Contractile characteristics of electrically evoked knee extensions
The rate at which muscle force develops during a fast voluntary contraction is influenced by both peripheral factors and neural activation properties. In order to separate these influences, the contractile response of the knee extensor group was also assessed by means of percutaneous sub-maximal muscle stimulation. This is a reliable method, which has been used to assess intrinsic muscle characteristics in various human populations (Binder-Macleod et al.
1995; de Haan et al.
2000; Gerrits et al.
2001; Harridge et al.
1996). Although it is not possible to assess the specific characteristics of the portion of the muscle fibre population that is recruited during the sub-maximal stimulation procedure of the present study, the activation of about 40% of the muscle fibres suffices to represent the global contractile characteristics of the quadriceps muscle. Previous studies have shown that the torque frequency relationship, as well as the contractile properties of the twitch are not intrinsically influenced by the absolute force level, provided that a force between 20 and 50% MVC is reached during maximal tetanic stimulation (Binder-Macleod et al.
1995).
In the absence of the exercise countermeasure, the knee extensors exhibited characteristics of a faster muscle following 56 days of bed rest. The degree of fusion at 10 Hz stimulation was decreased, the time to reach peak torque at 300 Hz stimulation was reduced and relaxation after tetanic stimulation at 150 Hz tended to be faster. The possibility of an error seems unlikely, since we found complementary changes towards enhanced contractile speed at all frequencies studied. In addition, these changes were observed only for the inactive control group.
The stiffness of the series elastic component is amongst the factors known to affect the rate of torque development (Bojsen-Moller et al.
2005). Although not measured in the present study, from previous other studies it appears that with muscle unloading tendon stiffness often decreases (Kubo et al.
2000; Reeves et al.
2005). This would tend to result in a reduced rate of torque development of the whole muscle–tendon complex, opposite to what we observed. The increased rate of torque development, as well as the tendency towards a faster rate of relaxation in the present study could, however, be explained by an elevated rate of cross-bridge cycling (Unsworth et al.
1982). Although at odds with some previous findings (e.g., Davies et al.
1987; Gondin et al.
2004; Narici et al.
2003) such interpretation would be consistent with documented elevations in maximal unloaded shortening velocity (Caiozzo et al.
1994; Widrick et al.
2001; Yamashita-Goto et al.
2001) potentially linked to shifts in muscle fibre phenotype from slow to fast as a direct consequence of muscle unloading (Fitts et al.
2000; Gerrits et al.
2003; Ohira et al.
1999; Talmadge
2000; Trappe et al.
2004). Because the assessed muscle torque in the present study is the resultant of the entire muscle–tendon complex, and given a likely increase in tendon compliance by bed rest, the observed enhanced contractile speed characteristics, might even underestimate the underlying intrinsic changes in the present study.
Despite faster contractile properties, torque production at 10 Hz stimulation relative to maximal tetanic stimulation was increased after bed rest. Although consistent with previous research (Seki et al.
2001), the higher relative torque responses at low frequency stimulation did not result from a significant enhancement of twitch summation, as previously opted (Gondin et al.
2004). In contrast, the level of force fusion substantially decreased during bed rest period in the present study. At present, the exact processes responsible for these anomalous findings remain unclear, but a similar phenomenon was reported in the paralyzed muscles of individuals with spinal cord injury (Gerrits et al.
1999), which may be considered as an extreme model for muscle unloading.
In part, our data supports the hypothesis postulated by Rittweger et al. (
2006) that the large number of contraction–relaxation cycles during resistive vibration exercise (Blottner et al.
2006) may be effective in preserving muscle fibre contractile properties. Indeed, no changes in time to reach peak torque at 300 Hz stimulation, the rate of relaxation after tetanic stimulation at 150 Hz, or the level of force fusion at low stimulation frequency (i.e., the FOA) were observed in the exercise trained subjects. The significant difference between some baseline values, e.g., FOA and
T
10/
T
150 ratio (Fig.
4a, d), and the tendencies for TPT
300 (
P = 0.098) and HRT
150 (
P = 0.057) to be lower in RVE compared to Ctrl at baseline deserves attention, since it may point towards a difference between groups with respect to muscle fibre type at the start of the study, with RVE exhibiting a faster muscle. Nonetheless, at least for the FOA it has been demonstrated that it is still much higher (i.e., 0.65 in Gerrits et al.
1999) in paralyzed muscles of people with spinal cord injury. This makes it unlikely that the preservation of FOA in the present study resulted from a ceiling effect for RVE.
