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Discharge properties of human motor units during sustained contraction at low level force
Journal of Electromyography and Kinesiology 11 (2001) 255–261 www.elsevier.com/locate/jelekin
Discharge properties of human motor units during sustained contraction at low level force Mifuyu Kamo *, Shigeru Morimoto Laboratory of Applied Physiology, Faculty of Education and Human Sciences, Yokohama National University, 79-2 Tokiwadai, Hodogaya-ku, Yokohama 240-8501, Japan Received 5 June 2000; received in revised form 20 November 2000; accepted 8 January 2001
Abstract The characteristic of discharge behaviors of motor units (MUs) during low level contraction was investigated. The discharge of MUs in the m. vastus medialis was observed during the sustained contraction at 4 different levels below 10% MVC (2, 4, 8 and 10% MVC) for 15 min. The spike interval of all observed MUs gradually elongated during an initial several minutes of the contraction and the characteristic discharge patterns following the elongation were observed. i.e. continuous discharge throughout the contraction (CONT), decruitment (D-N), and re-recruitment following decruitment (D-REC). The relationship between recruitment threshold force (Fth) and discharge pattern was not significant at 2% MVC but, at 10% MVC, there were significant differences in Fth between D-N and CONT, and between D-REC and CONT MU populations. In pooled data, the MUs with the shorter mean spike interval at the beginning of the contraction (MSI0, below 90 ms) tend to discharge continuously, but the MUs with longer MSI0 showed various discharge patterns. In conclusion, during low level contraction MUs discharge characteristically, and the MU with high excitation levels tend to discharge continuously, but individual MU represents an intrinsic discharge pattern at not a high excitation level. 2001 Elsevier Science Ltd. All rights reserved. Keywords: Low level contraction; Motor unit; Discharge pattern; Decruitment; Re-recruitment
1. Introduction Recruitment of motor units (MUs) and modulation of firing frequency have been known as the regulatory mechanisms for the muscular force development by the central nervous system [1,17]. During submaximal contraction, the recruitment is considered to be the main mechanism to compensate the contractile failure [2,7,18,26]. Moritani et al. [26] reported that MU recruited in an orderly manner from slow to fast type MU during sustained contraction at 50% MVC. On the other hand, Fallentin et al. [8] observed the conspicuous difference in the recruitment pattern of MUs during a 10 and 40% MVC contraction. Therefore, the contraction level is considered to influence the MU recruitment pattern during the submaximal contraction.
* Corresponding author. Tel.: +81-45-339-3271; fax: +81-45-3393271. E-mail address: [email protected] (M. Kamo).
The firing rate modulation might be affected by the contraction level like the recruitment strategy. Several researchers have studied the rate coding of MU during submaximal sustained contractions [3–5,9– 12,20,21,28,29]. In most studies, the contraction level was set at a force more than 10% MVC. We previously observed MU activities in the m. vastus medialis during the sustained contraction at the force just above the recruitment threshold (Fth)(⬍10% MVC) [12]. The result was that the MUs showed the elongation in spike interval at the initial phase of the contraction and was similar to the spike interval elongation at relatively high target forces. But we obtained the characteristic discharge pattern following the initial elongation, i.e., decruitment and decreuitment–rerecruitment pattern. In our previous study, we did not survey general behavior of all activated MUs during the contraction because behavior of MUs with Fth just below target force were only observed. In the present study, we set the target force at 4 levels less than 10% MVC to create a wide difference between
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the Fth of MU and the target force, and investigated the MU activities during the low level sustained contraction.
