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Medial gastrocnemius is a key muscle for involuntary alternate muscle activity of plantar flexor synergists
Neuroscience Letters 550 (2013) 145–149
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Medial gastrocnemius is a key muscle for involuntary alternate muscle activity of plantar flexor synergists Kaoru Kishibuchi, Motoki Kouzaki ∗ Laboratory of Neurophysiology, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
h i g h l i g h t s • Alternate muscle activity was associated with physiological tremor of ankle angular acceleration. • Activity of medial gastrocnemius muscle was accompanied by physiological tremor. • Medial gastrocnemius reduces redundant activities of synergists.
a r t i c l e
i n f o
Article history: Received 15 April 2013 Received in revised form 10 June 2013 Accepted 24 June 2013 Keywords: Cross-correlation analysis Tremor Synergistic muscles
a b s t r a c t Redundant and/or complicated muscle activations between synergist muscles have been demonstrated during low-level sustained contractions. Identification of a key muscle for this phenomenon allows for the simplification of motor control during prolonged contraction. In this study, we have identified a key muscle for involuntary alternate muscle activity of plantar flexor muscles based on a physiological tremor sequence that was recorded over 120 min. Two epochs where the muscle activity of medial gastrocnemius abruptly increased with decrease in other synergists (case ON) and vise verse (case OFF) were analyzed. Our results indicated that involuntary alternate muscle activity was associated with changes in physiological tremor of ankle angular acceleration when the muscle activity of medial gastrocnemius decreased in case OFF. In particular, the activity of the medial gastrocnemius muscle, but not the activity of other synergists, was accompanied by physiological tremor, demonstrating that the medial gastrocnemius is a key muscle for involuntary alternate muscle activity in plantar flexor synergists. In addition, weaker correlations between muscle activities and physiological tremor were found in case ON than case OFF. We suggest that, if the central nervous system can employ this unique muscle strategy, redundant and/or complicated neuromuscular activities will be reduced because of the existence of the key muscle. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction In low-level, prolonged contraction (≤10% of maximal voluntary contraction; MVC), the synergist muscles are not continuously activated, but rather are activated in an alternating pattern of activity and silence. Unique activation within synergistic muscles has been observed in synergist muscle groups, including knee extensor [1,11,14–16] and plantar flexor [19,22,23] muscles. This unique strategy of synergistic muscles has been referred to as “alternate muscle activity” [12,15]. However, the neural mechanism of alternate muscle activity has not been elucidated. Our studies using knee extensor muscles have reported that alternate muscle activity occurred in the rectus femoris muscle
∗ Corresponding author at: Laboratory of Neurophysiology, Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501, Japan. Tel.: +81 75 753 2927; fax: +81 75 753 2927. E-mail address: [email protected] (M. Kouzaki). 0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2013.06.052
and either vastus lateralis or vastus medialis muscles, suggesting that the emergence of alternate muscle activity in knee extensor synergists is related to the neural properties of the rectus femoris muscle [12,15]. Thus, this muscle can be defined as a key muscle for simplifying alternate muscle activity including complex neural circuit among synergists [11,12]. However, it is very difficult to reveal the aspect of the alternate muscle activity in plantar flexor muscles because alternations of plantar flexors are more complicated than those of knee extensors. In knee extensor muscles, the alternate muscle activity is found only between rectus femoris and both vasti-muscles [14,15]. On the other hand, there are numerous combinations of alternate muscle activity among individual muscles composing plantar flexor synergists [23], and it seems that alternate muscle activity of plantar flexors emerges without regularity [22,23]. In addition, overlapped activities between the muscles are observed in the plantar flexors [22] not in the knee extensors [14,15] during alternate muscle activity. This overlap complicates the characteristics of alternate muscle activity of plantar flexor synergists. Therefore, the key muscle in the involuntary alternate muscle activity of plantar flexor synergists remains unclear.
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Fig. 1. Representative data demonstrating involuntary activation during prolonged plantar flexion for 120 min. Ankle angle, surface electromyogram (EMG) of medial gastrocnemius (MG), lateral gastrocnemius (LG), soleus (SOL), and tibialis anterior (TA) muscles, results of the time-frequency analysis of ankle angular acceleration, and the tremor component sequence of ankle angular acceleration are shown. Time–frequency analysis of ankle angular acceleration for 1 s segments is represented as a color map. Blue and red indicate lower and higher power spectrum density, respectively. Tremor component was calculated by integrating 8–12 Hz of angular acceleration.
