Journal of Sports Science and Medicine
Journal of Sports Science and Medicine
ISSN: 1303 - 2968   
Ios-APP Journal of Sports Science and Medicine
Androit-APP Journal of Sports Science and Medicine
Views
6905
Download
221
from September 2014
 
©Journal of Sports Science and Medicine (2011) 10, 19 - 30

Research article
The Potential Neural Mechanisms of Acute Indirect Vibration
Darryl J. Cochrane 
Author Information
School of Sport and Exercise, Massey University, Palmerston North, New Zealand

Darryl J. Cochrane
✉ Schol of Sport and Exercise, Massey University, Private Bag 11 222, Palmerston North, New Zealand
Email: D.Cochrane@massey.ac.nz
Publish Date
Received: 27-05-2010
Accepted: 23-12-2010
Published (online): 01-03-2011
Share this article
 
ABSTRACT

There is strong evidence to suggest that acute indirect vibration acts on muscle to enhance force, power, flexibility, balance and proprioception suggesting neural enhancement. Nevertheless, the neural mechanism(s) of vibration and its potentiating effect have received little attention. One proposal suggests that spinal reflexes enhance muscle contraction through a reflex activity known as tonic vibration stretch reflex (TVR), which increases muscle activation. However, TVR is based on direct, brief, and high frequency vibration (>100 Hz) which differs to indirect vibration, which is applied to the whole body or body parts at lower vibration frequency (5-45 Hz). Likewise, muscle tuning and neuromuscular aspects are other candidate mechanisms used to explain the vibration phenomenon. But there is much debate in terms of identifying which neural mechanism(s) are responsible for acute vibration; due to a number of studies using various vibration testing protocols. These protocols include: different methods of application, vibration variables, training duration, exercise types and a range of population groups. Therefore, the neural mechanism of acute vibration remain equivocal, but spinal reflexes, muscle tuning and neuromuscular aspects are all viable factors that may contribute in different ways to increasing muscular performance. Additional research is encouraged to determine which neural mechanism(s) and their contributions are responsible for acute vibration. Testing variables and vibration applications need to be standardised before reaching a consensus on which neural mechanism(s) occur during and post-vibration.

Key words: Spinal reflexes, muscle tuning, motor unit firing frequency, motor unit synchronisation, inter-muscular co-ordination


           Key Points
  • There is strong evidence to suggest that acute indirect vibration acts on muscle to enhance force, power, flexibility, balance and proprioception, but little attention has been given to the neural mechanism(s) of acute indirect vibration.
  • Current findings suggest that acute vibration exposure may cause a neural response, but there is little consensus on identifying which neural mechanism(s) are specifically responsible. This is due to a number of studies using various vibration testing protocols (i.e.varying frequencies, amplitudes, durations, and methods of application).
  • Spinal reflexes, muscle tuning and neuromuscular aspects and central motor command are all viable neuromechanical factors that may contribute at different stages to transiently increasing muscular performance.
  • Additional research is encouraged to determine when (pre, during and post) the different neural mechanism(s) respond to direct and indirect vibration stimuli.

INTRODUCTION

Acute vibration training is gaining popularity as a modality for sport, exercise and physical rehabilitation as it initiates a rapidly and repeating eccentric-concentric action that evokes muscular work and elevates metabolic rate (Rittweger et al., 2003). Vibration exercise has taken on many different forms; custom built vibratory devices have recently been constructed specifically for flexibility training (Sands et al. , 2006), while other vibration units have been attached to resistance training equipment (Issurin and Tenenbaum, 1999) and smaller units have been directly applied to muscle and tendon. Over the past decade, two products have featured on the commercial market, an electric powered vibrating dumbbell and the vibrating platform. There are two types of vibrating platforms; the first produces vertical sinusoidal vibrations (VV), which are transmitted to the body via the platform, the second moves in a side-alternating motion (SV).

During vibration, the transference of energy occurs from the vibration source to the whole body or body part, which causes reactive forces within the body. These forces have the potential to be harmful, but also beneficial. The human body is a spring-mass system where tendons and muscles act like springs to store and release mechanical energy, where the stiffness and mass of these body parts will determine the natural frequency (Rittweger, 2010). Therefore, the body can acquire accumulated mechanical energy when the vibration frequency of the device matches parallels with the resonance frequency of the body (Rittweger, 2010). This can be controlled by adjusting body position and changing muscle stiffness (Mester et al., 2006) where muscles have innate damping characteristics that can absorb energy and generate heat (Wakeling et al., 2002).

The vibratory load is dependent on four variables: frequency (f), amplitude (A), acceleration (a), and duration (t). The number of cycles of oscillation determines the frequency (Hz); the amplitude refers to the maximal displacement of the oscillatory motion (mm); the acceleration (m·s-2 or g) determines the magnitude; and duration refers to the exposure time (min or s). Low vibration frequency (5-45Hz) has been reported to increase EMG activity, muscle force, and power (Bosco et al., 1999a; 1999b, Cardinale and Lim, 2003; Cochrane and Stannard, 2005; Cochrane et al., 2010b; Torvinen et al., 2002; Stewart et al., 2009) where excitatory responses of the muscle spindle are speculated to play a role in enhancing muscle activation, involving a spinal reflex mechanism. The muscle tuning response is another possible mechanism where the muscular system damps the vibration stimuli to promote muscle activity that may subsequently increase muscle function.

Additionally, the neural adaptations that occur from resistance and power training have been purported to be similar to that of acute indirect vibration (Bosco et al., 1998; 1999a; 1999b; Cardinale and Bosco, 2003; Delecluse et al., 2003). Neural aspects, such as motor unit recruitment, synchronisation, and co-contraction may be responsible for force and power increases following acute vibration. Other mechanisms of vibration, such as a warm-up effect, where friction between the vibrating tissues may raise muscle temperature (Issurin and Tenenbaum, 1999), coupled with a vibratory induced increase in blood flow (Kerschan-Schindl et al., 2001) may also contribute to enhancing muscle performance. To date, there has been no direct attempt to identify which mechanism(s) may contribute to the enhancement of neuromuscular performance. Therefore, this paper explores and assesses the possible neural mechanism(s) of acute indirect vibration.

Methodology

A search was conducted using the following electronic databases: Medline, PubMed, ISI Web of Knowledge and Scopus. Key search words included, vibration and whole-body vibration; which were used in combination with spinal reflexes, muscle tuning, neuromuscular (motor unit firing frequency, synchronisation, intermuscular co-ordination) and central motor command. Articles were checked for relevant content and were included based on the following criteria: 1. published in English; 2. examined acute (single session) vibration; 3. the participants were healthy and trained, 4. conference abstracts and proceedings were excluded.

Types of vibration

As mentioned previously there are many different methods of producing acute vibration. Small vibratory units have been applied directly to the muscle or tendon (Warman et al., 2002; Jackson and Turner, 2003); while larger custom-built vibratory units have been constructed for flexibility training (Kinser et al., 2008; Sands et al., 2006; 2008), and resistance training to elicit vibration transmission through cables of various machines (Issurin and Tenenbaum, 1999).

