EKBLOM, MARIA M. NORDLUND; THORSTENSSON, ALF
Muscle strength is dependent on a person's ability to voluntarily activate the muscles. This ability has been shown to vary between individuals, muscle groups, muscle action types and tasks (1,9,22,38). Several studies have demonstrated that neural activation is lower during maximal voluntary lengthening (eccentric) compared with shortening (concentric) and isometric muscle actions, despite a similar or higher strength output (14,15,38). Action-type-specific activation of a muscle could be caused by variations in net excitation from Ia-afferents, Ib-afferents, and/or corticospinal drive to the motoneuron pool. In this study, an attempt is made to investigate possible action-type-specific contribution of Ia-afferent input to maximal voluntary dynamic actions. During passive as well as active muscle lengthening, muscle spindles are known to fire at a high frequency, which accentuates with higher lengthening velocity (5,21,39). At the same time, the Ia-afferents are exposed to extensive presynaptic inhibition (13,28). During passive muscle shortening, the muscle spindles fall silent, and there seems to be very little presynaptic inhibition (5,23). During active shortening, on the other hand, the firing frequency of Ia-afferents is increased in a phase-, velocity-, and exerted force-dependent manner. With an acceleration in shortening, such as in the early phase of a shortening action, the Ia-afferents typically fall silent, but in slow velocity actions with high forces, the Ia-afferent firing is substantially increased and so is the amount of presynaptic inhibition (5,23,25). Because both muscle spindle firing and presynaptic inhibition of Ia-afferents are present in shortening as well as in lengthening muscle actions, the net contribution of Ia-afferents to neural activation during the two dynamicmuscle action types is unclear. During maximal voluntary isometric muscle actions, indirect evidence of significant net contribution from Ia-afferent input has been presented. Prolonged vibration was shown to cause a decrease in H-reflex amplitude, indicative of a decrease in Ia-afferent efficacy, and a concomitant decrease in activation and strength of the muscles (2,35,37). The hypothesis of this study was that Ia-afferents contribute significantly to muscle strength and activation during both maximal voluntary lengthening and shortening actions, but to a higher degree in lengthening. The aim of the current study was to investigate how prolonged vibration affected muscle activation and strength in maximal voluntary shortening and lengthening plantar flexor muscle actions.
Eight healthy, recreationally active, female subjects provided their informed written consent to participate in the study. Their mean ± SD for age was 23 ± 2 yr, that for height was 1.71 ± 0.02 m, and that for body mass was 65 ± 12 kg. The study was approved by the local ethics committee and performed in accordance with the Declaration of Helsinki.
Initially, subjects participated in three separate sessions to familiarize themselves to the experimental protocol. After finding an individually adjusted test position, each subject was given 10 practice trials, that is, 5 submaximal and 5 maximal voluntary shortening and lengthening plantar flexor actions at 20°·s−1 through a 40° range of motion. One week after the last familiarization session, the subjects underwent two main experiments (interventions), vibration and control, separated by at least 1 wk. The order of the two main experiments was randomized between subjects. In the vibration experiment, 30 min of vibration of the Achilles tendon was applied, and in the control experiment, vibration was substituted by 30 min of rest. Maximal voluntary shortening and lengthening plantar flexor strength was measured before and after the vibration and rest, respectively, and Hoffman reflexes (H-reflexes) and M-waves were elicited before each set of strength tests. All postmeasurements were completed within 5 min from the cessation of vibration or rest.
Subjects were lying prone with knees straight and their right foot firmly attached to a metal plate mounted to an isokinetic dynamometer (IsoMed 2000; D. & R. Ferstl GmbH, Hemau, Germany). The foot placement was adjusted so that the ankle joint was aligned with the axis of the torque motor. Shoulder pads and a broad Velcro strap over the right thigh of the subject were applied to prevent extraneous movements. The strapping of the foot was loosened during the 30 min of tendon vibration and rest, respectively.