In knee extensor synergists, alternate muscle activity is accompanied by physiological tremor, with cyclic force fluctuations of 8–12 Hz, and this parallel activity is related to the rhythmical activity of rectus femoris muscle, which is a key muscle for this activity [14]. By investigating high-frequency motor variability of these fluctuations, the physiological tremor that accompanies alternate muscle activity could be quantified, allowing the identification of a key muscle for alternate muscle activity. Hence, the present study identified the key muscle for the complicated alternate muscle activity of plantar flexor muscle based on the observed physiological tremor. The findings of this study indicate that the existence of this specific muscle reduces redundant and/or complicated neural commands from the central nervous system (CNS) during prolonged contraction. 2. Methods Twelve healthy male subjects (aged 23 ± 1.4 years) voluntarily participated in this study. The subjects provided written informed consent regarding participation in the study after receiving a detailed explanation of the purpose, potential benefits, and risks associated with participation. All procedures used in this study were in accordance with the Declaration of Helsinki and were approved by the Committee for Human Experimentation at the Graduate School of Human and Environmental Studies, Kyoto University. Each subject was seated on a chair designed to secure his leg in full extension. With the knee joint in full extension, the subject’s foot was placed on a footplate at 110◦ of plantar flexion
(90◦ equaling the right angle of the ankle). The subject maintained this ankle angle at 110◦ for 120 min while supporting a load hung from the footplate. The suspended load created horizontal tension pulled horizontally in the direction of dorsiflexion, and the load corresponded to 10% of subjects’ isometric maximal voluntary contraction at 110◦ of the ankle joint [22,23]. To maintain the ankle angle, the displacement of the ankle angle was measured from a distance with a charge-coupled device laser displacement sensor (LK-2500, Keyence, Osaka, Japan) with a spatial resolution of 10 m [10]. Laser displacement sensor was positioned 35 cm apart to the plastic plate attached to a footplate. Present study employed the position-holding task as prolonged contraction because greater fluctuations in motor output and more frequent bursting EMG activity during position-holding task than during isometric force task have been reported [7,8]. Surface electromyogram (EMGs) from skin surface over the medial head of gastrocnemius (MG), lateral head of gastrocnemius (LG), soleus (SOL), and tibialis anterior (TA) muscles were recorded with Ag-AgCl electrodes with a diameter of 5 mm and an interelectrode distance of 20 mm. The electrodes were connected to a preamplifier and a differential amplifier with a bandwidth of 5 Hz to 1 kHz (MEG-6116M, Nihon-kohden, Tokyo, Japan). All signals were sampled at a rate of 1 kHz by a 16-bit analog-to-digital converter (PowerLab/16SP, ADInstrument, Sydney, Australia) and were stored on the hard drive of a personal computer for later analyses. In the sustained contraction task, alternate EMG activity [11,14–16] was observed among plantar flexor synergists in all subjects. In particular, the reciprocal EMG activity between MG and either LG or SOL could be found throughout the task (Fig. 1).
K. Kishibuchi, M. Kouzaki / Neuroscience Letters 550 (2013) 145–149
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Fig. 2. Spatiotemporal relations between physiological tremor and muscle activities during alternate muscle activity. (A) Angular acceleration from 8 to 12 Hz sequence, average amplitude of EMG (AEMG) for every 1 s of MG, LG, and SOL, and time differentiation of filtered AEMG (AEMGdiff /dt) of MG at the occurrence of the alternate muscle activity. “ON” indicates when AEMG of MG dramatically increased with a decrease in LG according to a positive peak of AEMGdiff /dt. “OFF” indicates when AEMG of MG dramatically decreased with an increase in LG according to a negative peak of AEMGdiff /dt. Shaded areas indicate the calculation period for 120 s in case ON and OFF. (B) Group-averaged, normalized cross-correlation function (CCF) between angular acceleration from 8 to 12 Hz and AEMG of MG (blue lines), LG (red lines), and SOL (green lines) of the case ON and case OFF. Positive time lag means changes in AEMG of each muscle occurred after angular acceleration response.
We have confirmed that involuntary alternate muscle activity of knee extensor muscles was not due to changes in the force vector as well as changes in posture [15]. In similar to knee extensor muscles, Tamaki et al. [23] demonstrated that alternate muscle activity of plantar flexor muscles is not influenced by the position change and force direction. Hence, it has been established that the alternate muscle activity is not caused by changes in force vector or the adjustment of posture but rather to complex neurophysiological factors of the synergistic muscles [15,23]. The EMG of TA (antagonist muscle) was small and constant across the sustained contraction, and thus, it was not included in further analyses [15]. The EMG signals were full-wave rectified and averaged for 1 s to calculate the average amplitude EMG (AEMG). The AEMG signals were passed through a low-pass filter of 0.01 Hz using a fourth-order Butterworth filter to remove the high-frequency components [16]. To detect the abrupt increase and decrease in the EMG signals, AEMGdiff /dt was then given as a result of the time differentiation of the filtered AEMG sequence [16]. The ankle angular displacement series was digitally differentiated to obtain the ankle angular acceleration in the plantar flexion–dorsal flexion directions. To investigate the fluctuations in angular acceleration, time-frequency analysis was applied to ankle angular acceleration data. The acceleration data were divided into 1 s segments (1000 points long), and a fast-Fourier transform algorithm were then applied to every 1 s segment to yield the power spectrum density. The fluctuations in acceleration of about 8–12 Hz, referred to as “physiological tremor”, have been observed in fatigued muscle [17]. For further analysis of physiological tremor in a time series, the power spectrum of acceleration from 8 to 12 Hz was integrated and defined as the physiological tremor component of the acceleration fluctuations [3]. To evaluate the extent of correlation and the time relation between the AEMG of individual plantar flexor synergists
and physiological tremor component sequences, a normalized cross-correlation function (CCF) between the two time series was calculated [16]. Data for a 90-min period (between the 30th and the 120th min) of the sustained contraction task were selected for analysis because alternate muscle activity could not be observed ∼20 min after the sustained contraction commenced [15]. Furthermore, we focused in particular on the responses of the physiological tremor sequence around the two epochs at which alternate muscle activity emerged (Fig. 2A): the epoch where the AEMG of MG abruptly increased with the decrease in the AEMG of LG and/or SOL (case ON) and the epoch where the AEMG of MG dramatically decreased with an increase in the AEMG of LG and/or SOL (case OFF). On the basis of the previous study [16], data of the alternate muscle activities that involved case ON and case OFF were extracted as follows: for each epoch, a data set for the ∼120 s period that included the most abrupt change of MG in the center was selected by visual inspection. We used the abrupt change in MG as a reference because the changes in the AEMG of MG are more distinct than those of LG or SOL. AEMGdiff /dt was then given as a result of the time derivative of the low-pass filtered AEMG of MG. The extracted data were aligned to the positive and negative peaks of the AEMGdiff /dt of MG for case ON and case OFF, respectively. As a result, the number of all the epochs extracted for the 120 s duration from 12 subjects was 120 and 141 for case ON and case OFF, respectively.