2. Methods 2.1. Subjects The subjects were one female and three male healthy adult volunteers aged between 20–45 years without any signs or symptoms of neuro-muscular diseases, and all subjects were well skilled to develop the target force at low level with higher accuracy. All subjects were informed about the nature of the experimental procedures and gave their consent. 2.2. Motor unit action potential recording Action potentials of single MUs were recorded from the m. vastus medialis using Teflon-insulated bipolar copper wire electrodes (100 µm diameter). The cut ends of the wires were uncovered with Teflon and bent to hold the electrodes in the muscle. The action potentials of MU were amplified with a differential amplifier (DPA-400C, Dia-Medical System, Tokyo, Japan) with a low/high cut filter of 3 Hz/10 KHz. The input impedance was 20 M⍀. When an action potential of MU is recorded by use of the wire electrode, it is difficult to investigate the same identified single MU activity, reproducible, during the contraction at different experiments. But we want to compare discharge patterns between different target forces in the identified single MU. Therefore, in a part of the experiment, we applied the surface electrode method [22] because the method has the merit to record an action potential of single MU with high reproducibility and has been used in many studies [22–25]. The surface electrodes were Ag/AgCl discs with a diameter of 5 mm. 2.3. Experimental protocol The subjects were requested to sit on a high stool. To record developed force at the ankle, the right lower leg was fastened with a strap (23 mm wide) connected to a strain gauge (U3b1, Shinkoh Electronics, Tokyo) at the articulatio pedis. The angle of the knee joint was set at 90 degrees. The strain gauge was connected with a carrier amplifier (6M84, Nihon–Kohden, Tokyo). All electrical and mechanical signals were recorded on a cassette tape using an FM data recorder (R-31, TEAC, Tokyo). Afterward, the play-backed records were photographed on a film with a continuously recording camera (VC11, Nihon–Kohden, Tokyo) for the detailed analysis, i.e., identification of waveform of single MU. The mean value of the three trials of brief muscle con-
traction (3 s duration) under maximal efforts was determined as the maximal voluntary contraction (MVC), and the target force was set at 2, 4, 8 and 10% MVC. The force of recruitment threshold (Fth) was determined as the force at which the objective MU began to fire during linear force increment at 1% MVC·s⫺1. The subjects gradually increased force to the target force at 1% MVC·s⫺1 followed by sustaining the target force for 15 min. This slow ramp force tracking made it possible to avoid the “overshoot” of force beyond the target force. In some experiments, we set the duration of sustained contraction to 6 min to observe MU activity in initial stage of contraction. The subjects voluntarily controlled the developing force on the target force by selfmonitoring using an oscilloscope placed in front of them. Previously, we recorded simultaneously MU activity and surface EMG in the vastus medialis, vastus lateralis and rectus femoris muscle, and then compared them among three muscles [14,15]. As a result, we did not observe the difference in the change of electrical activity among muscles. Therefore, the results of the present study were not affected by the direction of foot force. Through the experiments, the ambient temperature ranged from 22 to 25°C. 2.4. Analysis on spike interval of motor unit The recording electrical signals sometimes, especially at higher target force, showed complicated wave forms because of the picking up of several MUs activities simultaneously. A high speed of recording film (1000 mm·s⫺1) made it possible to identify single MU activities from wave form visually. We analyzed only data in which the wave form of the MUs remained constant the entire period through the constant force developments for 15 min (cf. Fig. 1e, f and g). Spike intervals were measured on the film with time resolution up to 0.5 ms. We measured every MU spike interval though the contraction. In some cases, mean spike interval was calculated from 25 intervals at beginning of constant contraction and at every minute of the contraction. The difference of mean values of spike interval of MUs among discharge patterns was tested by ANOVA followed by post-hoc test. The difference of proportion of discharge pattern among target force was tested by a chi-square test. Fth among discharge pattern at every target force was compared by a Kruskal–Wallis test and post hoc test. The level of statistical significance was defined as P⬍0.05. 3. Results 3.1. Motor units with decruitment and re-recruitment discharge pattern during low level contraction Fig. 1 shows a typical result of the experiment. Two identified MUs with different wave forms and amplitude
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of every MU as shown in Fig. 2 and then divided the MU into three categories. 25 in 57 MUs decruited (decruitment pattern; D-N hereafer) within 6 minutes after the developed force reaching to the target force, and 15 of them presented re-recruitment (re-recruitment pattern; D-REC hereafer). The other 32 in 57 MUs continuously fired throughout the experiments for 15 min (continuous pattern; CONT hereafter). Fig. 2 shows typical examples of MUs with D-REC and CONT. All of the three discharge patterns (D-N, D-REC and CONT) were commonly observed independent of the subjects and the target force. Fig. 3 represents the proportion of the characterized MU discharge pattern in the stored data at each target experiment. Target force has not the effect on the proportion of the discharge patterns at all target forces.
