The adopted electromagnetic actuator was an industrial permanent magnet motor (MSK060C IndraDyn®, Bosch-Rexroth, Boxtel, The Netherlands) controlled by a dedicated drive (Rexroth IndraDrive®). The drive received its voltage input from a PC. The control software that generates the input waveform was developed with LabView® (National Instruments, Austin, TX). Torque transmitted to the user was hence determined in real time by the software controlling a PCI-5402 wave generator (National Instruments), inputting the motor drive the sum of a DC (constant) and a sinusoidal voltage.
As shown in Figure 2, the mechanical transmission transfers the torque generated by the motor to a rotating lever, which applies the force to the muscles. In static conditions, this force is linearly related to the input voltage to the motor drive.
To characterize the system in dynamic conditions, it was necessary to fully identify the transmission, measuring the moment of inertia of the transmission wheels as well as the elastic and damping coefficients of the transmission belts. This was done by measuring the dynamic response of the system for varying frequencies of the input voltage. Using this procedure, the transfer function of the system could be characterized between 20 and 40 Hz, showing a peak at 29 Hz and a deep at 30 Hz (30). In this study, the loading force was therefore modulated at 28 Hz to be able to superimpose a reliable vibration stimulation. Frequencies around 30 Hz are typically adopted in vibration training, and they are reported to provide the highest increase of electrical activation of the vastus lateralis (11). In the adopted setup, the amplitude of the input sinusoidal waveform was set to 1.2 V. Combining the linear and dynamic characterization of the mechanical system, the amplitude of the force oscillations was estimated to be equal to 400 N.
The test subjects were 12 healthy volunteering students of the Eindhoven University of Technology, five males and seven females with ages varying between 19 and 27 yr (mean = 22.7; SD = 2.6). The level of training varied significantly, from sedentary to physically active. None of the subjects had history of muscular injuries or diseases. Written informed consent was obtained from each subject, and the test procedures were approved by the board of the Student Sport Centre of the Eindhoven University of Technology.
The subjects were asked to perform an isometric arm flexion or extension task with the setup shown in Figure 2 to establish their maximum force. The subjects were sitting in the testing device with their elbow at a forward elevation of 30° and an angle of 90°. An increasing force was applied by the electromagnetic actuator until the subject could not sustain it. The maximum sustained force (MSF) was measured three times, and the average value was considered as the reference for the MSF.
After establishing the MSF, the subjects performed 15-s isometric contractions (five different loads) with a resistance between 20% and 100% of the MSF. Each measurement was performed with (experimental condition [V]) and without (control condition [C]) vibration. The arm flexion task was performed first, with a 3-min rest between the measurements. After 15-min rest, the arm extension measurements were performed following the same procedure.
During the isometric contractions, surface EMG was recorded simultaneously from the biceps and triceps by two pairs of electrodes in bipolar configuration. The electrode pairs were aligned with the muscle fiber direction and placed between the tendon (at the elbow side) and the muscle belly. Circular Ag-AgCl electrodes of 1-cm diameter were used. The interelectrode distance was 2 cm. The skin was prepared by abrasion before the application of the electrodes to reduce the contact impedance.
The measured signals were amplified and digitized by a Mobi8 amplifier (TMS International, Enschede, The Netherlands). The sampling frequency was 2048 Hz. Active grounding and shielding of the cables were used to minimize the electromagnetic interference coming from the electrical motor and the powerline (50 Hz) (38). The active ground electrode was placed on the wrist. The digitized signals were transmitted to a personal computer by Bluetooth® wireless technology.
The root mean square (RMS) of the recorded EMG signals was used to establish muscle activation patterns as also suggested by previous authors (28). During isometric exercise, the recorded EMG signals are expected to be stationary. As a result, the signal characteristics, such as the power spectrum, do not vary over time, and the RMS can be calculated over longer time segments.
Vibration measurements can be affected by motion artifacts resulting in spectral components at the modulating frequency and its harmonics (2). Therefore, we developed a simple approach to make the RMS measurement insensitive to motion artifacts. This approach was based on the Parseval's equality, which permits the estimation of the RMS in the frequency domain based on the power spectrum (28). Given the signal stationarity, the spectrum was analyzed in the time interval between 2 and 7 s, providing a frequency resolution of 0.2 Hz. The RMS of the signal s(nT s), being T s the sampling period (1/2048 s), was then derived from the sum of the power at each frequency S(2π/nT s) for n∈[1, 5/T s]. Therefore, the frequencies corresponding to the modulation frequency and its harmonics could be excluded very precisely from the estimation, without the transition band limits of standard filtering techniques.