3. Results The MVC was 719.5 ± 124.0 N, and as a result, the load for the sustained contraction task was equivalent to 5.35 ± 1.03 kg. All subjects were able to perform the entire sustained contraction task for
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120 min. A typical example of the changes in the AEMG and physiological tremor is shown in Fig. 1. Alternate muscle activity emerged between MG and both LG and SOL in all subjects. Time frequency analysis revealed that the power distribution of angular acceleration was about 10 Hz (Fig. 1, second panel from the bottom), and it seems likely that the fluctuations in angular acceleration between 8 and 12 Hz did not increase solely because of the sustained contraction task but appeared to be accompanied by MG activity (Fig. 1, bottom panel). The strength of the similarity and the time lag between the AEMG and physiological tremor sequences were assessed by crosscorrelation analysis (Fig. 2). The number of all the epochs extracted for the duration of 120 s from 12 subjects was 120 and 141 for case ON and case OFF, respectively. In case ON, a distinct sharp peak of normalized CCF was not observed for all the muscle activity observed (Fig. 2B, upper panel). In contrast, in case OFF, the normalized CCF showed a positive peak value at about a time lag of 0 s in MG, and a negative peak value at about a time lag of 0 s in both LG and SOL (Fig. 2B, lower panel).
4. Discussion In the present study, alternate muscle activity involuntarily occurred among plantar flexor synergists in all subjects during sustained contraction. The sustained contraction lasted for 120 min and was accomplished by holding an ankle position at a 110◦ angle while bearing a load equivalent to the weight at 10% of MVC (Fig. 1). Studies using knee extensor synergists demonstrate that alternate muscle activity occurs between bi- (rectus femoris) and mono-articular (either vastus lateralis or vastus medialis) muscles, suggesting that the emergence of alternate muscle activity of synergistic muscle is related to reciprocal complex physiological relations between bi- and mono-articular muscles [11,12,14,15]. However, the key muscle for the involuntary alternate muscle activity of plantar flexor synergists remains unclear because alternations of plantar flexors are more complicated than those of knee extensors [19,22,23]. The existence of a key muscle for alternate muscle activity allows for the simplification of this complex phenomenon. We demonstrated that activity alternations among knee extensor synergists are related to the unique muscle activity of the rectus femoris muscle, which augments the force fluctuations with a cyclic frequency of 8–12 Hz [3], and we have pointed out that factor of alternate muscle activity of knee extensor muscles is a physiological tremor-related neural circuit from the bi-articular rectus femoris muscle [14]. Therefore, the identification of a significant muscle for alternate muscle activity based on observed physiological tremor simplifies the complicated activities of synergistic muscles. In the present study, fluctuations of 8–12 Hz in ankle angular acceleration did not increase monotonically but instead varied widely during the sustained contraction task, which is consistent with a previous study examining knee extensor muscles [14]. Physical fluctuations of the muscle of about 8–12 Hz are termed ‘physiological tremor’, which arises from not only Ia afferent activity but also neural oscillations from central commands to motoneuron pool [17]. It has been reported that muscle spindles respond to even small force fluctuations that occur during isometric contractions [24] and that a reduction of physiological tremor by ischemia and vibration depresses Ia afferent inputs to the ␣-motoneuron pool during fatiguing contraction [3]. It has also been demonstrated that the physiological tremor during active contraction reflects the synchronization of active motor units at frequencies of approximately 10 Hz from central commands [18]. Animal studies have confirmed the existence of synchronized discharges of corticomotor neurons at certain frequencies [20,21],
suggesting a common rhythmic input from central commands. Therefore, it can be suggested that the discontinuous emergence of 8–12 Hz fluctuations in motor output are physiological tremor originating from Ia afferent activity as well as from the central commands. It seems that the amplitude of physiological tremor observed in the present study is accompanied by AEMG of MG (Fig. 1). Careful observations of the timing between physiological tremor and MG activity suggest that the tremor is not always relevant to AEMG of MG (e.g., the amplitude of tremor was constant when AEMG of MG began to increase abruptly; Fig. 2A). Thus, we evaluated the physiological tremor component at the two epochs where the AEMG of MG abruptly increased with the decrease in the AEMG of LG and/or SOL (case ON), and vice versa (case OFF). In case OFF, where the AEMG of MG dramatically decreased with the increase in the AEMG of LG and/or SOL, the CCF analysis revealed that there was a strong positive correlation between physiological