Fig. 1. Representative recording of motor unit (MU) action potentials. Two MUs were identified from amplitude and wave-form and had constant amplitude and wave-form through the prolonged contraction (record E: before experiment, records F and G: after experiment). The large MU and the small one showed the re-recruited and the decruited discharge pattern, respectively. (a) At the start of the contraction, two MUs recruited with different recruitment threshold (Fth). (b) The large MU stopped firing (decruit) at 150 s after the start of the contraction. (c) The small MU, also, decruited at 3 min 22 s after. (d) Continuing the contraction, the large unit began to fire again at 11 min 21 s (rerecruit). Arrows and star symbols represent the timing of decruit and re-recruit, and the difference of MU. Time bar shows 4 s and 50 ms in a–d and e–g, respectively.
to each other (Fig. 1e, f and g) represent their own discharge patterns during continuous force developments at 8% MVC. Although the spike intervals of both units gradually elongate (initial elongation) and their firing once stop (decruitment) at last, both the timing and duration of the decruitment are quite different from each other. Furthermore, the unit with larger amplitude restarts its neural activity following the decruitment with a pause (re-recruitment), but that with smaller amplitude does not recover its neural activities until the end of the experiment. We could measure completely the spike interval of 57 single MU during the contraction. 10, 15, 14 and 18 MUs were observed at 2, 4, 8 and 10% MVC of target force, respectively. We plotted the spike interval trains
Fig. 2. Spike interval of the motor units (MUs) through the contraction. MU discharge pattern characterized as re-recruitment (D-REC; A) and continuous (CONT; B). At an initial period of the contraction, the elongation of the spike interval was commonly observed.
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Fig. 3. Proportion of each discharge pattern of motor unit to the number of tested motor units at every target force experiment. Three discharge patterns appeared commonly in every target experiment. D-N, D-REC and CONT means decruitment, re-recruitment and continuous discharge pattern, respectively.
3.2. Relationship between discharge pattern and recruitment threshold force Fth of single MUs distributed from 0% MVC to 9.3% MVC. Fig. 4 shows the relationship between Fth and discharge pattern at every target force. At 2% MVC of the lowest target force, Fth was not related to the discharge pattern. Although Fth distribution was broad and overlapped among each discharge pattern at 4% MVC and 8% MVC target forces, the Fth of MUs with CONT was significantly lower than that of D-N, but no difference of Fth between CONT and D-REC, and between D-REC and D-N. At 10% MVC the Fth of MUs with CONT was significantly lower than those of D-N and D-REC, but no difference of Fth between D-N and D-REC. 3.3. Relationship between initial excitation level and discharge pattern At low target force, Fth did not relate the discharge pattern. In contrast, as higher target force, discharge pattern of MU tended to depend on Fth; low Fth MUs showed CONT, high Fth MUs were D-N or D-REC. The relationship between Fth and discharge pattern is considered that discharge pattern of MU during prolonged contraction at low level was changed with excitation level at the onset of constant force. Therefore, the mean spike interval of MU at the beginning of constant contraction (MSI0) was used as the index of an initial excitation level. Fig. 5 shows the relationship between Fth and MSI0 in each type of discharge pattern. Number (%)
Fig. 4. Appearance of discharge pattern against the difference in the recruitment threshold (Fth) in every target experiment. D-N, R-REC and CONT means decruitment, re-recruitment and continuous discharge pattern, respectively. *P⬍0.05.
in each box means the appearance rate of the CONT discharge pattern against the all plots inside the box. In the box of Fth: 0–2% MVC and MSI0: 70–90 ms the appearance ratio of CONT pattern was 100%. The higher appearance ratio of CONT (the number in each box) could be seen in lower Fth and shorter MSI0. On the other hand, the ratio of the D-N and D-REC patterns are higher in the higher Fth and longer MSI0. There was no difference of the distribution of appearance ratio between the D-N and the D-REC patterns.