Over the last decade, two commercial forms of acute indirect vibration are available for consumer use, the vibrating platform and vibrating dumbbell, which produce vertical sinusoidal vibration. As stated earlier, two types of vibrating platforms exist that involve standing and/or performing dynamic and/or static exercises. One type of platform oscillates around a central axis, where a crankshaft on each side of the platform translates to a rotationalmotion of the electro- motor into a vertical displacement, inducing a seesaw motion, of which the amplitude is either small closer to central axis or larger near the edge of the platform (0-10 mm). The second commercial machine has electro-motors that produce vertical synchronous vibration where both legs vibrate as the platform moves predominately in the vertical direction, which results in simultaneous and symmetrical movement of both sides of the body during the vibration exposure. The foot placement of this platform is independent of amplitude and has a pre-setting of two ranges; 0- 2 mm or 4-6 mm. Commercially manufactured hand-held powered vibrating dumbbells have also been developed to target the upper-body where the central handle of the dumbbell rotates producing oscillatory movements to the body.

Various vibration protocols have examined the purported neural mechanism(s), through the investigation of different vibration equipment, varying vibration frequencies, amplitudes and durations, various exercises and participant types; all of the above could potentially influence the outcome measures. Additionally, a difference exists in applying the vibration by direct or indirect methods. Direct vibration is normally applied to muscle or tendon at a high vibration frequency (100-150 Hz), at a small amplitude (1-2 mm) for a short period of time (2-15 s), resulting in a transient increase in muscle activity known as the tonic vibration reflex (Eklund and Hagbarth, 1966). However, indirect vibration typically uses a lower vibration frequency (25-45 Hz), set at a high amplitude (2-10 mm) with longer duration time of either continuous (3-5 min) or intermittent exposure (30-60 s), where the vibration is applied through the feet (platform) or hands (cable or dumbbell).

Even so, there is still a lack of prescriptive guidelines for vibration, which makes it difficult to compare the various studies. The optimal vibration frequency, amplitude, duration and the type of exercises to perform remains equivocal due to inadequate validation of these variables. This aside, some experiments have failed to include appropriate control and/or sham conditions, giving uncertainty to the value of vibration. There is additional concern over the potential difference in vibration transmission between side-alternating (SV) and vertical (VV) vibration platforms. Earlier, Rittweger et al., 2001 proposed a hypothesis that in SV, the feet alternate between up and down positions, causing pelvis rotation and flexion of the spinal column, which decreases vibration transmission to the head. To test this hypothesis Abercromby et al., 2007b compared SV and VV platforms at a set vibration frequency and amplitude (f=30 Hz, A=4 mm) while performing slow dynamic squats (4s up and 4 s down) from 10 to 35° knee flexion. They found that vibration transmitted to the upper-body and head was 71 to 189% greater during VV than SV and concluded that the pelvis damped the vibration energy more during SV than the VV. However, a complete kinematic analysis of SV and VV conducted over a larger range of knee angles across different vibration frequencies and amplitudes are required to validate this claim.

In another study, the same authors (Abercromby et al., 2007a) investigated muscle activity of SV and VV (f = 30 Hz, A = 4 mm). They reported that during dynamic (from 10° to 35°of knee flexion, at a tempo of 4 s up 4 s down) and static squatting (18.5° knee flexion) the lower limb extensors (vastus lateralis and gastrocnemius) were activated significantly more during SV than VV; and the activation of the tibialis anterior was significantly greater during VV than SV. Therefore, it would be of interest to conduct additional static squat experiments at a variety of fixed knee angles and perform dynamic squats over a larger range of knee flexion to identify if further differences in muscle activation exist between VV and SV.

Spinal reflexes

It is suggested that acute vibration may improve muscular performance via neurogenic potentiation involving the spinal reflexes and muscle activation (Cardinale and Bosco, 2003, Rittweger et al., 2003). The main evidence in supporting neurogenic potentiation is based on measurements of the tonic vibration reflex (TVR). Previous studies have reported that a vibration stimulus is capable of augmenting muscle spindle activity, which causes an excitatory response in the primary endings of non-contracting muscle (Burke et al., 1976; Ribot-Ciscar et al., 1998). As a result of direct vibration, an ensuing muscle contraction occurs with reciprocal inhibition of its antagonists, which has been termed the TVR (Eklund and Hagbarth, 1965; 1966; Matthews, 1966). This elicits an excitatory response of the muscle spindle Ia fibres (Burke et al., 1976, De Gail et al., 1966, Roll et al., 1989), which is mediated by monosynaptic and polysynaptic pathways (Matthews, 1966; Romaiguere et al., 1991). The excitability of the motoneurons innervating the antagonist muscles are depressed by reciprocal inhibition (De Gail et al., 1966; Lance et al., 1966), and the monosynaptic stretch reflexes of the vibrated muscle are suppressed during the vibration (De Gail et al., 1966; Marsden et al., 1969).

Burke et al., 1976 found that when direct vibrations of 20-220 Hz (Table 1) were applied to a tendon of non-contracting muscle, the primary endings responded more during high frequency vibration than secondary endings, which corresponded to earlier findings from cat studies conducted by Bianconi and van der Meulen (1963) and Brown et al., 1967. However, Burke et al. (1976) also found that both primary and secondary endings respond by discharging in synchrony to the vibration stimulus, which contradicts Bianconi et al. (1963) findings. The explanation for this discrepancy is that Bianconi et al. (1963) did not differentiate between endings that were unresponsive and those capable of being activated from vibration.

When the vibratory stimulus is applied to an agonist muscle it causes reciprocal inhibition of the antagonist motoneurons (Bishop, 1974); but when vibration is applied simultaneously to the agonist and antagonist muscles, the facilitatory effect of each muscle group is inhibited (Hagbarth, 1967). However, when both muscles independently vibrate they show a strong TVR (Bishop, 1974). Vibration also causes suppression of the muscle’s phasic stretch reflexes (De Gail et al., 1966; Marsden et al., 1969). Arcangel et al., 1971 observed that during tendon vibration, the Achilles tendon reflex and the Hoffmann response (H response) were suppressed, but in the post-vibratory period the reflexes were potentiated, indicating that pre-synaptic inhibition of the Ia afferent terminals occurred (Gillies et al., 1969). Desmedt et al. (1978) confirmed that motor unit recruitment was suppressed by the direct application of high vibration amplitudes, which caused pre-synaptic inhibition of Ia afferents.

According to Bishop, 1974, four factors affect the TVR response: 1) the location of the vibration; 2) the excitability state of the CNS; 3) the initial length of muscle i.e. pre-stretch; and 4) the vibration frequency and amplitude. Research has suggested that the initial muscle length influences the strength of the TVR where further lengthening of a muscle will induce a stronger TVR (Bishop, 1974;(Eklund and Hagbarth, 1966). Vibration amplitude can determine the amount of stretch occurring within the muscle. Matthews, 1966 and Brown et al., 1967 reported that in decerebrated cats increasing the vibration amplitude caused an increase in TVR, as this activated a larger number of muscle-spindle endings and caused more α motoneurons to be activated (Luo et al., 2005). However, the range of amplitude, which caused augmentation, occurred between 25-150 μm (Bishop, 1974). Moran et al., 2007 argued that higher vibration amplitudes may only benefit sub-maximal contractions and proposed that in maximal voluntary contractions the Ia afferent discharge may reach a saturation threshold, where vibration is unable to cause further increases in Ia afferent inflow. Supporting evidence is based on observations that state, vibration can only increase maximal isometric contraction force and EMG activity when fatigue is present in the intrafusal fibres (Bongiovanni and Hagbarth, 1990) or when α-fibre are blocked (Hagbarth et al., 1986).