tremor and MG and a strong negative correlation between physiological tremor and both LG and SOL without a time lag (Fig. 2B, lower panel). These results indicate that the decrease in physiological tremor was associated with both a decrease in MG activity and an increase in LG and SOL activity. The excitation of Ia afferents is considered to result from increased ␥-motoneuron activity, which controls muscle spindle sensitivity. Physiological tremor and MG activity decreased simultaneously, which indicates that the Ia afferent input to the ␣-motoneuron pool of MG is decreased. The reason for this decreased Ia afferent activity might be a reduction in muscle spindle activity after prolonged muscle spindle discharge [2,13]. Our results showed that decreases in physiological tremor and MG activity were associated with increases in both LG and SOL activity, which indicates that the ␣-motoneuron pool of both LG and SOL was excited despite an attenuation of the ␣-motoneuron pool of MG. One possibility for this result is that this reciprocal relation between MG and both LG and SOL is caused by the depression of inhibitory input to these muscles from the Ia afferent activity of MG [5]. In addition, motor unit synchronization increases as fatigue occurs [6], suggesting that the CNS synchronizes the active motor units when fatigue develops. It has been suggested that the changes in physiological tremor of knee extension force fluctuations are caused by the unique muscle activity of rectus femoris muscle during the alternate muscle activity [14]. Specific muscle activity of MG during alternate muscle activity in the present study would correspond to the rectus femoris in the previous study [14]. Taking into account, therefore, it can be speculated that the physiological tremor produced by MG is related to alternate muscle activity of plantar flexor synergists. On the other hand, in case ON where the AEMG of MG abruptly increased with the decrease in the AEMG of LG and/or SOL, there was no correlation between physiological tremor and any plantar flexor muscle (Fig. 2B, upper panel). During prolonged contraction, group III and IV afferents were activated by accumulated chemicals and metabolites resulting in muscle fatigue [4]. Group III and IV afferents activated ␥-motoneurons and enhanced muscle spindle sensitivity, and Ia afferent activity was then enhanced [9]. However, responses of these afferent activities are slower compared with those of Ia afferent activity. Therefore, fatigue-related physiological tremor due to small diameter afferents might have no influence on the alternate muscle activity of plantar flexor muscles. In conclusion, alternate muscle activity was associated with changes in the physiological tremor component of ankle angular acceleration during prolonged plantar flexion in a position-holding task; especially MG activity was accompanied by physiological tremor. These results suggest that the MG is a key muscle for involuntary alternate muscle activity in plantar flexor synergists.
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Acknowledgment This work was supported, in part, by a grant from the Ministry of Education #15700396, Science and Culture of Japan (to M. Kouzaki). References [1] H. Akima, A. Saito, K. Watanabe, M. Kouzaki, Alternate muscle activity patterns among synergists of the quadriceps femoris including the vastus intermedius during low-level sustained contraction in men, Muscle Nerve 46 (2012) 86–95. [2] L.G. Bongiovanni, K.E. Hagbarth, L. Stjernberg, Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man, J. Physiol. 423 (1990) 15–26. [3] A.G. Cresswell, W.N. Löscher, Significance of peripheral afferent input to the alpha-motoneurone pool for enhancement of tremor during an isometric fatiguing contraction, Eur. J. Appl. Physiol. 82 (2000) 129–136. [4] S.C. Gandevia, Spinal and supraspinal factors in human muscle fatigue, Physiol. Rev. 81 (2001) 1725–1789. [5] I. Gritti, M. Schieppati, Short-latency inhibition of soleus motoneurones by impulses in Ia afferents from the gastrocnemius muscle in human, J. Physiol. 416 (1989) 469–484. [6] A. Holtermann, C. Grönlund, J.S. Karlsson, K. Roeleveld, Motor unit synchronization during fatigue: described with a novel sEMG method based on large motor unit samples, J. Electromyogr. Kinesiol. 19 (2009) 232–241. [7] S.K. Hunter, D.L. Ryan, J.D. Ortega, R.M. Enoka, Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans, J. Neurophysiol. 88 (2002) 3087–3096. [8] S.K. Hunter, T. Yoon, L. Farinella, E.E. Griffith, A.V. Ng, Time to task failure and muscle activation vary with load type for a submaximal fatiguing contraction with the lower leg, J. Appl. Physiol. 105 (2008) 463–472. [9] H. Johansson, P. Sojka, Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: a hypothesis, Med. Hypotheses 35 (1991) 196–203. [10] M. Kouzaki, T. Fukunaga, Frequency features of mechanomyographic signals of human soleus muscle during quiet standing, J. Neurosci. Methods 173 (2008) 241–248. [11] M. Kouzaki, M. Shinohara, The frequency of alternate muscle activity is associated with the attenuation in muscle fatigue, J. Appl. Physiol. 101 (2006) 715–720.
