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To investigate muscle tone changes over time in contralateral homonymous muscles when unilateral muscles are stimulated, using F-wave measurements, we examined whether vibratory stimulation on the contralateral homonymous muscle of the affected side may reduce spasticity, whose optimal duration remains unclear.
Methods
Vibratory stimulation was applied to the right hand of healthy adults, using parameters of 80 Hz frequency, 0.4 mm amplitude, 400 g load, and 195 seconds of duration on the abductor digiti minimi muscle. F-wave was measured in the left hand before stimulation, at seven intervals during stimulation, and immediately after.
Results
The F/M amplitude ratio decreased immediately at stimulation onset, at 30 seconds, and at 60 seconds compared to baseline. A least-squares analysis revealed a negative slope from baseline to 60 seconds (f(x)=-0.11x+1.12), while the slope became positive after 90 seconds, continuing after stimulation ended (f(x)=0.04x+0.82).
Conclusion
Unilateral vibratory stimulation may decrease excitability in the spinal anterior horn cells of the contralateral homonymous muscle for up to 75 seconds post-stimulation, suggesting a potential mechanism for spasticity management.
Spasticity is a typical symptom of cerebrovascular disease, characterized by increased muscle tone, particularly in the fingers and wrist joints [1]. Furthermore, in rehabilitation situations, patients often experience spasticity in these areas, making it difficult for them to release objects they have grasped. Spasticity also inhibits patients’ activities of daily living (ADL) and quality of life [2], and increases the burden on caregivers [3]. Therefore, reducing muscle tone in the fingers is crucial for improving ADL. To address this issue, various methods have been developed to suppress muscle tone, including vibratory stimulation [4]. Vibration is a wave that remains constant and oscillates, and is composed of amplitude and wavelength. Amplitude refers to the height of the wave, and wavelength is the periodic length of the wave. Frequency is the number of times the vibration is repeated per unit time, and is closely related to wavelength. By applying these stimuli to the human body, it is possible to alter muscle tonus. Typical methods include direct stimulation of the affected muscle to induce neurotransmitter depletion and changes in muscle spindle sensitivity [5-7], as well as stimulation of the antagonist muscle corresponding to the affected muscle, to induce reciprocal inhibition. These aforementioned methods [8,9], have been reported to impede the inhibitory effect of the muscle tonus following vibratory stimulation [10,11]. This refers to the fact that exercise therapy after vibratory stimulation causes an immediate increase in muscle tonus. Furthermore, it is difficult to combine exercise therapy with vibratory stimulation because it is necessary to immobilize the stimulation site in order to provide vibratory stimulation to the affected muscle or its antagonist muscle. As such, the clinical application of combining vibratory stimulation and exercise therapy remains to be explored. One potential solution to this problem is to suppress the muscle tonus of the affected muscle by stimulating the contralateral homonymous muscle that corresponds to the affected muscle [12]. This approach involves providing vibratory stimulation to the contralateral homonymous muscle corresponding to the affected muscle while performing exercise therapy for the affected muscle, thereby combining vibratory stimulation and exercise therapy. However, in our previous research, the results were limited to those obtained when the vibration stimulation time was set to an extremely short 15 seconds, and it can be said that the appropriate vibration stimulation time needs to be investigated for application in clinical settings [12]. Muscle tonus and spinal nerve function are closely related, and F-wave and H-reflex are representative tests. Moreover, F-wave is often used as an evaluation index for demonstrating treatment efficacy for post-stroke spasticity due to its strong association with muscle tonus [13,14]. The F-wave is a compound action potential that is elicited from the dominant muscle after an electrical stimulus applied to the motor nerve conducts retrogradely through the axon and re-fires in the anterior horn cells of the spinal cord. Furthermore, this action potential can be easily derived from the abductor pollicis brevis (APB) muscle of the hand. In contrast, the H-reflex is generally derived from the radial carpometacarpal flexor and radial carpometacarpal extensor muscles, making it more challenging to be derived from the hand muscles. When focusing on the hand muscles that limit ADL, the F-wave is often used as an evaluation index. The objective of this study was to investigate the effect of the duration of unilateral vibratory stimulation on the muscle tonus of the contralateral homonymous muscle using the F-wave.