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Fig. 5. Relation among Fth (abscissa), MSI0 (ordinate), and discharge pattern (symbol) in all motor units (MUs) tested. The symbol of closed circle, closed triangle and open square shows the discharge pattern of decruitment (D-N), re-recruitment (D-REC) and continuous (CONT), respectively. We arbitrarily divided the abscissa and the ordinate into consecutive every 2% MVC and 20 ms, respectively. Each number in the boxes of the figure represents the appearance rate of continuous discharge pattern to all the plotted MUs in the box.
3.4. Discharge pattern of the identified single motor unit at different target force Morimoto et al. [22] have reported a “surface electrodes method” to detect activities of particular single MUs, and this method makes it possible to detect the discharge pattern of the identified single MUs at various contraction levels in different experiments. Fig. 6a and b shows the change in the mean spike interval (MSI) of two identified single MUs by using the surface method during the muscle contraction for 6 min at two different target forces. The symbols and attached bars represent mean value and standard deviation (SD) calculated from results of five different days. Each discharge pattern was highly reproducible. The Fth of MUs was 4% MVC (Fig. 6a) and 5% MVC (Fig. 6b), respectively. In the MU shown in Fig. 6a, the MSI0 was 104.9 ms and 78.3 ms at the target force of 5% MVC and 10% MVC, respectively. Regardless of the initial excitation level (MSI0), discharge pattern of the MU characterized was always CONT. In contrast, in Fig. 6b, at 5% MVC (MSI0: 117 ms) the MU discharged CONT pattern, but D-N pattern at 10% MVC (MSI0: 93.9 ms). Therefore, when MSI0 became lower at low target force, the two MUs represented different discharge patterns to each other.
Fig. 6. Discharge pattern of identified motor units (MUs) at various target force. Symbol and attached bar means the mean value and its standard deviation of 5 mean values obtained from five different experimental trials at the same target performed at different days. (A) MU fired continuously even at every target force, i.e., at different MSI0. Fth of the MU was 4% MVC. (B) MU represented the different discharge pattern under the different target force experiments. At 5% MVC or low value in MSI0, MU decruited, but at 10% MVC or high value in MSI0 MU fired continuously through the experiment.
4. Discussion 4.1. Discharge pattern of motor unit during low level contraction In the present study, we found the characteristic discharge behaviors in MUs from the m. vastus medialis during the submaximal constant isometric contraction (⬍10% MVC) i.e., the initial elongation in the spike interval and the following discharge pattern was able to divide the total discharge pattern into three categories. All the tested MUs showed the elongation of the spike
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interval at the initial phase (⬍6 min) of the prolonged contraction. Also, the initial elongation of spike interval (or decrease of firing rate) have been reported during the sustained contraction at the force of 10% MVC and over. The mechanisms of the initial elongation are still uncertain [4–6,10,16,19,27,28]. One of the possible mechanisms of the elongation is considered from the disfacilitation of the spinal αmotoneuron elicited indirectly by the changes in contracting properties of the muscle fiber(s) [4,5,16]. The potentiation in the force of muscle fiber(s) could compensate the decrease of the developed force of the MU resulted from the elongation of the spike interval. There was difference between the present results and the results at more than 10% MVC. Below 10% MVC in the present conditions, there could not be seen only the continuously discharged MUs but also the decruitment and the re-recruitment MUs. Our preliminary data indicated the simultaneous occurrence of the initial elongation and the recruitment of other MUs during the low level contraction [13,14]. The decruitment following the initial elongation, the re-recruitment following the decruitment and the recruitment of other MUs were considered to be the unique MU activities to control the constant force at low level contraction. The present decruitment and re-recruitment discharge pattern could be considered in relation with the rotational activity reported by Fellentin et al. [8]. They observed rotational activity among MUs on the m. biceps brachii during the fatiguing contraction at 10% MVC but at not 40% MVC. Extensive investigation is necessary to understand the rotation of MUs, such as the instant of rotation among MUs, the characteristics in the relationship between the decruitment MU and recruitment MU which works compensatory. 4.2. Possible factors influenced the discharge pattern In our previous study [12], we observed that the MU discharge pattern did not relate to Fth under the target force set at just above the recruitment threshold of the objective MU. Also, we could elucidate the difference of Fth only between CONT and D-N at the target force of ⭐8% MVC. However, at the 10% MVC experiment, it appeared as a significant difference in Fth distribution between DN and CONT MU populations, and between D-REC and CONT MU populations (cf. Fig. 4). This distinct relation in the 10% MVC experiment was considered to be provided from the extent in the difference between the target force and the Fth because that the large extent produced the large difference in MSI0 among MUs. As shown in Fig. 5, CONT MU distributed mainly in the range of shorter MSI0 and there was intermingled distribution among three discharge pattern MUs above 110 ms of MSI0. When the consideration was constructed from two