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[12] M. Kouzaki, M. Shinohara, Alternation in muscle activity to reduce muscle fatigue, in: M. Shinohara (Ed.), Advance in Neuromuscular Physiology of Motor Skills and Muscle Fatigue, Research Signpost, 2009, pp. 351–367. [13] M. Kouzaki, M. Shinohara, T. Fukunaga, Decrease in maximal voluntary contraction by tonic vibration applied to a single synergist muscle in humans, J. Appl. Physiol. 89 (2000) 1420–1424. [14] M. Kouzaki, M. Shinohara, K. Masani, T. Fukunaga, Force fluctuations are modulated by alternate muscle activity of knee extensor synergists during low-level sustained contraction, J. Appl. Physiol. 97 (2004) 2121–2131. [15] M. Kouzaki, M. Shinohara, K. Masani, H. Kanehisa, T. Fukunaga, Alternate muscle activity observed between knee extensor synergists during low-level sustained contractions, J. Appl. Physiol. 93 (2002) 675–684. [16] M. Kouzaki, M. Shinohara, K. Masani, M. Tachi, H. Kanehisa, T. Fukunaga, Local blood circulation among knee extensor synergists in relation to alternate muscle activity during low-level sustained contraction, J. Appl. Physiol. 95 (2003) 49–56. [17] J.H. McAuley, C.D. Marsden, Physiological and pathological tremors and rhythmic central motor control, Brain 123 (2000) 1545–1567. [18] J.H. McAuley, J.C. Rothwell, C.D. Marsden, Frequency peaks of tremor muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing, Exp. Brain Res. 114 (1997) 525–541. [19] L. McLean, N. Goudy, Neuromuscular response to sustained low-level muscle activation: within- and between-synergist substitution in the triceps surae muscles, J. Appl. Physiol. Eur. 91 (2004) 204–216. [20] V.N. Murthy, E.E. Fetz, Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys, J. Neurophysiol. 76 (1996) 3968–3982. [21] M.A. Nicolelis, L.A. Baccala, R.C. Lin, J.K. Chapin, Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system, Science 268 (1995) 1353–1358. [22] H. Tamaki, H. Kirimoto, K. Yotani, H. Takekura, Frequent alternate muscle activity of plantar flexor synergists and muscle endurance during low-level static contractions as a function of ankle position, J. Physiol. Sci. 61 (2011) 411–419. [23] H. Tamaki, K. Kitada, T. Akamine, F. Murata, T. Sakou, H. Kurata, Alternate activity in the synergistic muscles during prolonged low-level contraction, J. Appl. Physiol. 84 (1998) 1943–1951. [24] Å.B. Vallbo, Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque, Acta Physiol. Scand. 90 (1974) 319–336.
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Medial gastrocnemius is a key muscle for involuntary alternate muscle activity of plantar flexor synergists Kaoru Kishibuchi, Motoki Kouzaki ∗ Laboratory of Neurophysiology, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
h i g h l i g h t s • Alternate muscle activity was associated with physiological tremor of ankle angular acceleration. • Activity of medial gastrocnemius muscle was accompanied by physiological tremor. • Medial gastrocnemius reduces redundant activities of synergists.
a r t i c l e
i n f o
Article history: Received 15 April 2013 Received in revised form 10 June 2013 Accepted 24 June 2013 Keywords: Cross-correlation analysis Tremor Synergistic muscles
a b s t r a c t Redundant and/or complicated muscle activations between synergist muscles have been demonstrated during low-level sustained contractions. Identification of a key muscle for this phenomenon allows for the simplification of motor control during prolonged contraction. In this study, we have identified a key muscle for involuntary alternate muscle activity of plantar flexor muscles based on a physiological tremor sequence that was recorded over 120 min. Two epochs where the muscle activity of medial gastrocnemius abruptly increased with decrease in other synergists (case ON) and vise verse (case OFF) were analyzed. Our results indicated that involuntary alternate muscle activity was associated with changes in physiological tremor of ankle angular acceleration when the muscle activity of medial gastrocnemius decreased in case OFF. In particular, the activity of the medial gastrocnemius muscle, but not the activity of other synergists, was accompanied by physiological tremor, demonstrating that the medial gastrocnemius is a key muscle for involuntary alternate muscle activity in plantar flexor synergists. In addition, weaker correlations between muscle activities and physiological tremor were found in case ON than case OFF. We suggest that, if the central nervous system can employ this unique muscle strategy, redundant and/or complicated neuromuscular activities will be reduced because of the existence of the key muscle. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction In low-level, prolonged contraction (≤10% of maximal voluntary contraction; MVC), the synergist muscles are not continuously activated, but rather are activated in an alternating pattern of activity and silence. Unique activation within synergistic muscles has been observed in synergist muscle groups, including knee extensor [1,11,14–16] and plantar flexor [19,22,23] muscles. This unique strategy of synergistic muscles has been referred to as “alternate muscle activity” [12,15]. However, the neural mechanism of alternate muscle activity has not been elucidated. Our studies using knee extensor muscles have reported that alternate muscle activity occurred in the rectus femoris muscle
∗ Corresponding author at: Laboratory of Neurophysiology, Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501, Japan. Tel.: +81 75 753 2927; fax: +81 75 753 2927. E-mail address: [email protected] (M. Kouzaki). 0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2013.06.052
and either vastus lateralis or vastus medialis muscles, suggesting that the emergence of alternate muscle activity in knee extensor synergists is related to the neural properties of the rectus femoris muscle [12,15]. Thus, this muscle can be defined as a key muscle for simplifying alternate muscle activity including complex neural circuit among synergists [11,12]. However, it is very difficult to reveal the aspect of the alternate muscle activity in plantar flexor muscles because alternations of plantar flexors are more complicated than those of knee extensors. In knee extensor muscles, the alternate muscle activity is found only between rectus femoris and both vasti-muscles [14,15]. On the other hand, there are numerous combinations of alternate muscle activity among individual muscles composing plantar flexor synergists [23], and it seems that alternate muscle activity of plantar flexors emerges without regularity [22,23]. In addition, overlapped activities between the muscles are observed in the plantar flexors [22] not in the knee extensors [14,15] during alternate muscle activity. This overlap complicates the characteristics of alternate muscle activity of plantar flexor synergists. Therefore, the key muscle in the involuntary alternate muscle activity of plantar flexor synergists remains unclear.
