of SMV for motor impairment rehabilitation purposes in stroke patients, but needs to be confirmed by larger, controlled, prospective trials of SMV in motor rehabilitation following stroke. Declaration of interest All the authors are able to declare that there are no relationships of a financial nature, or other issues, that might lead to a conflict of interests. Funding This research received no specific grant from any funding agency in the public, commercial, or not-forprofit sectors. References Bohannon, R.W., & Smith, M.B. (1987). Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther, 67(2), 206-207. Bourbonnais, D., & Vanden Noven, S. (1989). Weakness in patients with hemiparesis. Am J Occup Ther, 43(5), 313-319. Brown, M.C., Engberg, I., & Matthews, P.B. (1967). The relative sensitivity to vibration of muscle receptors of the cat. J Physiol, 192(3), 773-800. Canning, C.G., Ada, L., & O’Dwyer, N. (1999). Slowness to develop force contributes to weakness after stroke. Arch Phys Med Rehabil, 80(1), 66-70. Chae, J., Yang, G., Park, B.K., & Labatia, I. (2002). Muscle weakness and cocontraction in upper limb hemiparesis: Relationship to motor impairment and physical disability. Neurorehabil Neural Repair, 16(3), 241-248. Forner-Cordero, A., Steyvers, M., Levin, O., Alaerts, K., & Swinnen, S.P. (2008). Changes in corticomotor excitability following prolonged muscle tendon vibration. Behav Brain Res, 190(1), 41-49. doi: 10.1016/j.bbr.2008.02.019 Frost, G., Dowling, J., Dyson, K., & Bar-Or, O. (1997). Cocontraction in three age groups of children during treadmill locomotion. J Electromyogr Kinesiol, 7(3), 179-186.
414
M. Paoloni et al. / SMV modifies muscle activation during reaching in chronic stroke
Gemperline, J.J., Allen, S., Walk, D., & Rymer, W.Z. (1995). Characteristics of motor unit discharge in subjects with hemiparesis. Muscle Nerve, 18(10), 1101-1114. doi: 10.1002/mus.880181006 Georgopoulos, A.P. (1986). On reaching. Annu Rev Neurosci, 9, 147170. doi: 10.1146/annurev.ne.09.030186.001051 Gladstone, D.J., Danells, C.J., & Black, S.E. (2002). The fugl-meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil Neural Repair, 16(3), 232-240. Hara, Y., Masakado, Y., & Chino, N. (2004). The physiological functional loss of single thenar motor units in the stroke patients: When does it occur? Does it progress? Clin Neurophysiol, 115(1), 97-103. Hu, X., Tong, K.Y., Song, R., Tsang, V.S., Leung, P.O., & Li, L. (2007). Variation of muscle coactivation patterns in chronic stroke during robot-assisted elbow training. Arch Phys Med Rehabil, 88(8), 1022-1029. doi: 10.1016/j.apmr.2007.05.006 Kisiel-Sajewicz, K., Fang, Y., Hrovat, K., Yue, G.H., Siemionow, V., Sun, C.K., Daly, J.J., et al. (2011). Weakening of synergist muscle coupling during reaching movement in stroke patients. Neurorehabil Neural Repair, 25(4), 359-368. doi: 10.1177/1545968310388665 Lang, C.E., & Bastian, A.J. (1999). Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol, 82(5), 2108-2119. Levin, M.F. (1996). It Interjoint coordination during pointing movements is disrupted in spastic hemiparesis. Brain, 119(Pt 1), 281-293. Marconi, B., Filippi, G.M., Koch, G., Giacobbe, V., Pecchioli, C., Versace, V., Caltagirone, C., et al. (2011). Long-term effects on cortical excitability and motor recovery induced by repeated muscle vibration in chronic stroke patients. Neurorehabil Neural Repair, 25(1), 48-60. doi: 10.1177/1545968310376757 McCrea, P.H., Eng, J.J., & Hodgson, A.J. (2005). Saturated muscle activation contributes to compensatory reaching strategies after stroke. J Neurophysiol, 94(5), 2999-3008. doi: 10.1152/jn.00732.2004 Moran, D.W., & Schwartz, A.B. (1999). Motor