The recorded data were analyzed using a custom written routine in Matlab® (The MathWorks, Natick, MA), and the frequency spectrum was estimated using a fast Fourier transform (28). On the basis of the frequency analysis, a bandwidth of ±0.8 Hz around each harmonic was excluded from the RMS calculation, and only frequencies between 20 and 450 Hz were considered. Previous studies have suggested that this is the EMG bandwidth, containing the most relevant information to estimate the level of muscular (electrical) activity (2,28). Figure 3 shows a power spectrum example together with the frequency intervals that were excluded from the RMS calculation.
Due to the active grounding and shielding of the cables, the measurements were not influenced by the 50-Hz powerline interference. This was verified by assessment of the ratio between the 50- and the 45-Hz frequency components over the complete set of measurements. The average ratio was close to one (1.07 ± 0.29), which proves the assumption of a negligible interference. The absence of the powerline interference can also be noticed in Figure 3.
The RMS of the data recorded from each subject with and without V was normalized with respect to the value measured at 100% of the MSF without 28-Hz V. This procedure was used for both biceps and triceps.
To evaluate the effect of V on the level of coactivation of the muscles acting on the elbow joint, the ratio between the normalized RMS values measured from the antagonist and the agonist muscle was also calculated with and without V.
All data are presented as mean and SD. EMG data were normalized to EMG recorded during MSF without V. A two-way ANOVA (treatment  × intensity ) was used to analyze the differences in average EMGRMS between treatments and intensities for each muscle. Alpha was set at 0.05. In addition, paired Student's t-tests (one tail, different variance) were applied at each load intensity (percentage of MSF) to compare EMG activity during V with C and to establish the significance level (P value) of the deviations of the mean values.
Effects of V on EMG activity
The statistical analysis revealed significant differences in both triceps and biceps muscle activity not only for different load intensities (P < 0.001) but also for different treatments (V and C, P < 0.05), with the exception of the triceps during the arm flexion task. In general, a larger EMGRMS activity of the biceps and the triceps brachii muscles was observed when V was applied. The analysis of the mean EMGRMS values at each intensity level revealed an average increase of the EMGRMS in V ranging from 18.2% to 77.2% when compared with C.
The triceps brachii EMG activity was more influenced by the V when used as agonist (arm extension task), with an average increase of 45.2% (P < 0.05) against the 18.2% (P = 0.15) when used as antagonist (arm flexion task). The opposite was shown to occur to the biceps brachii, which showed an average increase of 77.2% (P < 0.05) when used as antagonist (arm extension task) and of 26.1% (P < 0.05) when used as agonist (arm flexion task).
Effects of V on different levels of contractile activity
During the arm flexion task (see Fig. 4), the benefit of V on biceps brachii was significant when superimposed to load intensities equal to 80% (+28.3%, P < 0.05) and 100% of MSF (+37.7%, P < 0.05). The measured EMGRMS increase of the triceps was not statistically significant.
During the arm extension task (see Fig. 5), the effects of V on triceps brachii EMGRMS activity were significant when superimposed to loads equal to 80% (+68.7%, P < 0.05) and 100% (+97.9%, P < 0.05) of MSF, whereas a significant increase in biceps brachii EMGRMS activity was observed at 40% of MSF (+112.6%, P < 0.05).
A large variability was observed in the coactivation values. However, despite this variability, ANOVA revealed a significant difference between intensities and between treatments (V and C) during arm extension task (P < 0.01). In particular, for intensities equal to 20% and 40% of MSF, the level of coactivation increased by more than 125% (P < 0.05). During arm flexion, no significant difference could be observed (P values ranged from 0.2 to 0.3 for different intensities and treatments). Figure 6 shows the complete set of results for both tasks. The coactivation increase can be especially noticed at lower intensities in the arm extension task.
DISCUSSION AND CONCLUSION
The results confirm our hypothesis that superimposing a sinusoidal V signal to strengthening exercises increases neuromuscular activity. In fact, a higher EMG activity was found when V was applied as compared with the control condition in both the triceps and the biceps brachii muscles when acting as agonists in the extension and the flexion task, respectively. The effect of superimposing V was more evident when higher levels of muscular tension were exerted, reaching the maximum at 100% of the MSF.