METHODS
Participants
The subjects were 14 healthy right-handed adults (25.4±1.3 years) with no orthopedic or neurological history. Informed by previous studies indicating that a sample size of 10 to 20 participants is generally necessary, the number of participants in this study was set accordingly [15]. The Edinburgh Handedness Inventory was used to assess handedness, with a laterality index of 64 [16]. All the participants received verbal and written explanations of the study content and ethical considerations to ensure adequate understanding, including the risks and freedom to participate, before enrollment. Written informed consent was obtained from all participants. The study conformed to the guidelines of the Declaration of Helsinki. The Research Ethics Review Committee of Kansai University of Health Sciences approved the study (approval number 22-12) before initiation of the protocol.
Study procedure
Vibratory stimulation was administered to the right hand of all participants. F-wave were recorded from the left hand while vibratory stimulation was being administered to the right hand. F-wave measurements were taken while the participants were seated in a relaxed position. F-wave were recorded at the following time points: pre-vibratory stimulation (pre), immediately after initiating vibratory stimulation (0–15 seconds), 30 s (30–45 seconds), 60 s (60–75 seconds), 90 s (90–105 seconds), 120 s (120–135 seconds), 150 s (150–165 seconds), and 180 s (180–195 seconds), and immediately after the end of vibratory stimulation (post). The subjects were in a resting state without vibratory stimulation before and after the vibratory stimulation, and F-wave were recorded during the vibratory stimulation sessions.
Interventions
Vibratory stimulation typically involves setting the frequency, amplitude, load, stimulation site, and stimulation time [11,17]. In the present study, vibratory stimulation at a frequency of 80 Hz, an amplitude of 0.4 mm, and a load of 400 g was applied to the right short thumb abductor muscle. In previous studies, it was considered that by applying vibratory stimulation, the muscle spindles of the stimulated muscle become excited, and the sensation transmitted via the Ia fibers suppresses the excitability of the anterior horn cells of the spinal cord corresponding to the contralateral homonymous muscle [12]. In other words, it is necessary to set the vibratory stimulation conditions that make the muscle spindles of the stimulated muscle more likely to become excited. Therefore, we set the frequency, amplitude, load weight, and stimulation site that would easily excite the muscle spindle, with reference to previous studies [18-22]. The muscle belly of APB was identified in the middle of the line connecting the base of the first basal phalanx and the navicular bone to control the recording site. To confirm that the muscles could be stimulated during the vibratory stimulation, the movement of the thumb produced by the tonic vibration reflex was verified [8]. Regarding the duration of vibratory stimulation, in previous studies, when vibratory stimulation was administered to suppress the muscle tonus, the targeted muscle was often stimulated for 60–300 seconds [23,24]. In our study, the vibratory stimulation was set for 195 seconds, and changes in the F-wave derived from the contralateral homonymous muscle to the stimulated muscle were monitored. A muscle-tendon vibratory stimulation device, MGV-1000-F (Uchida Electron Co., Ltd.), was utilized to apply the vibratory stimulation (Fig. 1).
F-wave recording
Neuropack S3 (Nihon Kohden Co., Ltd.) was used for F-wave recording. The recording conditions for the F-wave were as follows: stimulation site, median nerve; stimulation frequency, 2 Hz; and stimulation duration, 0.2 ms. The minimum amplitude standard for the F-wave was set at 30 μV [25], and the waveform analysis items were F/M ratio and F-wave persistence. The F-wave measurements for each participant were performed at a randomly assigned time between 17:00 and 19:00, with the room temperature maintained at 25°C [26].
Statistical analysis
Statistical analysis was performed using a generalized liner mixed model with the F/M amplitude ratio at each time point as the dependent variables. The time factor was set as a fixed effect, and individual differences were set as a random effect. The main effect was compared with each time point starting from the F/M amplitude ratio at pre-stimulation. The effect size was evaluated by calculating the correlation coefficient between the observed and predicted values, and then squaring this value to obtain a pseudo coefficient of determination (R²), which was used to indicate the goodness of fit of the model. The slope was determined using the least squares method from the time before the significant difference to the time when the significant difference was observed, and from the time when the significant difference was not found to the time immediately following the vibration stimulus. In addition, by plotting the median for each time point, a scatter plot was created, and a regression line was drawn to provide a visual overview of the characteristics over time. Statistical analysis was performed using IBM SPSS Statistics for Windows version 28.0 (IBM Corp.) at a significance level of 5%.