parameters, Fth and MSI0, together, the MU with low Fth and with short MSI0 had the tendency to discharge continuously during the submaximal contraction (CONT MU). Two MUs represented the same discharge pattern of CONT at short MSI0. But, at longer MSI0, two MUs discharged in different patterns to each other, one (A) fired continuously and the other (B) decruited. In conclusion, during submaximal contraction at 10% MVC or below, the behavior of MUs show continuous discharge and unique characteristics following the elongation of spike interval at initial contraction, i.e. decruitement (D-N) and re-recruitment following the decruitment (D-REC). The MU with high initial excitation level tended to discharge continuously, but individual MU represents an intrinsic discharge pattern at not that high excitation level.
Acknowledgements I would like to thank Dr Watanabe, MD, PhD (The University of Jikei, School of Medicine) for variable comments on a draft of the manuscript.
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Mifuyu Kamo received a MSc degree in eduction from Yokohama National University. Since 1987 she has worked on the motor unit activity by use of fine wire electrodes and surface eletrodes in the Department of Applied (Exercise) Physiology at Yokhama National University. She is currently working to complete her PhD on behaviour of motor units during submaximal voluntary contraction. Her interest is the mechanism to maintain the development force constantly at the inhibitory phase in motor unit activity during the intital period of the submaximal prolonged contraction. Shigeru Morimoto was born in Japan in 1951. He received his MD degree from the Department of Physiology, The Jikei University, School of Medicine in 1983. In 1984 he was a lecturer of the Department of Physiology, The Jikei University, School of Medicine. In 1985, he started work at the Department of Applied (Exercise) Physiology, Faculty of Education, Yokhama National University. From 1997 to date he has been a professor of the Department of Applied (Exercise) Physiology, Faculty of Education and Human Science. His current research interests focus on the reconstruction of surface myoelectric signals from wave form of the motor unit action potential.
Discharge properties of human motor units during sustained contraction at low level force Mifuyu Kamo *, Shigeru Morimoto Laboratory of Applied Physiology, Faculty of Education and Human Sciences, Yokohama National University, 79-2 Tokiwadai, Hodogaya-ku, Yokohama 240-8501, Japan Received 5 June 2000; received in revised form 20 November 2000; accepted 8 January 2001
Abstract The characteristic of discharge behaviors of motor units (MUs) during low level contraction was investigated. The discharge of MUs in the m. vastus medialis was observed during the sustained contraction at 4 different levels below 10% MVC (2, 4, 8 and 10% MVC) for 15 min. The spike interval of all observed MUs gradually elongated during an initial several minutes of the contraction and the characteristic discharge patterns following the elongation were observed. i.e. continuous discharge throughout the contraction (CONT), decruitment (D-N), and re-recruitment following decruitment (D-REC). The relationship between recruitment threshold force (Fth) and discharge pattern was not significant at 2% MVC but, at 10% MVC, there were significant differences in Fth between D-N and CONT, and between D-REC and CONT MU populations. In pooled data, the MUs with the shorter mean spike interval at the beginning of the contraction (MSI0, below 90 ms) tend to discharge continuously, but the MUs with longer MSI0 showed various discharge patterns. In conclusion, during low level contraction MUs discharge characteristically, and the MU with high excitation levels tend to discharge continuously, but individual MU represents an intrinsic discharge pattern at not a high excitation level. 2001 Elsevier Science Ltd. All rights reserved. Keywords: Low level contraction; Motor unit; Discharge pattern; Decruitment; Re-recruitment
1. Introduction Recruitment of motor units (MUs) and modulation of firing frequency have been known as the regulatory mechanisms for the muscular force development by the central nervous system [1,17]. During submaximal contraction, the recruitment is considered to be the main mechanism to compensate the contractile failure [2,7,18,26]. Moritani et al. [26] reported that MU recruited in an orderly manner from slow to fast type MU during sustained contraction at 50% MVC. On the other hand, Fallentin et al. [8] observed the conspicuous difference in the recruitment pattern of MUs during a 10 and 40% MVC contraction. Therefore, the contraction level is considered to influence the MU recruitment pattern during the submaximal contraction.