Soft tissues have been suggested to act as wobbling masses that vibrate in a damped manner in response to mechanical stimulation (41). Muscle activity is able to alter the vibration characteristics of the soft tissues. In fact, changes in muscle tension alter frequency and damping coefficient of soft tissues. The muscle activation response observed when V was superimposed to various levels of force suggests that sinusoidal V signals of a relatively low frequency are effective when added to high levels of muscle tension (>70%).
This observed increase in EMG activity suggests that to dissipate the power of the sinusoidal stimulation, alterations in motor units recruitment patterns are necessary. Previous authors have suggested that faster motor units would be more suited to the damping of 15- to 50-Hz vibrations (42) when studying lower limbs muscles. The increase in EMG activity observed when muscles are exposed to sinusoidal stimulations, such as vibrations, has been previously attributed to the tonic vibration reflex (TVR) (20). The EMG response observed in the current experiment does not confirm the occurrence of TVR when V is applied. However, the large increase in EMG activity observed at force levels higher than 70% of MSF cannot be accounted for only by the TVR because only at this and at higher levels of muscle tension there was a large EMG increase.
Considering that rate coding and synchronization of motor units have been indicated as the main mechanisms able to increase force beyond 80% of maximal voluntary contraction in biceps brachii (18), it seems feasible to suggest that V may alter normal motor unit recruitment patterns, determining an increase in rate coding and synchronization and possibly facilitating the recruitment of faster motor units. In support of this hypothesis, Bongiovanni et al. (5) indicated a larger decline in the firing rates of high threshold motor units as a mechanism of prolonged vibration-induced maximal voluntary contraction depression.
Furthermore, Martin and Park (27) previously found an increase in motor units synchronization with increasing levels of force up until 20% of the maximum voluntary contraction in finger and wrist flexors muscles exposed to vibrations of frequencies ranging from 40 to 200 Hz. They concluded that the vibration-induced increases in EMG activity and the degree of motor unit synchronization were dependent on both vibration frequency and muscle contraction level. In our experiment, we aimed at understanding how a V affects muscle activation when superimposed to various levels of muscle contraction. Our results suggest that the effectiveness of such modulation is clearly muscle-tension dependent.
The large increase in EMGRMS of the target muscles observed in both arm flexion and extension tasks when acting as agonists supports our idea that muscle activation is larger, possibly due to recruitment of large motor units and improvements in voluntary drive when trying to perform such tasks with the superimposition of V. However, a central component should not be discarded. Previous studies have in fact suggested that vibration has an effect on motor cortical excitability modulation (16,37). Therefore, the increased neural drive cannot be ascribed only to local mechanisms, but some central involvement has to be taken in consideration and should be the focus of future studies.
Further consideration should be given to other mechanisms likely to be involved. It is well documented that applying a sinusoidal stimulation directly to a muscle or a tendon stimulates Ia afferents inducing the TVR (5,17). Ia afferent sensitivity has been previously shown to be affected by muscle length and muscle tension with TVR magnitudes affected also by muscle groups not directly stimulated with V (44). Furthermore, alterations in spindle sensitivity and γ-drive have been observed during reinforcement maneuver such as the Jendrassik maneuver (33). It follows that the increase in neuromuscular response observed with V may be the result not only of motor unit activation strategies but also of alterations in spindle sensitivity.
Although the activation of agonist muscles seems to benefit from V when the levels of muscle activity are high, cocontraction around the elbow joint follows the opposite pattern. The coactivation levels measured by the EMG ratio of antagonist to agonist were in fact higher at lower levels of force production. We hypothesized this was the case because when the agonist muscles produce low levels of force, joint rotation is mainly controlled by the antagonist, in particular when sinusoidal signals are superimposed. It is reasonable to suggest that the observed level of cocontraction served only to stabilize the joint and not to modulate agonist force output as both muscles were exposed to the V.
Interesting observations concern also the different increase of EMG activity in the triceps and the biceps brachii. Both triceps and biceps seem to be more sensitive to the use of V loading during elbow extension tasks, showing an average increase of EMG activity equal to 45.2% and 77.2%, respectively (P < 0.05). In general, arm flexion tasks are more commonly used in daily activities, and it is likely that our subjects were more capable of performing and controlling the arm flexion tasks. The large EMGRMS responses observed by both muscles during the arm extension task can be because the subjects were less accustomed to such movement and had more difficulty in controlling joint rotation, hence adopting a neural strategy favoring increased EMG activity.