The Jendrassik manoeuvre is a procedure that involves contracting remote muscles, normally of the upper-body (particularly the forearm and jaw muscles) to induce a reflex response (Jendrassik, 1885). A common method for eliciting a reflex is to grasp the hands and pull them apart - this potentiates the stretch reflex and H-reflex (Delwaide and Toulouse, 1980; Dowman and Wolpaw, 1988). Using a prototype vibration machine consisting of a motorised horizontal leg press fitted with two electrically powered motors to the rear of the foot plate; young (21.5y) and old (69.2y) participants were vibrated at 30 Hz (A = 1 mm), whilst performing the Jendrassik manoeuvre for four minutes (Cochrane et al., 2008). This involved pulling with both arms a dual handle load cell at 10% maximal voluntary contraction while seated with their feet on the vibrating plate of the leg press with the knees flexed at 70°. The authors reported that superimposing the Jendrassik manoeuvre upon vibration enhanced metabolic rate in both young (27.6%) and old (33%) groups, but there were no significant differences between the groups (Table 1). Further, using a side-alternating vibration (SV) platform, acute low frequency vibration (f = 6 Hz, A = 3.1 mm) produced a temporal association between EMG activity and muscle contractile tissue displacement suggesting that muscle lengthening may be a prerequisite to eliciting probable stretch reflexes (Cochrane et al., 2009).

However, in a follow up study (Cochrane et al., 2010a) reported that after five minutes of continuous acute indirect vibration (f = 26 Hz, A = 6 mm, SV) there was minimal change in patellar tendon reflex properties, but muscle twitch characteristics were potentiated indicating that a greater myogenic response was present compared to a neural-mediated effect of a reflex potentiation. Likewise, Hopkins et al., 2008 found no effect on the patellar tendon reflex after intermittent (5 x 1 min bouts) vibration exposure (f = 26 Hz, A = 4 mm, SV). Other studies have reported enhancement of the stretch reflex, for example, Melnyk et al., 2008 initiated the stretch reflex in the hamstrings by inducing an anterior tibial translation during standing; they also compared the reflex response between two groups that performed either intermittent (2 x 1 min) vibration (f=30 Hz, A= 4 mm, VV) or normal activity (control). The researchers found post-vibration, that anterior tibial translation displacement decreased with a corresponding increase in EMG of the hamstring short latency response. The authors concluded that the effect of increased knee stability caused reflex excitability. However, it is inconclusive whether the stretch reflex was the causal factor in decreasing anterior tibial translation because the control group did not perform the same protocol without vibration. An earlier study reported an increase in the patellar tendon reflex immediately following exhaustive squatting exercise with continuous vibration (f = 26 Hz, A = 12 mm, SV) and extra load (40% of body mass). The authors concluded that α motoneurons were augmented by the vibration, which recruited high-threshold units and muscle fibres (Rittweger et al., 2003). To date, only one study has confirmed that stretch reflexes were induced during vibration (f = 5-30 Hz, A = 4 mm, SV) (Ritzmann et al., 2010). This study measured the EMG activity of the soleus and medial gastrocnemius muscles during different vibration frequencies in comparison to an evoked stretch reflex of the same muscle groups using a custom-built ankle ergometer and found that the EMG activity was identical between the vibration and the evoked stretch reflex, indicating the existence of vibration-induced reflexes.

Currently, two studies have examined the response of the H-reflex following acute indirect vibration, both producing different results. Nishihira et al., 2002 found that the H-reflex and H max/M max ratio was enhanced, suggesting that motoneuron excitability was heightened; while Armstrong et al., 2008 found the H-reflex was suppressed (Table 1). The disagreement in these findings was most likely due to different vibration and H-reflex protocols. Nishihira et al., 2002 used three sets of three minute vibration protocol (f = 25 Hz, A = not reported, SV) where the H-reflex was activated from a seated position, which differed to Armstrong et al., 2008 one minute duration performed on a VV platform (f = 40 Hz, A = 2-4 mm) where the H-reflex was activated from a supine position. Major limitations to the above studies were that both lacked a control group and both failed to disclose the exact testing protocol of the H-reflex.

In summary, the proposed mechanism of acute indirect vibration causing a response similar to that of TVR cannot be supported (Nordlund and Thorstensson, 2007). TVR requires vibration to be directly applied to the muscle or tendon at high vibration frequencies (>100 Hz), typically other vibration methods such as, platforms and dumbbells are not directly applied to the body and are subjected to lower frequencies (20-45 Hz) and longer exposure times (>30s). Therefore, it is difficult to uphold the view that acute indirect vibration may act through a spinal mechanism, such as TVR. However, vibration may cause an indirect involvement of muscle spindles, where other sensory inputs may influence gamma (γ) motoneuron activity, causing changes to spindle input (Gandevia, 2001). Additionally, the evidence is inconclusive whether acute indirect vibration potentiates stretch reflexes, this is due to the different vibration protocols, applications and durations; therefore it remains undetermined whether spinal reflexes are the causal mechanism.

Muscle tuning

There is evidence to suggest that the body is capable of tuning its muscle activity in order to reduce the vibrations that are passing through the soft tissue that may produce a detrimental effect (Nigg, 1997). The amount of muscle activity required is dependent on the level of vibration, where maximal muscle activation can reduce or purge oscillations within the tissues. Everyday activities such as walking, running and jumping result in impact forces, from the collision of the heel with the ground, producing vibrations of 10-20 Hz to the lower limbs (Wakeling and Nigg, 2001), where an input signal from the impact force produces muscle activity or ‘tuning’ response to reduce soft tissue vibrations. This activation or tuning supposedly occurs shortly before the heel strikes the ground (Nigg, 1997). Consequently, muscle tuning relies on three components: i) the frequency and amplitude of the input force, ii) the vibration resonance of the soft tissue and iii) the level of muscle activity. To test the activation level of additional muscles from vibrations, a hydraulic actuator was used to mimic the force during running, by directly evoking vibrations onto the sole of a foot using a range of vibration frequencies (10-65 Hz) (Wakeling et al., 2002). The study found that damping occurred in the lower limb soft tissues and resonance reduction occurred at heel strike (Table 2). However, the natural frequency of the soft tissues did not change and paralleled the frequency of the input. The mechanism of this response remains unclear, but if damping does occur in soft-tissues, where resonance is minimised at heel strike and the changes in frequency are a consequence of altered muscle activity then energy absorbed by the muscle is likely to involve cross-bridge cycling (Ettema and Huijing, 1994, Wakeling et al., 2002). Consequently, damping vibration will depend on the individual’s neuromuscular (muscle spindle) response, the sensitivity of joint and skin receptors, the proportion of muscle fibre types and viscoelastic (stiffness) elements (Bazzett-Jones et al., 2008). Due to impact forces, there is a possibility of vibrations occurring in soft tissues that have viscoelastic properties. Mechanical energy from the vibration can be stored and returned from the elastic structures of the muscle-tendon complex where the damping of vibrations may result in a net dissipation of mechanical energy that can be absorbed by activated muscle.

