This is the first study that demonstrated an increase in synergistic EMG activity during maximal voluntary isometric contractions following NMES of one muscle. Due to the NMES of the GL, the EMG activity decreased to 81% in posttest. This decline was compensated by the EMG activity of SOL that increased to 112% in posttest. The force during MVC did not change significantly after NMES of the GL (D).
Following sustained NMES of the GL, voluntary GL muscle activity during maximal isometric contractions was reduced (A). The results are in line with other studies that found decreased EMG amplitudes after high-frequency NMES (Boerio et al. 2005
). The decline in EMG activity occurs due to failure of electrical propagation at the muscle fiber membrane of the GL induced by high-frequency fatigue (Cairns and Dulhunty 1995
; Badier et al. 1999
). Furthermore, studies using the interpolation twitch technique showed that electrical stimulation of the triceps surae lead to central fatigue (Boerio et al. 2005
) accompanied by a force decline. In our studies, the force did not change significantly (P
= 0.388) after NMES of the GL. For that reason, we assume that the decline in GL in the presented study occurred more prominently due to peripheral fatigue than due to central fatigue (Badier et al. 1999
Reducing knee angle leads to reduced GM length and decreased muscle activation during MVC (Cresswell et al. 1995
; Arampatzis et al. 2006
). This may be due to (1) the “drive,” i.e., the neural outflow from spinal motor neurons, may be reduced to a shortened muscle; (2) neuromuscular transmission–propagation in a shortened muscle may be impaired, and (3) shortening a muscle may alter the electrode configuration with respect to the recording volume, thereby resulting in less myoelectric activity recorded (Cresswell et al. 1995
In our experiments, knee and ankle angle and therefore the muscle length were kept constant during pre- and posttests. However, tendon length may increase during repeated high efforts (Kubo et al. 2001
). This would lead to shorter fascicles and therefore decreased muscle activations in all muscles of the m. triceps surae. However, we found only decreased muscle activation in GL but not in GM and even increased muscle activation in SOL.
As the GL activity decreased due to fatigue, compensatory strategies exist to produce the same force during the MVC. Those strategies were found in higher activation of synergistic muscle SOL in particular. Akima et al. (2002
) found increased activations of the m. rectus femoris, m. vastus medialis, and m. vastus intermedius in voluntary dynamic knee extension at 50% of MVC after NMES of the m. vastus lateralis. Similarly, our results show increased activity in the SOL (C). Contrary to Akima et al. (2002
), we used maximal isometric plantar flexions and examined the muscle activity in SOL, GM, and GL after NMES of GL.
There are several reasons why activity of synergistic unfatigued muscles is increased due to selective fatigue of the GL. It is possible that increased afferent drive increase the central activation at least in the SOL and GM. It is known that NMES, as we used in our experiment, provokes spinal contributions via afferent drives (Gondin et al. 2006
) and increases the excitability of spinal reflexes (Trimble and Harp 1998
; Kitago et al. 2004
). The increased spinal reflex excitability can be sustained for 16 min (Kitago et al. 2004
) after stimulation. Furthermore, Ia fibers of the GL are cross-linked to the α motoneurons of the GM and SOL (Nichols 1999
). From animal experiments, it is known that spinal cross-linkages between GL and SOL are strong, while they are weaker between GL and GM (Eccles et al. 1957
; Nichols 1989
). The muscle spindles are activated during MVC (Hagbarth et al. 1986
) and contribute to the voluntary force production up to 30% (Gandevia et al. 1990
). Considering the aforementioned facts, it is possible that in our experiments the NMES of the GL provoked a latent higher excitability of the spinal reflexes. The consequence would be higher muscle activity in SOL and comparably low increase in GM muscle activation during MVC. This explanation is based on several assumptions, which we did not measure directly. Therefore, it is hypothetical and needs to be proved in further studies.
NMES also affects supraspinal areas (Maffiuletti 2010
). Using magnetic resonance imaging Smith et al. (2003
) found, the higher the current intensity the greater the response of different brain areas. Furthermore, Mang et al. (2010
) stimulated the peroneal nerve with transcranial magnetic stimulation at different frequencies (20, 50, 100, 200 Hz) and measured increased corticospinal excitability. Corticospinal pathways were solely increased after high-frequency stimulation at 50 and 100 Hz and lasted for 24 min. This increased corticospinal excitability may also contribute to the EMG activity in the m. triceps surae.
At the peripheral level, increased EMG activity can result from decrease in muscle fiber conduction velocity (Rongen et al. 2002
). Rongen et al. (2002
) showed that the EMG amplitude increased whereas the muscle fiber conduction velocity decreased during sustained isometric contractions under ischemic conditions. During high-frequency NMES, muscle metabolism is highly utilized (Shenton et al. 1986
) and the muscle pH decreased (Vanderthommen et al. 2003
). For that reason, it is possible that changes of the muscle fiber conduction velocity can occur, but only in the stimulated GL. That does not explain the increased activity in SOL.
Our results indicated different activation strategies in synergistic muscles (SOL, GM). According to the results of Akima et al. (2002
) and de Ruiter et al. (2008
), it was hypothesized that EMG activity of both synergistic muscles would increase. On the other hand, Sacco et al. (1997
) reported decreased EMG activity in GM after NMES of GL. However, this decline in EMG activity is attributed to the ischemia conditions in their study. In our study, it is assumed that EMG activity of GM was affected by the NMES of the neighboring GL (Adams et al. 1993
). This might induce an unaltered EMG activity in GM (P
= 1.00) during NMES. Furthermore, in recovery, EMG activity of GM increased slightly compared with the baseline. The high correlations (r
= 0.847, P
< 0.01) between GM and GL during recovery support this assumption.
During recovery, the activation of the GL goes back to baseline values. The muscle activation of GM is unaltered and muscle activation of SOL is still increased. Therefore, one would expect significant increase of force. In fact, force does not increase significantly. This might be due to metabolic fatigue in the stimulated GL (Shenton et al. 1986
; Vanderthommen et al. 2003
In fact, EMG activity in the SOL increased after NMES of the GL at high frequencies, but not EMG activity of GM. Further studies are needed to clarify whether EMG activity of the synergistic muscles results from peripheral changes or improved central activations.
In conclusion, a progressive fatigue protocol of the GL by means of NMES resulted in (a) unaltered force during maximal voluntary isometric plantar flexions, (b) increased synergistic muscle activity of the SOL. It is suggested that these compensatory effects are caused by central contributions induced by NMES. The results provide new insights in neuromuscular control of synergist muscles.