In the present study, the frequency of V was fixed at 28 Hz. Previous studies on WBV exercise have suggested 30 Hz as the optimal training frequency for the vastus lateralis muscle (11). A variety of studies has been conducted with vibration exercise devices for the elbow (7) or vibrating plates (2,3,6,9,10). As reported in previous reviews, the adopted vibration frequencies have been in the range of 15-60 Hz (12). Although our study suggests the possibility of using such V frequency to determine a large EMG activity, the effect of different modulating frequencies could differ for different muscles, and the optimal frequency to determine the best training stimulus in the biceps and the triceps might be different. Our future research will therefore focus on these aspects and investigate the effects of different frequencies on the EMG activity of biceps and triceps.
Another interesting aspect that should be investigated concerns the EMG frequency components at the harmonics of the modulating frequency. Due to the presence of motion artifacts, these frequencies were excluded from the calculation of the EMGRMS. However, these components could contain interesting information that is worth investigating. Therefore, the use of electrodes that are less sensitive to motion artifacts and the implementation of adaptive filters based on motion estimation are being considered for future measurements.
This study is the first attempt to understand if superimposing V signals during resistance exercise can be effective. The observed effects of V on muscle activation and cocontraction as measured by EMG suggest this modality as a potential effective intervention not only for training athletes but also for developing rehabilitation programs. The observed cocontraction at low levels of muscle force suggests that such approach could be effective in subjects in the early stage of a rehabilitation program where low levels of muscle force are required paired with limited joint mobility.
Further studies are needed to elucidate the neurophysiological mechanisms involved with V and the most effective safe and effective protocols for various populations.
The realization of the force modulation prototype was supported by the Dutch technology foundation STW within the Valorization Grant program and the Innovation Lab of the Eindhoven University of Technology. The authors would also like to thank Anna Jackson for reviewing the grammar and the spelling of the manuscript.
The results of this study do not constitute endorsement by the American College of Sports Medicine.
1. Abercromby AF, Amonette WE, Layne CS, McFarlin BK, Hinman MR, Paloski WH. Vibration exposure and biodynamic responses during whole-body vibration training. Med Sci Sports Exerc
2. Abercromby AFJ, Amonette WE, Layne CS, McFarlin BK, Hinman MR, Paloski WH. Variation in neuromuscular responses during acute whole-body vibration exercise
. Med Sci Sports Exerc
3. Ahlborg L, Andersson C, Julin P. Whole-body vibration training compared with resistance training: effect on spasticity, muscle strength and motor performance in adults with cerebral palsy. J Rehabil Med
4. Bautmans I, Van Hees E, Lemper JC, Mets T. The feasibility of whole body vibration in institutionalised elderly persons and its influence on muscle performance, balance and mobility: a randomised controlled trial [ISRCTN62535013]. BMC Geriatr
5. Bongiovanni LG, Hagbarth KE, Stjernberg L. Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man. J Physiol
6. Bosco C, Cardinale M, Colli R, Tihanyi J, von Duvillard SP, Viru A. The influence of whole body vibration on jumping ability. Biol Sport
7. Bosco C, Cardinale M, Tsarpela O. Influence of vibration on mechanical power and electromyogram activity in human arm flexor muscles. Eur J Appl Physiol Occup Physiol
8. Bosco C, Colli R, Introini E, et al. Adaptive responses of human skeletal muscle to vibration exposure. Clin Physiol
9. Cardinale M, Ferrari M, Quaresima V. Gastrocnemius medialis and vastus lateralis oxygenation during whole-body vibration exercise
. Med Sci Sports Exerc
10. Cardinale M, Lim J. The acute effects of two different whole body vibration frequencies on vertical jump performance. Med Sport
11. Cardinale M, Lim J. Electromyography
activity of vastus lateralis muscle during whole-body vibrations of different frequencies. J Strength Cond Res
12. Cardinale M, Rittweger J. Vibration exercise
makes your muscles and bones stronger: fact or fiction? J Br Menopause Soc
13. Cardinale M, Wakeling J. Whole body vibration exercise
: are vibrations good for you? Br J Sports Med
. 2005;39(9):585-9; discussion 589.
14. Eklund G, Hagbarth KE. Normal variability of tonic vibration reflexes in man. Exp Neurol
15. Enoka RM. Muscle strength and its development. New perspectives. Sports Med
16. Fourment A, Chennevelle JM, Belhaj-Saif A, Maton B. Responses of motor cortical cells to short trains of vibration. Exp Brain Res
17. Fromm C, Noth J. Reflex responses of gamma motoneurones to vibration of the muscle they innervate. J Physiol
18. Gabriel DA, Kamen G. Experimental and modeling investigation of spectral compression of biceps brachii SEMG activity with increasing force levels. J Electromyogr Kinesiol
. in press.