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Fig. 1. Representative data demonstrating involuntary activation during prolonged plantar flexion for 120 min. Ankle angle, surface electromyogram (EMG) of medial gastrocnemius (MG), lateral gastrocnemius (LG), soleus (SOL), and tibialis anterior (TA) muscles, results of the time-frequency analysis of ankle angular acceleration, and the tremor component sequence of ankle angular acceleration are shown. Time–frequency analysis of ankle angular acceleration for 1 s segments is represented as a color map. Blue and red indicate lower and higher power spectrum density, respectively. Tremor component was calculated by integrating 8–12 Hz of angular acceleration.
In knee extensor synergists, alternate muscle activity is accompanied by physiological tremor, with cyclic force fluctuations of 8–12 Hz, and this parallel activity is related to the rhythmical activity of rectus femoris muscle, which is a key muscle for this activity [14]. By investigating high-frequency motor variability of these fluctuations, the physiological tremor that accompanies alternate muscle activity could be quantified, allowing the identification of a key muscle for alternate muscle activity. Hence, the present study identified the key muscle for the complicated alternate muscle activity of plantar flexor muscle based on the observed physiological tremor. The findings of this study indicate that the existence of this specific muscle reduces redundant and/or complicated neural commands from the central nervous system (CNS) during prolonged contraction. 2. Methods Twelve healthy male subjects (aged 23 ± 1.4 years) voluntarily participated in this study. The subjects provided written informed consent regarding participation in the study after receiving a detailed explanation of the purpose, potential benefits, and risks associated with participation. All procedures used in this study were in accordance with the Declaration of Helsinki and were approved by the Committee for Human Experimentation at the Graduate School of Human and Environmental Studies, Kyoto University. Each subject was seated on a chair designed to secure his leg in full extension. With the knee joint in full extension, the subject’s foot was placed on a footplate at 110◦ of plantar flexion
(90◦ equaling the right angle of the ankle). The subject maintained this ankle angle at 110◦ for 120 min while supporting a load hung from the footplate. The suspended load created horizontal tension pulled horizontally in the direction of dorsiflexion, and the load corresponded to 10% of subjects’ isometric maximal voluntary contraction at 110◦ of the ankle joint [22,23]. To maintain the ankle angle, the displacement of the ankle angle was measured from a distance with a charge-coupled device laser displacement sensor (LK-2500, Keyence, Osaka, Japan) with a spatial resolution of 10 m [10]. Laser displacement sensor was positioned 35 cm apart to the plastic plate attached to a footplate. Present study employed the position-holding task as prolonged contraction because greater fluctuations in motor output and more frequent bursting EMG activity during position-holding task than during isometric force task have been reported [7,8]. Surface electromyogram (EMGs) from skin surface over the medial head of gastrocnemius (MG), lateral head of gastrocnemius (LG), soleus (SOL), and tibialis anterior (TA) muscles were recorded with Ag-AgCl electrodes with a diameter of 5 mm and an interelectrode distance of 20 mm. The electrodes were connected to a preamplifier and a differential amplifier with a bandwidth of 5 Hz to 1 kHz (MEG-6116M, Nihon-kohden, Tokyo, Japan). All signals were sampled at a rate of 1 kHz by a 16-bit analog-to-digital converter (PowerLab/16SP, ADInstrument, Sydney, Australia) and were stored on the hard drive of a personal computer for later analyses. In the sustained contraction task, alternate EMG activity [11,14–16] was observed among plantar flexor synergists in all subjects. In particular, the reciprocal EMG activity between MG and either LG or SOL could be found throughout the task (Fig. 1).
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Fig. 2. Spatiotemporal relations between physiological tremor and muscle activities during alternate muscle activity. (A) Angular acceleration from 8 to 12 Hz sequence, average amplitude of EMG (AEMG) for every 1 s of MG, LG, and SOL, and time differentiation of filtered AEMG (AEMGdiff /dt) of MG at the occurrence of the alternate muscle activity. “ON” indicates when AEMG of MG dramatically increased with a decrease in LG according to a positive peak of AEMGdiff /dt. “OFF” indicates when AEMG of MG dramatically decreased with an increase in LG according to a negative peak of AEMGdiff /dt. Shaded areas indicate the calculation period for 120 s in case ON and OFF. (B) Group-averaged, normalized cross-correlation function (CCF) between angular acceleration from 8 to 12 Hz and AEMG of MG (blue lines), LG (red lines), and SOL (green lines) of the case ON and case OFF. Positive time lag means changes in AEMG of each muscle occurred after angular acceleration response.
