Introduction
In an exercise inducing muscle damage, inadequate neural drive can be an attempt of the neuromuscular system to protect the muscle-tendon unit from additional damage (Strojnik and Komi
2000; Nicol et al.
2006). This inadequate neural drive could be the result from a combination of three factors: the conscious and unconscious will of the subject to reduce the exercise intensity; an inability of the motor cortex to generate sufficient output to maximally activate the muscle; and/or a decreased transmission of the supraspinal input to the muscle by the spinal motor axons.
A decrement in H-reflex amplitude has been observed immediately after an exhausting voluntary contraction of a single muscle group (i.e., Duchateau et al.
2002; Garland and McComas
1990; Kuchinad et al.
2004). It has been proposed that this decline in the transmission of the action potentials from the Ia afferent to the α-motoneuron may be a consequence of a presynaptic inhibition mediated by group III and IV afferents (Bigland-Ritchie et al.
1986; Duchateau et al.
2002; Garland and McComas
1990; Garland
1991; Woods et al.
1987) induced by muscle damage (Avela et al.
2006). Furthermore, increased group III and IV muscle afferent inputs could induce H-reflex depression when muscle soreness progresses as muscle pain is believed to reflect activity in group III and IV muscle afferents (O’Connor and Cook
1999). But only a few studies have observed a decrease in H-reflex amplitude after exercise of multiple muscle groups as occurs for example in running (Avela et al.
1999; Bulbulian and Bowles
1992; Racinais et al.
2007b) raising the question of whether spinal modulation occurs after whole body exercise. Recently it has been shown that walking backward induces muscle soreness in the muscles of the lower limb (Nottle and Nosaka
2005). Accordingly, this exercise model allows the study of the effects of muscle soreness on alteration in neural drive. Thus the goal of this study was to determine whether the impaired exercise performance of muscles with delayed onset muscle soreness (DOMS) is due to an alteration in neural drive related to spinal modulation.
Discussion
The downhill walking exercise induced a significant decrease in the MVT of the plantar flexor muscles. Immediately after the walking exercise, the torque decrement of −15% (Fig.
2a) appeared to be caused partly by an alteration in muscle contractile properties (i.e., −23% for Pt, Fig.
2c). This alteration is typically referred to as “peripheral fatigue” [for a review, see Millet and Lepers
2004]. Furthermore, this peripheral fatigue was also associated with a decrease in VA (i.e., −5.3%, Fig.
2b) suggesting the concomitant existence of a “central modulation” [for a review, see Gandevia
2001]. The first finding of this study is that the maximum voluntary torque failed to recover before the third day (i.e., −12% and −10% after 24-h and 48-h of recovery, respectively, Fig.
2a) whereas the measure of the (peripheral) contractile properties had recovered significantly within the first 24 h after exercise (
P < 0.01, Fig.
2c). This delayed recovery in MVT appeared to be mainly associated with a decrease in voluntary muscle activation (Fig.
2b). The time course of change in VA presents similarities with the time course of torque changes.
A significant decrease in the VA reaching the muscle has previously been observed after prolonged (Millet et al.
2002,
2003) and short-duration (Racinais et al.
2007a) fatiguing exercise, but our data showed that a backward downhill walking exercise did produce a decrease in muscle activation persisting for a few days after the exercise. It has been suggested that this central component could explain as well the reduction in force production by the respiratory muscles after heavy exercise (Verin et al.
2004) and represents a protective mechanism in order that peripheral muscle fatigue does not exceed a critical threshold (Amann et al.
2006). This central protection of the muscle from further peripheral fatigue and damage will be performed at the expense of a truly maximal performance in which all the motor units are activated (Gandevia et al.
1996).
It has recently been suggested that a “central governor” in the brain regulates the extent of skeletal muscle recruitment during exercise (Noakes et al.
2005). According to this theory, the sensation of fatigue is the conscious interpretation of these homoeostatic control mechanisms during prolonged exercise (Noakes et al.
2005). Our results could partly support this theory but with the proviso that the modulation of central activation in this experiment appears to be related not only to fatigue immediately after exercise but also to the development of DOMS the days following the exercise. However, regulation of muscle recruitment by the brain (i.e., supraspinal regulation) is not the only system that could explain the observed decrease in skeletal muscle activation since reflex pathways need also to be considered (i.e., spinal modulation). Previous results showed impairment in VA after eccentric exercise when VA was estimated by nerve stimulation but not by cortical stimulation (Prasartwuth et al.
2005). That suggests that the VA deficit lies within these two site of stimulations, i.e., in the motor cortex or at spinal level (Prasartwuth et al.
2005), rather than a governor upstream to the motor cortex.
In the present study, we used H-reflex amplitude as a tool to evaluate the spinal modulation (Aagaard et al.