Vibration at 100 Hz was applied over the Achilles tendon using a commercial vibrator (Melissa 631-066; Adexi AB, Mölndal, Sweden) with a plastic concave stimulator head (contact area, approximately 1 cm2). The stimulator head was applied onto the Achilles tendon at the level of the lateral malleolus and was pressed toward the tendon by a constant force of 12.5 N via a weight. The weight and the concave shape of the stimulator head ensured that the placement of thestimulator was maintained during the 30-min vibration. A frequency of 100 Hz was used because this frequency has been shown to fairly selectively activate Ia-afferents (27) and because prolonged 100-Hz vibration has been shown to reduce Ia-afferent efficacy (37).
During the strength tests, a torque motor moved the ankle at an angular velocity of 20°·s−1 through a range of movement of 40°, starting at an ankle angle of 70° in shortening trials and 110° in lengthening trials. Strength (torque) was measured in two trials per action type (shortening and lengthening) with 45 s of rest between trials. The trial resulting in the highest torque for each action type was used for further analysis. The order of action-type trials was counterbalanced between subjects, but the same for each individual subject in both before and after tests in the vibration as well as the control experiment. Plantar flexor strength was taken as the mean torque over 1 s (approximately 20°) in the middle of the range of movement. Torque signals were analog-to-digital converted at 5 kHz using CED 1401 data acquisition system and Signal software (Cambridge Electronic Design, Cambridge, UK).
Transcutaneous electrical stimulation was applied to the tibial nerve through a cathode (Ag-AgCl, Blue M-00-A, electrode sensor area 13.2 mm2; Ambu, Ølstycke, Denmark) taped to the skin in the popliteal fossa and an anode (carbon rubber electrode, 100 × 50 mm; CEFAR Medical, Malmö, Sweden) positioned on the anterior aspect of the thigh, just proximal to the patella. The stimulation consisted of a square 1-ms pulse delivered by a constant current stimulator (Digitimer DS7A; Digitimer Ltd., Hertfordshire, UK) to induce H-reflexes and M-waves in the EMG signal from the soleus muscle. At the beginning of the main experiments, H-reflex and M-wave recruitment curves were obtained to establish the stimulation intensities to be used for eliciting H-reflexes and M-waves. Two supramaximal M-waves were evoked by stimulation at 150% of the intensity causing a leveling off in the M-wave recruitment curve. The peak-to-peak amplitude of the largest of the two M-waves (MMAX) was used for further analysis. For H-reflexes, the intensity resulting in the highest peak-to-peak H-reflex amplitude was applied, first to elicit 5 H-reflexes each separated by 15 s of rest and then to elicit 15 H-reflexes each separated by 1 s of rest. HMAX was calculated as the mean peak-to-peak amplitude of the 5 H-reflexes separated by 15 s of rest and H1Hz as the mean peak-to-peak amplitude of the last 10 of the 15 H-reflexes separated by 1 s of rest. Both HMAX and H1Hz were normalized to the MMAX. At all times, electrical stimulation was performed at an ankle angle of 90° and with the muscles relaxed.
EMG activity was recorded from soleus, medial gastrocnemius, and tibialis anterior using pairs of surface electrodes (Ag-AgCl, Blue M-00-A, electrode sensor area 13.2 mm2; Ambu) placed in a belly-belly configuration to record overall activity. An extra pair of electrodes was placed over the soleus muscle and the Achilles tendon in a belly-tendon configuration for the registration of H-reflexes and M-waves. Signals were band-pass-filtered between 10 and 500 Hz and amplified 2000 times (soleus, gastrocnemius, and tibialis anterior) or band-pass-filtered between 20 and 500 Hz and amplified by 100 (soleus belly-tendon) and analog-to-digital converted at 5 kHz (1401; Cambridge Electronic Design). The 20-Hz high-pass filter was applied to the soleus belly-tendon EMG to avoid movement artifacts in the EMG associated with the reflexes. Root mean square (RMS) EMG from the soleus, medial gastrocnemius, and tibialis anterior were measured over the same 1-s period as the plantar flexor torque. The EMGRMS from the soleus and medial gastrocnemius muscle was normalized to the MMAX of each muscle in the corresponding situation, i.e., before or after vibration and rest, respectively. The rationale for normalizing the EMGRMS to the MMAX is that any potentiating effect (or the opposite) that the protocol may have on the motor axons or muscle fibers will thereby not influence the results (11,26).