In summary, impact forces create vibrations in the foot where the vibrations travel through the lower limb musculature. To prevent resonance, soft tissues damp the vibrations, which cause sensory organs to send impulses to the CNS to increase muscle activity and adjust joint stiffness. The muscle tuning mechanism relies on the input force, the vibration response of the tissue and the level of muscle activity, which can make it difficult to analyse (Cardinale and Wakeling, 2005). There are similarities between single repeated impact inputs and continuous vibrations suggesting that the tissues minimise vibrations despite the input force mode. However, the validation of the muscle tuning hypothesis is dependent on developing further studies to determine the effect of vibration amplitude on tissue response.

Neuromuscular

The increase in muscle force and power following acute indirect vibrations are purported to be similar to resistance training (Bosco et al., 1998; 1999a; 1999b; Cardinale and Bosco, 2003; Delecluse et al., 2003). According to Cardinale and Bosco, 2003, resistance training and vibration place load on the neuromuscular system. During resistance training, extra load is added to increase the influence of gravity, in the form of barbells, dumbbells, rubber bands or manual resistance. Resistance in terms of vibration is altered by adjusting vibration frequency and/or amplitude, which increases the acceleration and force placed on the body. Increasing the acceleration has the ability to modify the neuromuscular aspects through neurogenic and myogenic factors. The initial changes (1-3 weeks) due to resistance and power training are often attributed to neural adaptations (Aagaard et al., 2002; Gabriel et al., 2006; Sale, 1988; Staron et al., 1994). However, protein synthesis, a precursor for hypertrophy can occur after one resistance training session (Chesley et al., 1992), changes in muscle size (hypertrophy) occur four to six weeks after training commences (Kraemer et al., 2002). Therefore, a closer examination of how acute indirect vibration may influence neural responses of motor unit firing, motor unit synchronisation, inter-muscular co-ordination is required.

Motor unit firing frequency

Motor unit firing frequency refers to the number of impulses per second that the muscle fibre of a motor unit receives from the motoneuron. The force output of every motor unit can be varied by the firing frequency from 10 to 60 impulses per second during sustained contractions (Sale, 2003). However, in high speed movements firing rates of 60-120 impulses per second are common during force production (Desmedt and Godaux, 1977). Force production increases as a result of increased motor unit recruitment and/or firing frequency. Therefore, when motor unit recruitment patterns and firing frequency rates are optimized, a maximal contraction force may occur. However, not all muscles exhibit the same characteristics; firing frequency and recruitment may differ from muscle to muscle.

Rapid changes in motor unit firing frequency have been reported in both young and older adults, after completing six weeks of resistance training (Kamen and Knight, 2004). The authors found that vastus lateralis motor unit firing frequency increased by 15% and 49% in young and older adults, respectively during maximal isometric knee extension. Likewise, Patten et al., 2001 reported that the firing frequency of the abductor digiti minimi was significantly increased 48 hours after completing maximal isometric contractions. These results indicate that early increases in force output due to resistance training are partly caused by increased firing frequency. When high frequency vibrations (150 Hz) were applied over the tendons of ankle dorsiflexor muscles, Bongiovanni and Hagbarth, 1990 reported that the firing frequency in non-fatigued muscle did not change; but the vibration caused an increase in force, EMG and firing frequency during fatiguing isometric maximal voluntary contractions (Table 3). Similarly, Griffin et al., 2001 reported that the firing frequency increased when direct vibration was applied to the distal tendon of the triceps brachii following a two minute sustained 20% maximal voluntary contraction (MVC). The authors suggest that during the isometric contraction muscle spindle activity declined to support the motoneuron pool, and consequently firing frequency decreased. However, muscle spindles are responsive to vibration, especially the Ia afferents (Burke et al., 1976; De Gail et al., 1966; Roll et al., 1989), which may prevent a decline in muscle spindle activity to support the motoneuron pool (Griffin et al., 2001).

In summary, application of direct brief vibration (10-20 s) to fatigued dorsiflexor muscles increased motor unit firing rate, enhanced EMG and augmented maximal force (Bongiovanni and Hagbarth, 1990). Likewise, motor unit firing frequency and isometric force increased in fatigued arm muscles when short duration direct vibrations were applied every 2s for 10s (Griffin et al., 2001) suggesting that motor output facilitation occurs during brief vibratory periods. However, current research has focused on direct vibration in fatigued and non-fatigued muscle, the effects of acute indirect vibration on the rate of motor unit firing frequency of non-fatigued muscle during range vibration frequencies (25-45 Hz) and amplitudes (2-10 mm) are relatively untested. Therefore, carefully well-designed studies with the appropriate electrophysiological techniques are required to determine if motor unit firing frequency plays a role in enhancing neuromuscular measures.

Motor unit synchronisation

Motor unit synchronisation relies on the number of motor units firing at any one time. Synchronisation occurs from branched inputs of pre-synaptic neurons that produce a common synaptic input to increase the chance of motoneurons discharging simultaneously (Fling et al., 2009). Increased motor unit synchronisation is one explanation used to account for the increase in force and power production following resistance training (Gabriel et al., 2006, Sale, 1988, Semmler, 2002). Milner-Brown et al., 1975 investigated the discharge rates of the first dorsal interosseous muscle and found that synchronisation was greater in weightlifters than control participants. However, synchronisation was estimated using an indirect method of averaging surface EMG signal with respect to motor unit discharge, which has since been challenged (Yue et al., 1995). By using direct motor unit measurements, Semmler and Nordstrom, 1998 reported that resistance trained weightlifters produced a higher level of synchronisation compared to highly skilled musicians, indicating that synchronisation may be an adaptation of resistance training to enhance force production. Yao et al., 2000 found that during motor unit synchronisation, EMG increased by 65-135% with corresponding force fluctuations. Martin and Park, 1997 reported that when direct vibration was applied to finger and wrist muscles, harmonic synchronisation decreased. However, sub-harmonic synchronisation increased when vibration frequency increased from 40 to 200 Hz, where high vibration frequency (>150 Hz) produced less motor unit synchronisation (Table 4).

Following acute indirect vibration, an enhancement in EMG, force, and power production provides evidence of improved motor unit recruitment (Bosco et al., 1998; 1999a; 2000; Cardinale and Bosco, 2003; Delecluse et al., 2003). However, according to Yue et al., 1995, surface EMG is a poor indicator of motor unit synchronisation and caution is required when interpreting results.

In summary, it has been well documented that direct vibration activates the primary afferent endings of the motor spindles which activate the α motoneurons to recruit previous inactive muscle fibres into contraction (Bishop, 1974). Future indirect vibration studies should focus on whether a greater number of potential motor units are synchronised due to the transmission of vibration from proximal to distal muscle groups. Further, it is there is a suggestion that an optimal vibration frequency exists to increase motor unit synchronisation and any vibration frequencies above this level may cause motor unit synchronisation to decrease (Jackson and Turner, 2003; Martin and Park, 1997). It remains unclear to whether motor unit synchronisation occurs during acute indirect vibration, as no studies have specifically assessed single motor unit discharge.