19. Griffin MJ. Minimum health and safety requirements for workers exposed to hand-transmitted vibration and whole-body vibration in the European Union; a review. Occup Environ Med
20. Hagbarth KE, Burke D, Wallin G, Lofstedt L. Single unit spindle responses to muscle vibration in man. Prog Brain Res
21. Hagbarth KE, Eklund G. Tonic vibration reflexes (TVR) in spasticity. Brain Res
22. Issurin VB. Vibrations and their applications in sport. A review. J Sports Med Phys Fitness
23. Issurin VB, Liebermann DG, Tenenbaum G. Effect of vibratory stimulation training on maximal force and flexibility. J Sports Sci
24. Issurin VB, Tenenbaum G. Acute and residual effects of vibratory stimulation on explosive strength in elite and amateur athletes. J Sports Sci
25. Kinser AM, Ramsey MW, O'Bryant HS, Ayres CA, Sands WA, Stone MH. Vibration and stretching effects on flexibility and explosive strength in young gymnasts. Med Sci Sports Exerc
26. Kraemer WJ, Adams K, Cafarelli E, et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc
27. Martin BJ, Park HS. Analysis of the tonic vibration reflex: influence of vibration variables on motor unit synchronization and fatigue. Eur J Appl Physiol Occup Physiol
28. Merletti R, Parker PA. Electromyography
. Hoboken (NJ): Wiley, John & Sons, Inc.; 2004, 494 p.
29. Milner TE. Adaptation to destabilizing dynamics by means of muscle cocontraction. Exp Brain Res
30. Mischi M, Kaashoek I. Electromyographic hyperactivation of skeletal muscles by time-modulated mechanical stimulation. Conf Proc IEEE Eng Med Biol Soc
31. Nordlund MM, Thorstensson A. Strength training effects of whole-body vibration? Scand J Med Sci Sports
32. Poston B, Holcomb WR, Guadagnoli MA, Linn LL. The acute effects of mechanical vibration on power output in the bench press. J Strength Cond Res
33. Ribot-Ciscar E, Rossi-Durand C, Roll JP. Increased muscle spindle sensitivity to movement during reinforcement manoeuvres in relaxed human subjects. J Physiol
34. Roelants M, Verschueren SM, Delecluse C, Levin O, Stijnen V. Whole-body-vibration-induced increase in leg muscle activity during different squat exercises. J Strength Cond Res
35. Sale DG. Neural adaptation to resistance training. Med Sci Sports Exerc
36. Sands WA, McNeal JR, Stone MH, Russell EM, Jemni M. Flexibility enhancement with vibration: acute and long-term. Med Sci Sports Exerc
37. Siggelkow S, Kossev A, Schubert M, Kappels HH, Wolf W, Dengler R. Modulation of motor evoked potentials by muscle vibration: the role of vibration frequency. Muscle Nerve
38. van Rijn ACM, Peper A, Grimbergen CA. High-quality recording of bioelectric events. Med Biol Eng Comput
39. Wakeling JM, Liphardt AM. Task-specific recruitment of motor units for vibration damping. J Biomech
40. Wakeling JM, Liphardt AM, Nigg BM. Muscle activity reduces soft-tissue resonance at heel-strike during walking. J Biomech
41. Wakeling JM, Nigg BM. Modification of soft tissue vibrations in the leg by muscular activity. J Appl Physiol
42. Wakeling JM, Nigg BM, Rozitis AI. Muscle activity damps the soft tissue resonance that occurs in response to pulsed and continuous vibrations. J Appl Physiol
43. Ward K, Alsop C, Caulton J, Rubin C, Adams J, Mughal Z. Low magnitude mechanical loading is osteogenic in children with disabling conditions. J Bone Miner Res
44. Yasuda T, Izumizaki M, Ishihara Y, Sekihara C, Atsumi T, Homma I. Effect of quadriceps contraction on upper limb position sense errors in humans. Eur J Appl Physiol
Keywords:©2009The American College of Sports Medicine
VIBRATION EXERCISE; ELECTROMYOGRAPHY; SINUSOIDAL FORCE MODULATION; MUSCLE ACTIVATION; ANTAGONIST MUSCLES