* Corresponding author. Tel.: +81-45-339-3271; fax: +81-45-3393271. E-mail address: [email protected] (M. Kamo).
The firing rate modulation might be affected by the contraction level like the recruitment strategy. Several researchers have studied the rate coding of MU during submaximal sustained contractions [3–5,9– 12,20,21,28,29]. In most studies, the contraction level was set at a force more than 10% MVC. We previously observed MU activities in the m. vastus medialis during the sustained contraction at the force just above the recruitment threshold (Fth)(⬍10% MVC) [12]. The result was that the MUs showed the elongation in spike interval at the initial phase of the contraction and was similar to the spike interval elongation at relatively high target forces. But we obtained the characteristic discharge pattern following the initial elongation, i.e., decruitment and decreuitment–rerecruitment pattern. In our previous study, we did not survey general behavior of all activated MUs during the contraction because behavior of MUs with Fth just below target force were only observed. In the present study, we set the target force at 4 levels less than 10% MVC to create a wide difference between
1050-6411/01/$ - see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S 1 0 5 0 - 6 4 1 1 ( 0 1 ) 0 0 0 0 5 - 0
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M. Kamo, S. Morimoto / Journal of Electromyography and Kinesiology 11 (2001) 255–261
the Fth of MU and the target force, and investigated the MU activities during the low level sustained contraction.
2. Methods 2.1. Subjects The subjects were one female and three male healthy adult volunteers aged between 20–45 years without any signs or symptoms of neuro-muscular diseases, and all subjects were well skilled to develop the target force at low level with higher accuracy. All subjects were informed about the nature of the experimental procedures and gave their consent. 2.2. Motor unit action potential recording Action potentials of single MUs were recorded from the m. vastus medialis using Teflon-insulated bipolar copper wire electrodes (100 µm diameter). The cut ends of the wires were uncovered with Teflon and bent to hold the electrodes in the muscle. The action potentials of MU were amplified with a differential amplifier (DPA-400C, Dia-Medical System, Tokyo, Japan) with a low/high cut filter of 3 Hz/10 KHz. The input impedance was 20 M⍀. When an action potential of MU is recorded by use of the wire electrode, it is difficult to investigate the same identified single MU activity, reproducible, during the contraction at different experiments. But we want to compare discharge patterns between different target forces in the identified single MU. Therefore, in a part of the experiment, we applied the surface electrode method [22] because the method has the merit to record an action potential of single MU with high reproducibility and has been used in many studies [22–25]. The surface electrodes were Ag/AgCl discs with a diameter of 5 mm. 2.3. Experimental protocol The subjects were requested to sit on a high stool. To record developed force at the ankle, the right lower leg was fastened with a strap (23 mm wide) connected to a strain gauge (U3b1, Shinkoh Electronics, Tokyo) at the articulatio pedis. The angle of the knee joint was set at 90 degrees. The strain gauge was connected with a carrier amplifier (6M84, Nihon–Kohden, Tokyo). All electrical and mechanical signals were recorded on a cassette tape using an FM data recorder (R-31, TEAC, Tokyo). Afterward, the play-backed records were photographed on a film with a continuously recording camera (VC11, Nihon–Kohden, Tokyo) for the detailed analysis, i.e., identification of waveform of single MU. The mean value of the three trials of brief muscle con-