We have confirmed that involuntary alternate muscle activity of knee extensor muscles was not due to changes in the force vector as well as changes in posture [15]. In similar to knee extensor muscles, Tamaki et al. [23] demonstrated that alternate muscle activity of plantar flexor muscles is not influenced by the position change and force direction. Hence, it has been established that the alternate muscle activity is not caused by changes in force vector or the adjustment of posture but rather to complex neurophysiological factors of the synergistic muscles [15,23]. The EMG of TA (antagonist muscle) was small and constant across the sustained contraction, and thus, it was not included in further analyses [15]. The EMG signals were full-wave rectified and averaged for 1 s to calculate the average amplitude EMG (AEMG). The AEMG signals were passed through a low-pass filter of 0.01 Hz using a fourth-order Butterworth filter to remove the high-frequency components [16]. To detect the abrupt increase and decrease in the EMG signals, AEMGdiff /dt was then given as a result of the time differentiation of the filtered AEMG sequence [16]. The ankle angular displacement series was digitally differentiated to obtain the ankle angular acceleration in the plantar flexion–dorsal flexion directions. To investigate the fluctuations in angular acceleration, time-frequency analysis was applied to ankle angular acceleration data. The acceleration data were divided into 1 s segments (1000 points long), and a fast-Fourier transform algorithm were then applied to every 1 s segment to yield the power spectrum density. The fluctuations in acceleration of about 8–12 Hz, referred to as “physiological tremor”, have been observed in fatigued muscle [17]. For further analysis of physiological tremor in a time series, the power spectrum of acceleration from 8 to 12 Hz was integrated and defined as the physiological tremor component of the acceleration fluctuations [3]. To evaluate the extent of correlation and the time relation between the AEMG of individual plantar flexor synergists
and physiological tremor component sequences, a normalized cross-correlation function (CCF) between the two time series was calculated [16]. Data for a 90-min period (between the 30th and the 120th min) of the sustained contraction task were selected for analysis because alternate muscle activity could not be observed ∼20 min after the sustained contraction commenced [15]. Furthermore, we focused in particular on the responses of the physiological tremor sequence around the two epochs at which alternate muscle activity emerged (Fig. 2A): the epoch where the AEMG of MG abruptly increased with the decrease in the AEMG of LG and/or SOL (case ON) and the epoch where the AEMG of MG dramatically decreased with an increase in the AEMG of LG and/or SOL (case OFF). On the basis of the previous study [16], data of the alternate muscle activities that involved case ON and case OFF were extracted as follows: for each epoch, a data set for the ∼120 s period that included the most abrupt change of MG in the center was selected by visual inspection. We used the abrupt change in MG as a reference because the changes in the AEMG of MG are more distinct than those of LG or SOL. AEMGdiff /dt was then given as a result of the time derivative of the low-pass filtered AEMG of MG. The extracted data were aligned to the positive and negative peaks of the AEMGdiff /dt of MG for case ON and case OFF, respectively. As a result, the number of all the epochs extracted for the 120 s duration from 12 subjects was 120 and 141 for case ON and case OFF, respectively.
3. Results The MVC was 719.5 ± 124.0 N, and as a result, the load for the sustained contraction task was equivalent to 5.35 ± 1.03 kg. All subjects were able to perform the entire sustained contraction task for
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120 min. A typical example of the changes in the AEMG and physiological tremor is shown in Fig. 1. Alternate muscle activity emerged between MG and both LG and SOL in all subjects. Time frequency analysis revealed that the power distribution of angular acceleration was about 10 Hz (Fig. 1, second panel from the bottom), and it seems likely that the fluctuations in angular acceleration between 8 and 12 Hz did not increase solely because of the sustained contraction task but appeared to be accompanied by MG activity (Fig. 1, bottom panel). The strength of the similarity and the time lag between the AEMG and physiological tremor sequences were assessed by crosscorrelation analysis (Fig. 2). The number of all the epochs extracted for the duration of 120 s from 12 subjects was 120 and 141 for case ON and case OFF, respectively. In case ON, a distinct sharp peak of normalized CCF was not observed for all the muscle activity observed (Fig. 2B, upper panel). In contrast, in case OFF, the normalized CCF showed a positive peak value at about a time lag of 0 s in MG, and a negative peak value at about a time lag of 0 s in both LG and SOL (Fig. 2B, lower panel).