RESULTS
The mean F/M amplitude ratio was 1.2±0.8% before vibratory stimulation, 0.7±0.4% immediately after initiating vibratory stimulation, 0.8±0.4% at 30 s, 0.8±0.5% at 60 s, 1.0±0.8% at 90 s, 1.0±0.7% at 120 s, 0.9±0.7% at 150 s, 1.0±0.7% at 180 s, and 1.0±0.7% immediately after vibratory stimulation was completed. The results are summarized in Table 1.
The results at each time point were compared using the pre-vibratory stimulation value as the reference time point. The results revealed a significant decrease from immediately after inhibition of vibration stimulation to 60 s, and no change was observed at the later time points (Fig. 2). The pseudo R² was 0.042, indicating a low goodness of fit between the observed and predicted values. The slope of the regression line from before the start of the vibratory stimulation to the 60-second time point was calculated to be f(x)=-0.11x+1.12. The slope of the regression line from the time of 90 s to just after the end of the vibratory stimulation showed a positive slope of f(x)=0.04x+0.82 (Figs. 3, 4).
DISCUSSION
In this study, vibratory stimulation at a frequency of 80 Hz, an amplitude of 0.4 mm, and a load of 400 g was applied to the right APB for 195 seconds, with F-waves recorded from the left APB every 15 seconds after stimulation onset. The F/M amplitude ratio decreased until 60 seconds but gradually returned to baseline levels thereafter. There are several previous studies that have examined the effects of unilateral vibration stimulation on muscle tone in the contralateral side [27,28]. However, there is no consistent view on the effects. One reason for this is the variation in vibration stimulation conditions. In particular, parameters such as frequency, amplitude, duration, site of stimulation, and muscle condition during stimulation vary across studies. Therefore, in order to solve these problems, this study differs from previous studies in that it confirmed the effects of vibratory stimulation after setting the vibratory stimulation conditions that are considered to be likely to excite the muscle spindle based on a review of previous studies. It has been demonstrated that vibration-induced excitation of the muscle spindle transmits sensory information via Ia fibers [29,30]. Furthermore, sensory input from the stimulated APB muscle spindle transmitted via Ia fibers and spinal interneurons activates inhibitory interneurons on the opposite side, contributing to the suppression of muscle tone in the opposite APB [31,32]. Previous studies have emphasized that there are no changes in the primary motor cortex that controls the contralateral homonymous muscle corresponding to the vibrated muscle [33,34]. These results suggest that the vibration stimulus transmitted sensory input from the muscle spindle of the stimulated APB via spinal interneurons, and suppressed the F/M amplitude ratio of the contralateral APB. The F/M amplitude ratio of the contralateral homonymous muscle corresponding to the vibratory stimulation muscle was suppressed via the commissural interneurons in the spinal cord. Next, regarding the change in F/M amplitude ratio over time, past research has shown that when a vibration stimulus is applied, the muscle spindle of the stimulated muscle can remain in an excited state for up to 20 seconds [18]. As a neurophysiological mechanism for these findings, previous studies have shown that the stimulation of the spinal cord by vibratory stimulation produces a tonic vibration reflex, a monosynaptic reflex mediated by Ia fibers, in the vibratory stimulation muscle, which acts promptly on the spinal cord anterior horn cells corresponding to the vibratory stimulation muscle [8,9]. However, the sensory input via Ia fibers is not a stimulatory stimulus because the sensitivity of the muscle spindle changes over time and the stimulating muscles are not affected. The sensitivity of the muscle spindle to sensory input via Ia fibers changes over time, inhibiting sensory input from the stimulating muscle and making it difficult to transmit sensory information [7]. The results of the present study suggest that, although the sensory information via Ia fibers is input at 20 seconds after the start of stimulation, the sensitivity of the muscle spindle on the vibratory stimulation side gradually changes, and the suppression effect of the muscle tonus on the contralateral homonymous muscle corresponding to the stimulated muscle is impaired after 75 seconds. In summary, the F/M amplitude ratio decreased immediately after the start of vibratory stimulation and continued to do so up to 75 seconds. This decrease in the F/M amplitude ratio likely reflects the suppression of anterior horn cell excitability in the contralateral homonymous muscle, mediated by Ia fiber input and commissural interneurons. However, after 90 seconds, a threshold shift in the muscle spindle’s responsiveness is believed to reduce its inhibitory influence on the excitability of anterior horn cells in the spinal cord of the contralateral homonymous muscle corresponding to the stimulated muscle, and the muscle approaches a resting state.