Inter-muscular co- ordination

Inter-muscular co-ordination is the interaction between muscle groups during muscular activity. Contraction of the agonists may be associated with simultaneous contraction of their antagonists (Sale, 1988). Tyler and Hutton (1986) reported antagonist co-contraction reduced agonist force production, indicated by a decrease in muscle activity (EMG). When performing new and complex tasks the co- contraction of antagonists through reciprocal inhibition may impair agonist contraction (Sale, 1988). However, through continual practice and training the level of co-contraction may be reduced, which could allow for a greater activation of the agonists. Carolan and Cafarelli, 1992 reported that after eight weeks of knee extensor resistance training, force increased in the knee extensors with a reduction in antagonist (bicep femoris) co-contraction, which was shown by a decrease in bicep femoris EMG activity (Table 5).

It has been stated that acute indirect vibration causes neural changes synonymous to that of resistance and power training (Bosco et al., 2000). If true, an improvement in agonist activation and increased inhibition of antagonist muscles should also exist. Evidence from acute direct vibration studies suggest that an excitatory response of the muscle spindle occurs, which activates the Ia afferents. These afferents in turn, excite the α motoneurons of the homonymous muscle, which may uncouple the co-contraction of agonist-antagonists (Eklund and Hagbarth, 1966). Rothmuller and Cafarelli, 1995 have reported that antagonist co-contraction increased during fatigue and vibration elicited a greater co-contraction than the control condition, but the co-contraction did not change during the fatigue of either condition.

Recently, Abercromby et al., 2007a suggested that acute indirect vibration causes neuromuscular responses that could be partly modulated by the co-contraction of the musculature acting at the knee joint. A study conducted by Mischi and Cardinale, 2009, investigated muscle activation and co-contraction of the biceps and triceps brachii muscles during isometric exercise with and without vibration. Using an electromagnetic actuator, mechanical sinusoidal vibrations generated a frequency of 28 Hz, which was applied to the biceps and triceps brachii for 15 s. They observed that co-contraction occurred at low levels of muscle force (20% and 40% maximum sustained force) during elbow extension, suggesting that co-contraction may serve to stabilise the joint, but it does not modulate agonist force production (Table 5). The authors concluded that vibration could be a viable option in the early stages of rehabilitation where low levels of muscle force are required due to limited joint mobility.

In summary, Mischi and Cardinale, 2009 findings provide some new insights to the response of superimposing vibration on agonist, antagonist and co-contraction of muscles. However, caution is advised, as the study utilized a single vibration frequency (28 Hz) with brief exposures to vibration and the recorded absence of amplitude also limits the findings of the study. Therefore, further studies investigating lower and upper limb vibration would assist in explaining the role that intramuscular co-ordination has in vibration.

Central motor command

Direct application of high frequency vibration on muscle and tendon activates Ia afferent of the muscle spindles and to a lesser extent, the secondary afferents and Ib afferents of the golgi tendon organ (Roll et al., 1989). However, there is evidence to support the notion that cortical areas of the brain receive and process proprioceptive information when direct high frequency vibration is applied, which generates evoked cortical potentials (Munte et al., 1996). It appears that muscle afferent input to the cerebral cortex plays a role in motor control (Wiesendanger and Miles, 1982); 30% of central motor drive is attributed to muscle afferent excitability (Macefield et al., 1993). Moreover, it has been reported that Ia afferent input has the ability to excite the corticospinal pathway (Carson et al., 2004) and activate the cortical motor areas (Lewis et al., 2001). To examine the potential changes of the motor cortex, the transcranial magnetic stimulation (TMS) method has been used to study the excitability of the corticospinal system, as well as the intracortical inhibitory and facilitatory processes. In brief, TMS delivers pulses to the motor cortex through a double cone coil placed over the scalp. It has been reported that motor-evoked potentials of TMS were enhanced when direct vibration (f = 80 Hz) was applied to extensor carpi radialis muscle (Kossev et al., 2001). Researchers have also suggested anecdotally that acute indirect vibration may influence the motor cortex to increase muscular performance (Cardinale and Bosco, 2003).

Mileva et al., 2009 investigated the effects of acute indirect vibration (f = 30 Hz, A = 1.5mm, VV) on corticospinal excitability and intracortical processes by studying motor-evoked potentials in the tibialis anterior and soleus muscles in response to TMS of the contralateral motor cortical leg area (Table 6). They found that acute indirect vibration increased the tibialis anterior corticospinal excitability pathway, but the intracortical facilitatory processing for the tibialis anterior was reduced. However, no significant changes were evident in the corticospinal excitability or intracortical facilitatory of the soleus. These findings suggest that acute indirect vibration may stimulate the corticospinal pathway; however, no performance measures were included with TMS.

In summary, there have been promising findings on vibration training and central motor command. Studies both confirm and refute the concept that direct and indirect vibration elicits a motor cortex response. Therefore, extensive research is required in the area of indirect vibration training to confirm that vibration causes an excitatory response in the motor cortex. Future indirect vibration studies should focus on expanding vibration platform research utilizing a range of vibration frequencies, amplitudes, durations and postural positions. Further vibration work is also required on the quadriceps and hamstrings to determine if acute indirect vibration truly increases the excitability of the corticospinal pathway.

CONCLUSION

Acute direct vibration is normally applied to the muscle or tendon using a high vibration frequency (>100 Hz), a low amplitude (1-2mm) and brief duration (2-15 s). Contrary, acute indirect vibration is administered intermittently (5 x 1 min) or continuously (3-5 min) at a frequency of 25-45 Hz and amplitude of 2-10 mm, which increases muscle (EMG) activity, muscle force, and power, suggesting that neural mechanisms are the main contributor. Spinal reflexes, muscle tuning, neuromuscular aspects and central motor command have been purported as possible neural mechanisms. However, it is unclear from the current research which mechanism(s) are responsible for enhancing muscular performance, it could be, that multiple mechanisms are involved. Current acute indirect vibration research lack standardization of testing and training protocols. Therefore, direct comparisons between studies are impractical, making it difficult to identify the underlying mechanism(s). The current inconsistency that exists in reporting and standardising acute indirect vibration protocols can be eliminated if future acute indirect vibration research adheres to the procedural recommendations developed by an expert international vibration research panel in 2010 (Rauch et al., 2010). Future acute indirect vibration research should focus on assessing single motor unit discharge, as this would provide further information in regards to motor unit frequency and motor unit synchronisation and assessing spinal reflexes during vibration would further enhance valuable knowledge of confirming the possible neural mechanisms.

AUTHOR BIOGRAPHY

Journal of Sports Science and Medicine Darryl J. Cochrane
Employment: Senior Lecturer, School of Sport & Exercise Massey University, Palmerston North, New Zealand.
Degree: PhD.
Research interests: Vibration exercise for performance, health and rehabilitation. Physical conditioning. Muscle physiology.
E-mail: D.Cochrane@massey.ac.nz
 