All statistical analyses were conducted using Statistica (version 8; Statsoft, Inc., Tulsa, OK). Normal distribution was confirmed using the Shapiro-Wilk W-test. Maximal voluntary plantar flexor strength was analyzed using a three-way repeated-measures ANOVA, with the following factors: time (before or after), intervention (vibration or rest), and action type (shortening or lengthening). Normalized EMGRMS from the soleus, medial gastrocnemius, and tibialis anterior was analyzed using a three-way repeated-measures multivariate ANOVA, with the following factors: time (before or after), intervention (vibration or rest), and action type (shortening or lengthening). Normalized H-reflexes (HMAX:MMAX and H1Hz:MMAX) were analyzed using a three-way repeated-measures ANOVA, with the following factors: time (before or after), intervention (vibration or rest), and reflex ratio (HMAX:MMAX or H1Hz:MMAX). Finally, the soleus MMAX was analyzed using a two-way repeated-measures ANOVA, with the following factors: time (before or after) and intervention (vibration or rest). Where interactions or main effects were found, Tukey HSD post hoc tests were applied. Significance was accepted when P < 0.05. Data are presented as means ± SD.
For reflexes (Figs. 1 and 2), no interactions were found between time, intervention, and reflex ratio, i.e., changes were similar for HMAX:MMAX and H1Hz: MMAX (F1,7 = 1.8, P = 0.223). There was a significant interaction between time and intervention (F1,7 = 28.6, P = 0.001). Before vibration, the overall mean reflex ratio was 0.46 ± 0.20, and after vibration, it was reduced by 33% to 0.31 ± 0.17 (P = 0.001), whereas in the control experiment, overall mean reflex ratio remained unchanged after rest (P = 0.992). There was a significant main effect of reflex ratio (F1,7 = 43.5, P = 0.0003) with the mean HMAX:MMAX being significantly (40%, P = 0.0005) higher than the overall mean H1Hz:MMAX. For MMAX, no significant interactions between time and intervention (F1,7 = 5.1, 0.058) or main effect of time (F1,7 = 0.0, P = 0.863) or intervention (F1,7 = 1.0, P = 0.066) were seen.
For normalized EMGRMS from the soleus (Figs. 3 and 4), medial gastrocnemius, and tibialis anterior (not normalized) muscles, no significant interactions were observed between time, intervention, and action type (F3,5 = 0.5, P = 0.694); between time and intervention (F3,5 = 0.3, P = 0.848); or between time and action type (F3,5 = 1.7, P = 0.279). There was no main effect of time (F3,5 = 4.6, P = 0.070) or action type (F3,5 = 1.2, P = 0.389) on the normalized EMGRMS.
For plantar flexor strength (Fig. 5), no significant interactions were present between time, intervention, and action type (F1,7 = 0.0, P = 0.830); between time and intervention (F1,7 = 3.3); or between time and action type (F1,7 = 0.0, P = 0.886). A significant main effect of time was found on plantar flexor strength (F1,7 = 14.0, P = 0.007), with overall mean values being, on the average, 4% lower after 30 min of intervention (P = 0.007). A significant main effect was seen also for action type (F1,7 = 79.6, P = 0.00005), with overall mean lengthening strength being 25% higher than shortening strength (P = 0.0003).
FIGURE 5-Mean values...Image Tools
The main finding of this study was that 30 min of continuous vibration over the Achilles tendon reduced the amplitude of the H-reflex, indicating a decreased Ia efficacy without any associated decrease in muscle activation and plantar flexor strength either during maximal voluntary shortening or lengthening muscle actions.