2002; Schieppati
1987) to provide a differentiation within these possible regulatory mechanisms. The DOMS produced by our experimental protocol would have induced an increased discharge of group III and IV muscle afferents (Avela et al.
1999) and thus a pre-synaptic inhibition of the transmission from the Ia afferent stimulation to the α-motoneurons (Avela et al.
2006; Bigland-Ritchie et al.
1986; Duchateau et al.
2002; Garland and McComas
1990; Garland
1991; Woods et al.
1987). The extent to which this inhibition occurs will depend on whether the input producing the inhibition is ongoing or has ceased. But, in theory, increased group III and IV muscle afferent input induced by the DOMS should induce H-reflex depression as the soreness progresses. Indeed, muscle pain is believed to reflect activity in group III and IV muscle afferents (O’Connor and Cook
1999). However, our results failed to show significant variations in the evoked reflex-wave amplitudes throughout the experiment (i.e.,
H
max/
M
max and
H
sup/
M
sup ratios) suggesting that the motoneuron pool excitability was well preserved.
A number of previous studies have demonstrated a significant H-reflex decrease in the exercised muscle group after an exhausting voluntary contraction of that muscle group (i.e., Duchateau et al.
2002; Garland and McComas
1990; Kuchinad et al.
2004). But only a few studies have observed this decrease after more generalized muscular exercise such as running, (Avela et al.
1999; Bulbulian and Bowles
1992; Racinais et al.
2007b). Our results support these findings by showing that after a 30-min downhill walking exercise, electrically evoked reflex-wave activity was not decreased. Thus we conclude that non-exhausting walking exercise, sufficient to induce significant DOMS seems not to induce alteration of the spinal modulation.
Since the persistence of a decrease in VA during several days in this study could not be explained by spinal modulation, it seems likely that a supraspinal component must have played a part. Accordingly the changes in VA that occurred at the same time that the subjective symptoms of DOMS suggest a supraspinal regulation of muscle recruitment. Indeed it has been known for some time that exercise performance is regulated at least in part by supraspinal factors. For example, Bigland-Ritchie (
1981) showed that central fatigue during repeated isometric contraction is minimized by exhorting the subject to produce a “super” effort at the end of each voluntary contraction. Our results add to that interpretation by suggesting the possibility that supraspinal modulation can also occurs after locomotory activity such as walking, even without exhaustion.
As we have already argued, the observed increase in DOMS could represent the conscious interpretation of an increased discharge of group III and IV muscle afferents (O’Connor and Cook
1999). Even though we failed to observe a significant alteration of the spinal modulation at the time of increased muscle soreness, this would not prove that the discharge of these afferents had not increased since it is still unclear whether group III and IV muscle afferents induce a post-exercise decrease in motoneurons excitability in healthy humans. Indeed, previous studies have shown that maintained firing of ischaemically sensitive group III and IV muscle afferents does not influence the altered muscle responses to cortical or corticospinal stimulation observed after fatiguing exercise (Andersen et al.
2003; Gandevia et al.
1996; Taylor et al.
2000). All these findings might suggest that, after exercise, increased output from group III and IV muscle afferents may not directly inhibit the motoneurons but may act upstream of the motor cortex to impair voluntary descending motor drive (Taylor et al.
2006).
Accordingly, a novel contribution of this study is that VA significantly recovered on the third day, when the DOMS displayed also a significant decrement (
F
1,9 > 12,
P < 0.01, for the both scales). Although this temporal relationship does not prove causality, this finding could suggest a relationship between the persistence of the decrease in VA and the subjective symptoms of DOMS in these subjects. This observation is consistent with the data of Le Pera et al. (
2001) showing that muscle pain could induce a long-lasting depression in motor activation. Their data suggest that this inhibition in motor system excitability could be linked to a decreased excitability of the motor cortex as well as spinal modulation (Le Pera et al.
2001). However, Prasartwuth et al. (
2005) observed a different time course in muscle soreness after eccentric exercise and changes in VA leading these authors to suggest that muscle pain did not directly cause the change in voluntary drive.
These different data emphasised the complexity of the relation within muscle soreness and voluntary muscle drive. It has been recently observed that motoneuron excitability in elbow flexors, but not extensors, was able to recover when ischemia is maintained after fatiguing contractions (Martin et al.
2006), a finding that suggests differential influences of group III and IV muscle afferents on different motoneuron pools (Martin et al.
2006). In this study concerning the plantar flexors, we observed some statistical similarities within DOMS and VA (i.e., lowest value of VA at 48-h when DOMS was the highest and significant recovery for the both at 72-h). However, from a functional point of view, VA returned at control level at 72-h whereas DOMS at 72-h was not less than DOMS at 24-h, and VA decreased after exercise when DOMS was weak. That suggests that subjective DOMS of the plantar flexors can not be considered as an objective indicator of VA capability.