 
REFERENCES
Journal of Sports Science and Medicine Aagaard P., Simonsen E.B., Andersen J.L., Magnusson P., Dyhre-Poulsen P. (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. Journal of Applied Physiology 93, 1318-1326.
Journal of Sports Science and Medicine Abercromby A.F.J., Amonette W.E., Layne C.S., McFarlin B.K., Hinman M.R., Paloski W.H. (2007a) Variation in neuromuscular responses during acute whole-body vibration exercise. Medicine and Science in Sports and Exercise 39, 1642-1650.
Journal of Sports Science and Medicine Abercromby A.F.J., Amonette W.E., Layne C.S., McFarlin B.K., Hinman M.R., Paloski W.H. (2007b) Vibration exposure and biodynamic responses during whole-body vibration training. Medicine and Science in Sports and Exercise 39, 1794-1800.
Journal of Sports Science and Medicine Arcangel C.S., Johnston R., Bishop B. (1971) The achilles tendon reflex and the h-response during and after tendon vibration. Physical Therapy 51, 889-905.
Journal of Sports Science and Medicine Armstrong W.J., Nestle H.N., Grinnell D.C., Cole L.D., Van Gilder E.L., Warren G.S., Capizzi E.A. (2008) The acute effect of whole-body vibration on the hoffmann reflex. Journal of Strength and Conditioning Research 22, 471-476.
Journal of Sports Science and Medicine Bazett-Jones D.M., Finch H.W., Dugan E.L. (2008) Comparing the effects of various whole-body vibration accelerations on counter-movement jump performance. Journal of Sports Science and Medicine 7, 144-150.
Journal of Sports Science and Medicine Bianconi R., van der Meulen J. (1963) The response to vibration of the end organs of mammalian muscle spindles. Journal of Neurophysiology 26, 177-190.
Journal of Sports Science and Medicine Bishop B. (1974) Vibratory stimulation - neurophysiology of motor responses evoked by vibratory stimulation. Physical Therapy 54, 1273-1282.
Journal of Sports Science and Medicine Bongiovanni L.G., Hagbarth K.E. (1990) Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. Journal of Physiology-London 423, 1-14.
Journal of Sports Science and Medicine Bosco C., Cardinale M., Tsarpela O. (1999a) Influence of vibration on mechanical power and electromyogram activity in human arm flexor muscles. European Journal of Applied Physiology and Occupational Physiology 79, 306-311.
Journal of Sports Science and Medicine Bosco C., Cardinale M., Tsarpela O., Colli R., Tihanyi J., Duvillard S.P., Viru A. (1998) The influence of whole body vibration on jumping performance. Biology of Sport 15, 157-164.
Journal of Sports Science and Medicine Bosco C., Colli R., Introini E., Cardinale M., Tsarpela O., Madella A., Tihanyi J., Viru A. (1999b) Adaptive responses of human skeletal muscle to vibration exposure. Clinical Physiology 19, 183-187.
Journal of Sports Science and Medicine Bosco C., Iacovelli M., Tsarpela O., Viru A. (2000) Hormonal responses to whole body vibration in men. European Journal of Applied Physiology and Occupational Physiology 81, 449-454.
Journal of Sports Science and Medicine Brown M.C., Engberg I., Matthews P.B. (1967) The relative sensitivity to vibration of muscle receptors of the cat. Journal of Physiology-London 192, 773-800.
Journal of Sports Science and Medicine Burke D., Hagbarth K.E., Lofstedt L., Wallin B.G. (1976) Responses of human muscle-spindle endings to vibration of non-contracting muscles. Journal of Physiology-London 261, 673-693.
Journal of Sports Science and Medicine Cardinale M., Bosco C. (2003) The use of vibration as an exercise intervention. Exercise and Sport Sciences Reviews 31, 3-7.
Journal of Sports Science and Medicine Cardinale M., Lim J. (2003) Electromyography activity of vastus lateralis muscle during whole-body vibrations of different frequencies. Journal of Strength and Conditioning Research 17, 621-624.
Journal of Sports Science and Medicine Cardinale M., Wakeling J. (2005) Whole body vibration exercise: Are vibrations good for you?. British Journal of Sports Medicine 39, 585-589.
Journal of Sports Science and Medicine Carolan B., Cafarelli E. (1992) Adaptations in coactivation after isometric resistance training. Journal of Applied Physiology 73, 911-917.
Journal of Sports Science and Medicine Carson R.G., Riek S., Mackey D.C., Meichenbaum D.P., Willms K., Forner M., Byblow W.D. (2004) Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb. Journal of Physiology-London 560, 929-940.
Journal of Sports Science and Medicine Chesley A., Macdougall J.D., Tarnopolsky M.A., Atkinson S.A., Smith K. (1992) Changes in human muscle protein-synthesis after resistance exercise. Journal of Applied Physiology 73, 1383-1388.
Journal of Sports Science and Medicine Cochrane D.J., Loram I.D., Stannard S.R., Rittweger J. (2009) Changes in joint angle, muscle-tendon complex length, muscle contractile tissue displacement and modulation of emg activity during acute whole-body vibration. Muscle and Nerve 40, 420-429.
Journal of Sports Science and Medicine Cochrane D.J., Sartor F., Winwood K., Stannard S.R., Narici M., Rittweger J. (2008) A comparison of the acute physiologic effects of acute whole-body vibration exercise in young and older people. Archives of Physical Medicine and Rehabilitation 89, 815-821.
Journal of Sports Science and Medicine Cochrane D.J., Stannard S.R. (2005) Acute whole body vibration training increases vertical jump and flexibility performance in elite female field hockey players. British Journal of Sports Medicine 39, 860-865.
Journal of Sports Science and Medicine Cochrane D.J., Stannard S.R., Firth E.C., Rittweger J. (2010a) Acute whole-body vibration elicits post-activation potentiation. European Journal of Applied Physiology 108, 311-319.
Journal of Sports Science and Medicine Cochrane D.J., Stannard S.R., Firth E.C., Rittweger J. (2010b) Comparing muscle temperature during static and dynamic squatting with and without whole-body vibration. Clinical Physiology and Functional Imaging 30, 223-229.
Journal of Sports Science and Medicine De Gail P., Lance J.W., Neilson P.D. (1966) Differential effects on tonic and phasic reflex mechanisms produced by vibration of muscles in man. Journal of Neurology Neurosurgery and Psychiatry 29, 1-11.
Journal of Sports Science and Medicine Delecluse C., Roelants M., Verschueren S. (2003) Strength increase after whole-body vibration compared with resistance training. Medicine and Science in Sports and Exercise 35, 1033-1041.
Journal of Sports Science and Medicine Delwaide P.J., Toulouse P. (1980) Jendrassik maneuver vs controlled contractions conditioning the excitability of soleus mono-synaptic reflexes. Archives of Physical Medicine and Rehabilitation 61, 505-510.
Journal of Sports Science and Medicine Desmedt J.E., Godaux E. (1977) Ballistic contractions in man - characteristic recruitment pattern of single motor units of tibialis anterior muscle. Journal of Physiology-London 264, 673-693.
Journal of Sports Science and Medicine Desmedt J.E., Godaux E. (1978) Mechanism of the vibration paradox - excitatory and inhibitory effects of tendon vibration on single soleus muscle motor units in man. Journal of Physiology-London 285, 197-207.