There are several possible mechanisms behind decreased H-reflexes, e.g., decreased excitability of the Ia-afferent axons (18), decreased motoneuron excitability, or decreased synaptic efficacy due to increased presynaptic inhibition, either via increased homosynaptic postactivation depression (7,8,13) or increased primary afferent depolarization (30,40). Our finding of lower H1Hz:MMAX than HMAX:MMAX ratio before vibration indicates that the repetitive stimulation used to achieve the H1Hz:MMAX brought about homosynaptic postactivation depression in the synapses due to neurotransmitter depletion (8,13). The maintenance of a similar difference between the two reflex ratios even after the vibration suggests that mechanisms other than homosynaptic postactivation depression may have contributed to the reduced overall Ia synaptic efficacy. Such a mechanism could be primary afferent depolarization, either of central or peripheral origin. Speaking against primary afferent depolarization is the time factor. While homosynaptic postactivation depression takes a long time to restore (8,13), presynaptic inhibition induced via primary afferent depolarization can recover in a fraction of a second (30) and would most likely have vanished in the time elapsed from the end of vibration to the onset of reflex testing. Although the exact mechanisms of how vibration decreased the H-reflexes cannot be resolved in the current study, decreased excitability of the Ia-afferent axons or decreased synaptic efficacy would both result in reduced Ia-afferent input to the motoneurons.
No changes in muscle activation or plantar flexor strength were seen despite a decrease in the amplitude of the H-reflex after vibration. This is contraintuitive assuming that Ia-afferents normally contribute substantially to neural activation during dynamic maximal voluntary actions, particularly lengthening ones. A vibration-induced decrease of excitatory input from plantar flexor Ia-afferents would then be expected to cause a decrease in motoneuron activation and in strength. Because this was not the case, other mechanisms are likely to have counteracted the effects of a decreased Ia afferent efficacy and maintained the net excitation of the motoneurons. Such mechanisms include increased sensitivity of the muscle spindles and increased net motoneuron excitation via other afferent and/or supraspinal inputs. The latter mechanism has some support in the literature. Short-term vibration of the extensor carpi radialis muscle caused an acute increase of transcranial magnetically evoked potentials without affecting potentials induced from transcranial electrical stimulation (16). This was interpreted as a vibration-induced increase in excitability of the motor cortex, possibly as a result of proprioceptive input via the somatosensory cortex. It seems that during the first 15 min of vibration of a hand or wrist muscle, the excitability of the motor cortex controlling the vibrated muscle increases (16,29,33), whereas after a longer-duration vibration (33) or after repeated vibrations, there is instead a decrease in excitability or the homonymous motor cortex, possibly via increased intracortical inhibition (19,20). Furthermore, prolonged vibration, as here but on the upper limbs, has been shown to increase the transcranial magnetically evoked potentials of antagonist muscles via a transcortical pathway (12,34). Such a vibration-induced increase of antagonist activation or decrease in agonist activation would lead to a decrease in measured strength output, everything else equal. However, in the present study, no change in the activation of the antagonist ankle flexor, tibialis anterior, or in plantar flexor strength was observed. This suggests either that the effects of prolonged tendon vibration on the motor cortex differ between upper and lower limbs or that any such changes in cortical excitability did not influence muscle activation and strength.
Although our study seems to be the first to observe that a decrease in H-reflex amplitude does not reduce neural activation and strength in maximal voluntary dynamic actions, previous studies have shown dissimilar changes in activation and H-reflex amplitudes in other situations. For example, dynamic strength training has been demonstrated to induce increases in voluntary activation in isometric (31) and dynamic (10,24) muscle actions without concurrent increases in H-reflexes evoked in a passive muscle. It is possible that the control of presynaptic inhibition will be different between passive and active tasks so that the amount of presynaptic inhibition in a passive task is not representative of that in an active task. If so, this could imply that the presynaptic inhibition was increased by vibration only when the muscles were passive and not, or to a lesser extent, in active muscles. To measure reflexes, as done here, in a passive muscle and neural activation and strength in an active muscle could have lead to an underestimation of the effect of increased presynaptic inhibition of Ia-afferents on activation level and strength output during active, dynamic muscle actions.