Next, we will discuss clinical applications. The F-wave used in this study is a typical indicator for evaluating spasticity and is closely related to clinical indicators. In previous studies, persistence and F/M amplitude ratio were used as evaluation indicators for F-waves, and it was interpreted that the smaller these values were, the less spasticity there was [25,35]. In the results of this study, the F/M amplitude ratio at 0, 30, and 60 seconds after vibration stimulation was significantly reduced compared to before vibration stimulation. This suggests that the vibration stimulation used in this study may contribute to the alleviation of spasticity for about one minute. Recently, this method has been applied in clinical practice as a rehabilitation technique that promotes motor control [36]. However, limited clinical studies have been conducted in spasticity patients, and the efficacy of this intervention remains inconclusive. Patients with spasticity are forced to exert excessive force due to increased muscle tone, and abnormal joint movement is likely to occur. As a result, it becomes difficult to properly regulate force, and this may lead to incorrect motor learning. From the perspective of clinical application, the results of this study suggest that applying vibration stimulation to patients with spasticity may reduce muscle tone in the contralateral limb and promote deviation from abnormal joint movement. However, the results of this study only suggest short-term effects, and further research is needed to investigate the long-term effects of sustained stimulation and the cumulative effects of repeated application.
In addition, the small number of subjects is a limitation of this study, which may limit the generalizability of the findings. Therefore, it is necessary to increase the sample size and conduct further studies in the future.
CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.
FUNDING INFORMATION
None.
AUTHOR CONTRIBUTION
Conceptualization: Kunoh K, Suzuki T. Methodology: Kunoh K, Suzuki T. Formal analysis: Kunoh K, Kimura D. Project administration: Suzuki T. Visualization: Kunoh K. Writing – original draft: Kunoh K. Writing – review and editing: Takenaka T, Kimura D, Suzuki T. Approval of final manuscript: all authors.
ACKNOWLEDGEMENTS
We would like to thank all those who participated in this study.
Fig. 1.
Vibration stimulator used in this study. The vibratory stimulation head is the part that provides the vibration stimulus. The panel allows you to adjust the frequency, amplitude and stimulus time (A). The location of the focal vibrator was the muscle belly of the right abductor pollicis brevis (B).
Fig. 2.
Generalized liner mixed model results in F/M amplitude ratio. *Statistically significant, p<0.05.
Fig. 3.
Regression line from the start of the least-squares stimulation to the 60-second time point.
Fig. 4.
Regression line from the time of 90 seconds to the end of stimulation by the least-squares method.
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Unilateral Vibratory Stimulation Inhibits Contralateral Spinal Anterior Horn Cells in Homonymous Muscles for the First 75 Seconds
Fig. 1. Vibration stimulator used in this study. The vibratory stimulation head is the part that provides the vibration stimulus. The panel allows you to adjust the frequency, amplitude and stimulus time (A). The location of the focal vibrator was the muscle belly of the right abductor pollicis brevis (B).
Fig. 2. Generalized liner mixed model results in F/M amplitude ratio. *Statistically significant, p<0.05.
Fig. 3. Regression line from the start of the least-squares stimulation to the 60-second time point.
Fig. 4. Regression line from the time of 90 seconds to the end of stimulation by the least-squares method.
Graphical abstract
Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Graphical abstract
Unilateral Vibratory Stimulation Inhibits Contralateral Spinal Anterior Horn Cells in Homonymous Muscles for the First 75 Seconds
F/M amplitude ratio±SD (％)
95％ CI lower
95％ CI upper
p-value
Pre stimulation
1.2±0.8
-
-
-
0 s
0.7±0.4
-0.756
-0.115
0.002*
30 s
0.8±0.4
-0.671
-0.029
0.024*
60 s
0.8±0.5
-0.699
-0.058
0.011*
90 s
1.0±0.8
-0.456
0.185
>0.999
120 s
1.0±0.7
-0.521
0.121
0.678
150 s
0.9±0.7
-0.549
0.092
0.394
180 s
1.0±0.7
-0.456
0.185
>0.999
Post stimulation
1.0±0.7
-0.449
0.192
>0.999
Table 1. Changes over time in the F/M amplitude ratio