Journal of Sports Science and Medicine Dowman R., Wolpaw J.R. (1988) Jendrassik maneuver facilitates soleus h-reflex without change in average soleus motoneuron pool membrane-potential. Experimental Neurology 101, 288-302.
Journal of Sports Science and Medicine Eklund G., Hagbarth K.E. (1965) Motor effects of vibratory muscle stimuli in man. Electroencephalography and Clinical Neurophysiology 19, 619-.
Journal of Sports Science and Medicine Eklund G., Hagbarth K.E. (1966) Normal variability of tonic vibration reflexes in man. Experimental Neurology 16, 80-92.
Journal of Sports Science and Medicine Ettema G.J.C., Huijing P.A. (1994) Frequency-response of rat gastrocnemius medialis in small amplitude vibrations. Journal of Biomechanics 27, 1015-1022.
Journal of Sports Science and Medicine Fling B.W., Christie A., Kamen G. (2009) Motor unit synchronization in fdi and biceps brachii muscles of strength-trained males. Journal of Electromyography and Kinesiology 19, 800-809.
Journal of Sports Science and Medicine Gabriel D.A., Kamen G., Frost G. (2006) Neural adaptations to resistive exercise: Mechanisms and recommendations for training practices. Sports Medicine 36, 133-139.
Journal of Sports Science and Medicine Gandevia S.C. (2001) Spinal and supraspinal factors in human muscle fatigue. Physiological Reviews 81, 1725-1789.
Journal of Sports Science and Medicine Gillies J.D., Lance J.W., Neilson P.D., Tassinar C.A. (1969) Presynaptic inhibition of monosynaptic reflex by vibration. Journal of Physiology-London 205, 329-339.
Journal of Sports Science and Medicine Griffin L., Garland S.J., Ivanova T., Gossen E.R. (2001) Muscle vibration sustains motor unit firing rate during submaximal isometric fatigue in humans. Journal of Physiology-London 535, 929-936.
Journal of Sports Science and Medicine Hagbarth K.E. (1967) Emg studies of stretch reflexes in man. Electroencephalography and Clinical Neurophysiology Suppl 25, 74-79.
Journal of Sports Science and Medicine Hagbarth K.E., Kunesch E.J., Nordin M., Schmidt R., Wallin E.U. (1986) Gamma-loop contributing to maximal voluntary contractions in man. Journal of Physiology-London 380, 575-591.
Journal of Sports Science and Medicine Hopkins J.T., Fredericks D., Guyon P.W., Parker S., Gage M., Feland J.B., Hunter I. (2008) Whole body vibration does not potentiate the stretch reflex. International Journal of Sports Medicine 30, 124-129.
Journal of Sports Science and Medicine Issurin V.B., Tenenbaum G. (1999) Acute and residual effects of vibratory stimulation on explosive strength in elite and amateur athletes. Journal of Sports Sciences 17, 177-182.
Journal of Sports Science and Medicine Jackson S.W., Turner D.L. (2003) Prolonged muscle vibration reduces maximal voluntary knee extension performance in both the ipsilateral and the contralateral limb in man. European Journal of Applied Physiology 88, 380-386.
Journal of Sports Science and Medicine Jendrassik E. (1885) Zur untersuchgamethode des kniephanomens. Neuroloogisches Centralblatt 4, 412-415.
Journal of Sports Science and Medicine Kamen G., Knight C.A. (2004) Training-related adaptations in motor unit discharge rate in young and older adults. Journals of Gerontology Series A-Biological Sciences and Medical Sciences 59, 1334-1338.
Journal of Sports Science and Medicine Kerschan-Schindl K., Grampp S., Henk C., Resch H., Preisinger E., Fialka-Moser V., Imhof H. (2001) Whole-body vibration exercise leads to alterations in muscle blood volume. Clinical Physiology 21, 377-382.
Journal of Sports Science and Medicine Kinser A.M., Ramsey M.W., O'Bryant H.S., Ayres C.A., Sands W.A., Stone M.H. (2008) Vibration and stretching effects on flexibility and explosive strength in young gymnasts. Medicine and Science in Sports and Exercise 40, 133-140.
Journal of Sports Science and Medicine Kossev A., Siggelkow S., Kapels H.H., Dengler R., Rollnik J.D. (2001) Crossed effects of muscle vibration on motor-evoked potentials. Clinical Neurophysiology 112, 453-456.
Journal of Sports Science and Medicine Kraemer W.J., Adams K., Cafarelli E., Dudley G.A., Dooly C., Feigenbaum M.S., Fleck S.J., Franklin B., Fry A.C., Hoffman J.R., Newton R.U., Potteiger J., Stone M.H., Ratamess N.A., Triplett-McBride T. (2002) Joint position statement: Progression models in resistance training for healthy adults. Medicine and Science in Sports and Exercise 34, 364-380.
Journal of Sports Science and Medicine Lance J.W., Degail P., Neilson P.D. (1966) Tonic and phasic spinal cord mechanisms in man. Journal of Neurology Neurosurgery and Psychiatry 29, 535-544.
Journal of Sports Science and Medicine Lewis G.N., Byblow W.D., Carson R.G. (2001) Phasic modulation of corticomotor excitability during passive movement of the upper limb: Effects of movement frequency and muscle specificity. Brain Research 900, 282-294.
Journal of Sports Science and Medicine Luo J., McNamara B., Moran K. (2005) The use of vibration training to enhance muscle strength and power. Sports Medicine 35, 23-41.
Journal of Sports Science and Medicine Macefield V.G., Gandevia S.C., Bigland-Ritchie B., Gorman R.B., Burke D. (1993) The firing rates of human motoneurons voluntarily activated in the absence of muscle afferent feedback. Journal of Physiology-London 471, 429-443.
Journal of Sports Science and Medicine Marsden C.D., Meadows J.C., Hodgson H.J.F. (1969) Observations on reflex response to muscle vibration in man and its voluntary control. Brain 92, 829-846.
Journal of Sports Science and Medicine Martin B.J., Park H.S. (1997) Analysis of the tonic vibration reflex: Influence of vibration variables on motor unit synchronization and fatigue. European Journal of Applied Physiology and Occupational Physiology 75, 504-511.
Journal of Sports Science and Medicine Matthews P.B. (1966) The reflex excitation of the soleus muscle of the decerebrate cat caused by vibration applied to its tendon. Journal of Physiology-London 184, 450-472.
Journal of Sports Science and Medicine Melnyk M., Kofler B., Faist M., Hodapp M., Gollhofer A. (2008) Effect of a whole-body vibration session on knee stability. International Journal of Sports Medicine 29, 839-844.
Journal of Sports Science and Medicine Mester J., Kleinoder H., Yue Z. (2006) Vibration training: Benefits and risks. Journal of Biomechanics 39, 1056-1065.
Journal of Sports Science and Medicine Mileva K.N., Bowtell J.L., Kossev A.R. (2009) Effects of low-frequency whole-body vibration on motor-evoked potentials in healthy men. Experimental Physiology 94, 103-116.
Journal of Sports Science and Medicine Milner-Brown H.S., Stein R.B., Lee R.G. (1975) Synchronization of human motor units: Possible roles of exercise and supraspinal reflexes. Electroencephalography and Clinical Neurophysiology 38, 245-254.
Journal of Sports Science and Medicine Mischi M., Cardinale M. (2009) The effects of a 28-hz vibration on arm muscle activity during isometric exercise. Medicine and Science in Sports and Exercise 41, 645-652.
Journal of Sports Science and Medicine Moran K., McNamara B., Luo J. (2007) Effect of vibration training in maximal effort (70% 1RM) dynamic bicep curls. Medicine and Science in Sports and Exercise 39, 526-533.