Contrary to the current findings on dynamic muscle actions, continuous vibration over a tendon or muscle under maximal voluntary isometric conditions has been shown to cause a decrease of H-reflex amplitude and a concomitant reduction in muscle activation and strength (2,17,35,37). This discrepancy between effects of vibration in static and dynamic actions may, in some cases, be related to methodological differences, e.g., vibration site, vibration duration (2,35). In others, the vibration paradigms were similar to the current one (e.g., Ushiyama et al. (37)) and yet the vibration caused a decrease in isometric strength that was about four times as large as that found for dynamic actions here, albeit a similar decrease in H-reflex amplitude. It would therefore seem that the difference in results could be related to a lesser sensitivity to reduced Ia efficacy in maximal voluntary dynamic than isometric muscle actions. It might even be that Ia-afferent excitation is not contributing to a significant extent to neural activation during maximal voluntary dynamic actions, neither during shortening nor lengthening, at least not in the plantar flexor actions investigated here. Limited contribution to neural activation despite a presumed high firing frequency of Ia-afferents would probably function to allow smooth movements to progress in lengthening muscle actions. In shortening muscle actions, however, the function seems less evident. Bongiovanni et al. (2) suggested fusimotor-driven Ia-afferent feedback to contribute to the recruitment of high-threshold (fast-twitch) motor units during MVC, and Simoneau et al. (32) suggested that females may have a lower proportion of fast-twitch muscle fibers than males. This might mean that enhanced recruitment of high-threshold (fast-twitch) motor units may have been less influential on torque and EMGRMS in the current study based on only females compared with previous studies, based only on men (37). Carter et al. (6) indicated that gender differences are present in absolute volume but not in proportions of fiber types in sedentary subjects. This was also corroborated by Toft et al. (36), who used a larger sample size than previous studies, and failed to find gender differences in fiber composition. It is therefore unlikely, but cannot be excluded, that differences in fiber-type composition, possibly gender-related, could be one of the reasons for the somewhat surprising results that, although HMAX:MMAX significantly decreased due to prolonged vibration, the current study on females only did not observe significant effects of vibration on torque and EMG. Moreover, in the current study, we investigated the effects of vibration on H-reflex, activation, and strength, in a prone position, although presynaptic inhibition of Ia-afferents has been shown to be more extensive in upright postures as opposed to the prone position (3,4). Bove et al. (4) demonstrated that, although standing in itself reduced the H-reflex, applying vibration to the Achilles tendon during standing reduced the H-reflex even more, suggesting that our method might be used also in standing. It is still possible, however, that the effects of prolonged vibration on strength and activation may have been different in standing. To understand more about the contribution of Ia-afferent excitation to neural activation and strength, a variety of muscle activation intensities and velocities of muscle lengthening and shortening should be studied in tasks with different postural demands in subjects of different muscle fiber compositions. It is possible that Ia-afferents would contribute more to neural activation and strength in muscles composed of a higher percentage of fast-twitch muscle fibers that are lengthened at higher velocities than that used here.
In conclusion, sustained vibration over the Achilles tendon induced decreased H-reflex amplitudes in the soleus muscle, suggestive of a decreased efficacy of Ia-afferent excitation at rest, without significantly affecting muscle activation or maximal voluntary shortening or lengthening plantar flexor strength. The findings suggest that Ia-afferent input may not substantially contribute to maximal voluntary dynamic muscle strength of the plantar flexor muscles, as tested here, and thus, the results do not lend support to the notion that Ia-afferent excitation would contribute more to neural activation in maximal voluntary lengthening than shortening muscle actions.
The authors thank the financial support from the Swedish Center for Sports Research.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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