cortical representation of speed and direction during reaching. J Neurophysiol, 82(5), 2676-2692. Murillo, N., Kumru, H., Vidal-Samso, J., Benito, J., Medina, J., Navarro, X., & Valls-Sole, J. (2011). Decrease of spasticity with muscle vibration in patients with spinal cord injury. Clin Neurophysiol, 122(6), 1183-1189. doi: 10.1016/j.clinph.2010.11.012 Noma, T., Matsumoto, S., Etoh, S., Shimodozono, M., & Kawahira, K. (2009). Anti-spastic effects of the direct application of vibratory stimuli to the spastic muscles of hemiplegic limbs in post-stroke patients. Brain Inj, 23(7), 623-631. doi: 10.1080/02699050902997896 Noma, T., Matsumoto, S., Shimodozono, M., Etoh, S., & Kawahira, K. (2012). Anti-spastic effects of the direct application of vibratory stimuli to the spastic muscles of hemiplegic limbs in post-stroke patients: A proof-of-principle study. J Rehabil Med, 44(4), 325-330. doi: 10.2340/16501977-0946
Paoloni, M., Giovannelli, M., Mangone, M., Leonardi, L., Tavernese, E., Di Pangrazio, E., Pozzilli, C., et al. (2013). Does giving segmental muscle vibration alter the response to botulinum toxin injections in the treatment of spasticity in people with multiple sclerosis? A single-blind randomized controlled trial. Clin Rehabil, 27(9), 803-812. doi: 10.1177/0269215513480956 Paoloni, M., Mangone, M., Scettri, P., Procaccianti, R., Cometa, A., & Santilli, V. (2010). Segmental muscle vibration improves walking in chronic stroke patients with foot drop: A randomized controlled trial. Neurorehabil Neural Repair, 24(3), 254-262. doi: 10.1177/1545968309349940 Reina, G.A., Moran, D.W., & Schwartz, A.B. (2001). On the relationship between joint angular velocity and motor cortical discharge during reaching. J Neurophysiol, 85(6), 2576-2589. Roll, J.P., Vedel, J.P., & Ribot, E. (1989). Alteration of proprioceptive messages induced by tendon vibration in man: A microneurographic study. Exp Brain Res, 76(1), 213-222. Rosenkranz, K., Pesenti, A., Paulus, W., & Tergau, F. (2003). Focal reduction of intracortical inhibition in the motor cortex by selective proprioceptive stimulation. Exp Brain Res, 149(1), 9-16. doi: 10.1007/s00221-002-1330-3 Rosenkranz, K., & Rothwell, J.C. (2003). Differential effect of muscle vibration on intracortical inhibitory circuits in humans. J Physiol, 551(Pt 2), 649-660. doi: 10.1113/jphysiol.2003.043752 Siggelkow, S., Kossev, A., Schubert, M., Kappels, H.H., Wolf, W., & Dengler, R. (1999). Modulation of motor evoked potentials by muscle vibration: The role of vibration frequency. Muscle Nerve, 22(11), 1544-1548. Steyvers, M., Levin, O., Van Baelen, M., & Swinnen, S.P. (2003). Corticospinal excitability changes following prolonged muscle tendon vibration. Neuroreport, 14(15), 1901-1905. doi: 10.1097/01.wnr.0000093296.63079.fa Tavernese, E., Paoloni, M., Mangone, M., Mandic, V., Sale, P., Franceschini, M., & Santilli, V. (2013). Segmental muscle vibration improves reaching movement in patients with chronic stroke. A randomized controlled trial. NeuroRehabilitation, 32(3), 591599. doi: 10.3233/NRE-130881 Wagner, J.M., Dromerick, A.W., Sahrmann, S.A., & Lang, C.E. (2007). Upper extremity muscle activation during recovery of reaching in subjects with post-stroke hemiparesis. Clin Neurophysiol, 118(1), 164-176. doi: 10.1016/j.clinph.2006.09.022 Wu, C., Trombly, C.A., Lin, K., & Tickle-Degnen, L. (2000). A kinematic study of contextual effects on reaching performance in persons with and without stroke: Influences of object availability. Arch Phys Med Rehabil, 81(1), 95-101.
Copyright of NeuroRehabilitation is the property of IOS Press and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