Journal of Sports Science and Medicine Munte T.F., Jobges E.M., Wieringa B.M., Klein S., Schubert M., Johannes S., Dengler R. (1996) Human evoked potentials to long duration vibratory stimuli: Role of muscle afferents. Neuroscience Letters 216, 163-166.
Journal of Sports Science and Medicine Nigg B.M. (1997) Impact forces in running. Current Opinion in Orthopedics 8, 43-47.
Journal of Sports Science and Medicine Nishihira Y., Iwaski T., Hatta A., Wasaka T., Kanada T., Kuroiwa K., Akiyawa S., Kida T., Ryol K. (2002) Effect of whole body vibration stimulus and voluntary contraction on motoneuron pool. Advances in Exercise and Sports Physiology 8, 83-86.
Journal of Sports Science and Medicine Nordlund M.M., Thorstensson A. (2007) Strength training effects of whole-body vibration?. Scandinavian Journal of Medicine and Science in Sports 17, 12-17.
Journal of Sports Science and Medicine Patten C., Kamen G., Rowland D.M. (2001) Adaptations in maximal motor unit discharge rate to strength training in young and older adults. Muscle and Nerve 24, 542-550.
Journal of Sports Science and Medicine Rauch F., Sievanen H., Boonen S., Cardinale M., Degens H., Felsenberg D., Roth J., Schoenau E., Verschueren S., Rittweger J. (2010) Reporting whole-body vibration intervention studies: Recommendations of the international society of musculoskeletal and neuronal interactions. Journal of Musculoskeletal and Neuronal Interactions 10, 193-198.
Journal of Sports Science and Medicine Ribot-Ciscar E., Rossi-Durand C., Roll J.P. (1998) Muscle spindle activity following muscle tendon vibration in man. Neuroscience Letters 258, 147-150.
Journal of Sports Science and Medicine Rittweger J. (2010) Vibration as an exercise modality: How it may work, and what its potential might be. European Journal of Applied Physiology 108, 877-904.
Journal of Sports Science and Medicine Rittweger J., Mutschelknauss M., Felsenberg D. (2003) Acute changes in neuromuscular excitability after exhaustive whole body vibration exercise as compared to exhaustion by squatting exercise. Clinical Physiology and Functional Imaging 23, 81-86.
Journal of Sports Science and Medicine Rittweger J., Schiessl H., Felsenberg D. (2001) Oxygen uptake during whole-body vibration exercise: Comparison with squatting as a slow voluntary movement. European Journal of Applied Physiology 86, 169-173.
Journal of Sports Science and Medicine Ritzmann R., Kramer A., Gruber M., Gollhofer A., Taube W. (2010) EMG activity during whole body vibration: Motion artifacts or stretch reflexes?. European Journal of Applied Physiology 110, 143-151.
Journal of Sports Science and Medicine Roll J.P., Vedel J.P., Ribot E. (1989) Alteration of proprioceptive messages induced by tendon vibration in man - a microneurographic study. Experimental Brain Research 76, 213-222.
Journal of Sports Science and Medicine Romaiguere P., Vedel J.P., Azulay J.P., Pagni S. (1991) Differential activation of motor units in the wrist extensor muscles during the tonic vibration reflex in man. Journal of Physiology-London 444, 645-667.
Journal of Sports Science and Medicine Rothmuller C., Cafarelli E. (1995) Effect of vibration on antagonist muscle coactivation during progressive fatigue in humans. Journal of Physiology-London 485, 857-864.
Journal of Sports Science and Medicine Sale D.G. (1988) Neural adaptation to resistance training. Medicine and Science in Sports and Exercise 20, S135-S145.
Journal of Sports Science and Medicine Sale D.G., Komi P.V. (2003) Strength and power in sport. Neural adaptations to strength training. Oxford. Blackwell Science.
Journal of Sports Science and Medicine Sands W.A., McNeal J.R., Stone M.H., Haff G.G. (2008) Effect of vibration on forward split flexibility and pain perception in young male gymnasts. International Journal of Sports Physiology and Performance 3, 469-481.
Journal of Sports Science and Medicine Sands W.A., McNeal J.R., Stone M.H., Russell E.M., Jemni M. (2006) Flexibility enhancement with vibration: Acute and long-term. Medicine and Science in Sports and Exercise 38, 720-725.
Journal of Sports Science and Medicine Semmler J.G. (2002) Reviews.
Journal of Sports Science and Medicine Semmler J.G., Nordstrom M.A. (1998) Motor unit discharge and force tremor in skill- and strength-trained individuals. Experimental Brain Research 119, 27-38.
Journal of Sports Science and Medicine Staron R.S., Karapondo D.L., Kraemer W.J., Fry A.C., Gordon S.E., Falkel J.E., Hagerman F.C., Hikida R.S. (1994) Skeletal-muscle adaptations during early phase of heavy-resistance training in men and women. Journal of Applied Physiology 76, 1247-1255.
Journal of Sports Science and Medicine Stewart J.A., Cochrane D.J., Morton R.H. (2009) Differential effects of whole body vibration durations on knee extensor strength. Journal of Science and Medicine in Sport 12, 50-53.
Journal of Sports Science and Medicine Torvinen S., Kannus P., Sievanen H., Jarvinen T.A.H., Pasanen M., Kontulainen S., Jarvinen T.L.N., Jarvinen M., Oja P., Vuori I. (2002) Effect of a vibration exposure on muscular performance and body balance. Randomized cross-over study. Clinical Physiology and Functional Imaging 22, 145-152.
Journal of Sports Science and Medicine Tyler A.E., Hutton R.S. (1986) Was Sherrington right about co-contractions. Brain Research 370, 171-175.
Journal of Sports Science and Medicine Wakeling J.M., Nigg B.M. (2001) Modification of soft tissue vibrations in the leg by muscular activity. Journal of Applied Physiology 90, 412-420.
Journal of Sports Science and Medicine Wakeling J.M., Nigg B.M., Rozitis A.I. (2002) Muscle activity damps the soft tissue resonance that occurs in response to pulsed and continuous vibrations. Journal of Applied Physiology 93, 1093-1103.
Journal of Sports Science and Medicine Warman G., Humphries B., Purton J. (2002) The effects of timing and application of vibration on muscular contractions. Aviation Space and Environmental Medicine 73, 119-127.
Journal of Sports Science and Medicine Wiesendanger M., Miles T.S. (1982) Ascending pathway of low-threshold muscle afferents to the cerebral-cortex and its possible role in motor control. Physiological Reviews 62, 1234-1270.
Journal of Sports Science and Medicine Yao W.X., Fuglevand A.J., Enoka R.M. (2000) Motor-unit synchronization increases emg amplitude and decreases force steadiness of simulated contractions. Journal of Neurophysiology 83, 441-452.
Journal of Sports Science and Medicine Yue G., Fuglevand A.J., Nordstrom M.A., Enoka R.M. (1995) Limitations of the surface electromyography technique for estimating motor unit synchronization. Biological Cybernetics 73, 223-233.
 
 
 
Home Issues About Authors
Contact Current Editorial board Authors instructions
Email alerts In Press Mission For Reviewers
Archive Scope
Supplements Statistics
Most Read Articles
  Most Cited Articles
 
  
 
JSSM | Copyright 2001-2020 | All rights reserved. | LEGAL NOTICES | Publisher

It is forbidden the total or partial reproduction of this web site and the published materials, the treatment of its database, any kind of transition and for any means, either electronic, mechanic or other methods, without the previous written permission of the JSSM.

This work is licensed under a Creative Commons License Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.