Despite the observation that speed characteristics were unaltered for the exercise-trained group, the relative peak torque at low stimulation frequency also increased for this group. As the level of force fusion remained unaltered during bed rest for RVE, other factors are likely involved. Once possibility is that the peak torque during 10 Hz stimulation increased as a consequence of an enlarged twitch response. Although not directly measured in the present study, the torque developed during the first response of the 10 Hz tetanus increased during the course of the bed rest by about 26%, which was comparable to the elevation in 10 Hz peak torque (∼40%) for RVE. Interestingly, the relative torque production of the first response of the 10 Hz contraction also increased (by about 30%) for the inactive control group. However, the reduced fusion of successive individual twitches diminished the increase in peak torque at 10 Hz stimulation to about 15%. Despite the differences in contractile speed characteristics, the percent change in 10 Hz peak torque after 56 days of bed rest was not different between groups. At present, the selectivity of the exercise countermeasure paradigm to prevent changes in contractile speed properties, but not in the torque response at low frequencies of stimulation, remains difficult to explain. Indeed, more research is needed to determine the effectiveness of resistive vibration exercise as a countermeasure, since the individual merits of resistance training versus vibration training could not be quantified in the present study.
Fast voluntary isometric knee extensions at maximal effort
Adequate preservation of the rate at which muscle torque develops during a forceful volitional contraction is imperative for astronauts, as neuromuscular deconditioning, coupled to a weakened load-bearing skeleton, increases the risk of fall-related bone fractures after prolonged space missions. To add to the concern, compared to steady-state contractions, much higher levels of neural activation are needed for contractions where torque develops as rapidly as possible (de Haan
1998; de Ruiter et al.
1999). As such, we hypothesised that the ability to perform fast and forceful voluntary contractions would be more deteriorated by bed rest confinement than the ability to perform maximal steady-state contractions. Surprisingly, and at odds with the finding of others (di Prampero and Narici
2003; Koryak
1998), we found no evidence for such bed rest induced functional impairment in either group (Fig.
3).
For the same inactive control subjects as used in the present study, we previously reported an absence of neural deconditioning for maximal voluntary steady-state contractions, whether examined by the twitch interpolation technique, or by the assessment of electromyographic activity of the quadriceps femoris muscle (Mulder et al.
2006,
2007). We concluded that the preservation of neural activation of this specific motor task was likely associated with the repeated functional retesting sequence employed during bed rest. The observation that the percent reduction in maximal isometric knee extension strength of the left leg, which was not repeatedly retested during bed rest, exceeded the level of atrophy by a factor of two after 8 weeks of bed rest, strengthened this notion (Mulder et al.
2006). Based on the findings of the present study, we are inclined to suggest that the repeated retesting regime also served as a contributory factor in maintaining neural activation during fast isometric knee extensions. Although such an effect was not intended at the time, this supposition is important since it suggests that neural activation of different isometric motor tasks can be maintained during bed rest without rigorous exercise training regimes.
In part, the absence of loss of muscle functionality following bed rest might have resulted from changes in the contractile properties of unloaded muscles. Widrick et al. (
1998) reported significant atrophy of single human soleus muscle fibres after 17 days of spaceflight. Absolute peak power of these fibres was, however, partly or fully preserved by an elevated contraction velocity. In the present study, the examined muscle group in the inactive control group also acquired mechanical characteristics of a faster muscle during the course of the bed rest. As selective neural deconditioning could not be demonstrated for the fast voluntary contractions, the expectation might arise of an increased rate of voluntary torque development for the inactive control group. Such a systematic change was not observed. Although it seems difficult to explain this absence based on the changes in intrinsic contractile characteristics, it is clear that neural activation and the subsequent mechanical response during voluntary contractions are much more variable than the activation and response when contractions are electrically evoked. To overcome this variability, larger alterations than those observed in intrinsic contractile characteristics would have been required to allow for detectable changes for the fast voluntary isometric actions.
Interestingly, an increase in the rate of torque development could have also been expected for the exercise trained RVE group. For this group we previously found that the amplitude of the surface EMG during the maximal steady-state contractions was substantially increased at the end of bed rest (by ∼30%; Mulder et al.
2007). The latter was suggested to result from an increase in the mean motor unit firing rate, due to a change in the excitability of the alpha motoneurons (Mulder et al.
2007). Such modulation has been associated with increased rate of force development after resistance training (Holtermann et al.
2007). However, in the present study the neural activation during the fast voluntary contractions and the subsequent initial rate of torque development remained unaltered for the exercise trained group. The current exercise-training regime consisted mainly of relatively slow dynamic loaded contractions while vibration was simultaneously applied to the feet. Such a motor task is quite different from the isometric contractions performed during the testing of the subjects. Based on the selectivity of training, and the fact that the number of exercise training sessions by far outweighed the number of testing sessions (89 vs. 7), it is likely that neural activation strategies employed by the subjects were more guided towards optimal performance during the training sessions, than optimal performance during the fast voluntary isometric actions during testing.
In conclusion, in the subjects who were confined to 8 weeks of bed rest without preventive measures the knee extensor muscle group acquired intrinsic contractile properties of a faster muscle. Resistive vibration exercise proved effective to counteract these changes at the muscle level. An unexpected finding of the present study was that neither group showed deterioration in the capacity to maximally activate the knee extensors at the very start of a voluntary contraction performed as fast and forcefully as possible. For the RVE group this might indicate an effective countermeasure design. However, considering that neural activation and voluntary muscle function were also maintained in the Ctrl group, it is also conceivable that the multiple retesting of the subjects resulted in or at least contributed to these preservations.