4. Discussion In the present study, alternate muscle activity involuntarily occurred among plantar flexor synergists in all subjects during sustained contraction. The sustained contraction lasted for 120 min and was accomplished by holding an ankle position at a 110◦ angle while bearing a load equivalent to the weight at 10% of MVC (Fig. 1). Studies using knee extensor synergists demonstrate that alternate muscle activity occurs between bi- (rectus femoris) and mono-articular (either vastus lateralis or vastus medialis) muscles, suggesting that the emergence of alternate muscle activity of synergistic muscle is related to reciprocal complex physiological relations between bi- and mono-articular muscles [11,12,14,15]. However, the key muscle for the involuntary alternate muscle activity of plantar flexor synergists remains unclear because alternations of plantar flexors are more complicated than those of knee extensors [19,22,23]. The existence of a key muscle for alternate muscle activity allows for the simplification of this complex phenomenon. We demonstrated that activity alternations among knee extensor synergists are related to the unique muscle activity of the rectus femoris muscle, which augments the force fluctuations with a cyclic frequency of 8–12 Hz [3], and we have pointed out that factor of alternate muscle activity of knee extensor muscles is a physiological tremor-related neural circuit from the bi-articular rectus femoris muscle [14]. Therefore, the identification of a significant muscle for alternate muscle activity based on observed physiological tremor simplifies the complicated activities of synergistic muscles. In the present study, fluctuations of 8–12 Hz in ankle angular acceleration did not increase monotonically but instead varied widely during the sustained contraction task, which is consistent with a previous study examining knee extensor muscles [14]. Physical fluctuations of the muscle of about 8–12 Hz are termed ‘physiological tremor’, which arises from not only Ia afferent activity but also neural oscillations from central commands to motoneuron pool [17]. It has been reported that muscle spindles respond to even small force fluctuations that occur during isometric contractions [24] and that a reduction of physiological tremor by ischemia and vibration depresses Ia afferent inputs to the ␣-motoneuron pool during fatiguing contraction [3]. It has also been demonstrated that the physiological tremor during active contraction reflects the synchronization of active motor units at frequencies of approximately 10 Hz from central commands [18]. Animal studies have confirmed the existence of synchronized discharges of corticomotor neurons at certain frequencies [20,21],
suggesting a common rhythmic input from central commands. Therefore, it can be suggested that the discontinuous emergence of 8–12 Hz fluctuations in motor output are physiological tremor originating from Ia afferent activity as well as from the central commands. It seems that the amplitude of physiological tremor observed in the present study is accompanied by AEMG of MG (Fig. 1). Careful observations of the timing between physiological tremor and MG activity suggest that the tremor is not always relevant to AEMG of MG (e.g., the amplitude of tremor was constant when AEMG of MG began to increase abruptly; Fig. 2A). Thus, we evaluated the physiological tremor component at the two epochs where the AEMG of MG abruptly increased with the decrease in the AEMG of LG and/or SOL (case ON), and vice versa (case OFF). In case OFF, where the AEMG of MG dramatically decreased with the increase in the AEMG of LG and/or SOL, the CCF analysis revealed that there was a strong positive correlation between physiological tremor and MG and a strong negative correlation between physiological tremor and both LG and SOL without a time lag (Fig. 2B, lower panel). These results indicate that the decrease in physiological tremor was associated with both a decrease in MG activity and an increase in LG and SOL activity. The excitation of Ia afferents is considered to result from increased ␥-motoneuron activity, which controls muscle spindle sensitivity. Physiological tremor and MG activity decreased simultaneously, which indicates that the Ia afferent input to the ␣-motoneuron pool of MG is decreased. The reason for this decreased Ia afferent activity might be a reduction in muscle spindle activity after prolonged muscle spindle discharge [2,13]. Our results showed that decreases in physiological tremor and MG activity were associated with increases in both LG and SOL activity, which indicates that the ␣-motoneuron pool of both LG and SOL was excited despite an attenuation of the ␣-motoneuron pool of MG. One possibility for this result is that this reciprocal relation between MG and both LG and SOL is caused by the depression of inhibitory input to these muscles from the Ia afferent activity of MG [5]. In addition, motor unit synchronization increases as fatigue occurs [6], suggesting that the CNS synchronizes the active motor units when fatigue develops. It has been suggested that the changes in physiological tremor of knee extension force fluctuations are caused by the unique muscle activity of rectus femoris muscle during the alternate muscle activity [14]. Specific muscle activity of MG during alternate muscle activity in the present study would correspond to the rectus femoris in the previous study [14]. Taking into account, therefore, it can be speculated that the physiological tremor produced by MG is related to alternate muscle activity of plantar flexor synergists. On the other hand, in case ON where the AEMG of MG abruptly increased with the decrease in the AEMG of LG and/or SOL, there was no correlation between physiological tremor and any plantar flexor muscle (Fig. 2B, upper panel). During prolonged contraction, group III and IV afferents were activated by accumulated chemicals and metabolites resulting in muscle fatigue [4]. Group III and IV afferents activated ␥-motoneurons and enhanced muscle spindle sensitivity, and Ia afferent activity was then enhanced [9]. However, responses of these afferent activities are slower compared with those of Ia afferent activity. Therefore, fatigue-related physiological tremor due to small diameter afferents might have no influence on the alternate muscle activity of plantar flexor muscles. In conclusion, alternate muscle activity was associated with changes in the physiological tremor component of ankle angular acceleration during prolonged plantar flexion in a position-holding task; especially MG activity was accompanied by physiological tremor. These results suggest that the MG is a key muscle for involuntary alternate muscle activity in plantar flexor synergists.
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