traction (3 s duration) under maximal efforts was determined as the maximal voluntary contraction (MVC), and the target force was set at 2, 4, 8 and 10% MVC. The force of recruitment threshold (Fth) was determined as the force at which the objective MU began to fire during linear force increment at 1% MVC·s⫺1. The subjects gradually increased force to the target force at 1% MVC·s⫺1 followed by sustaining the target force for 15 min. This slow ramp force tracking made it possible to avoid the “overshoot” of force beyond the target force. In some experiments, we set the duration of sustained contraction to 6 min to observe MU activity in initial stage of contraction. The subjects voluntarily controlled the developing force on the target force by selfmonitoring using an oscilloscope placed in front of them. Previously, we recorded simultaneously MU activity and surface EMG in the vastus medialis, vastus lateralis and rectus femoris muscle, and then compared them among three muscles [14,15]. As a result, we did not observe the difference in the change of electrical activity among muscles. Therefore, the results of the present study were not affected by the direction of foot force. Through the experiments, the ambient temperature ranged from 22 to 25°C. 2.4. Analysis on spike interval of motor unit The recording electrical signals sometimes, especially at higher target force, showed complicated wave forms because of the picking up of several MUs activities simultaneously. A high speed of recording film (1000 mm·s⫺1) made it possible to identify single MU activities from wave form visually. We analyzed only data in which the wave form of the MUs remained constant the entire period through the constant force developments for 15 min (cf. Fig. 1e, f and g). Spike intervals were measured on the film with time resolution up to 0.5 ms. We measured every MU spike interval though the contraction. In some cases, mean spike interval was calculated from 25 intervals at beginning of constant contraction and at every minute of the contraction. The difference of mean values of spike interval of MUs among discharge patterns was tested by ANOVA followed by post-hoc test. The difference of proportion of discharge pattern among target force was tested by a chi-square test. Fth among discharge pattern at every target force was compared by a Kruskal–Wallis test and post hoc test. The level of statistical significance was defined as P⬍0.05. 3. Results 3.1. Motor units with decruitment and re-recruitment discharge pattern during low level contraction Fig. 1 shows a typical result of the experiment. Two identified MUs with different wave forms and amplitude
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of every MU as shown in Fig. 2 and then divided the MU into three categories. 25 in 57 MUs decruited (decruitment pattern; D-N hereafer) within 6 minutes after the developed force reaching to the target force, and 15 of them presented re-recruitment (re-recruitment pattern; D-REC hereafer). The other 32 in 57 MUs continuously fired throughout the experiments for 15 min (continuous pattern; CONT hereafter). Fig. 2 shows typical examples of MUs with D-REC and CONT. All of the three discharge patterns (D-N, D-REC and CONT) were commonly observed independent of the subjects and the target force. Fig. 3 represents the proportion of the characterized MU discharge pattern in the stored data at each target experiment. Target force has not the effect on the proportion of the discharge patterns at all target forces.
Fig. 1. Representative recording of motor unit (MU) action potentials. Two MUs were identified from amplitude and wave-form and had constant amplitude and wave-form through the prolonged contraction (record E: before experiment, records F and G: after experiment). The large MU and the small one showed the re-recruited and the decruited discharge pattern, respectively. (a) At the start of the contraction, two MUs recruited with different recruitment threshold (Fth). (b) The large MU stopped firing (decruit) at 150 s after the start of the contraction. (c) The small MU, also, decruited at 3 min 22 s after. (d) Continuing the contraction, the large unit began to fire again at 11 min 21 s (rerecruit). Arrows and star symbols represent the timing of decruit and re-recruit, and the difference of MU. Time bar shows 4 s and 50 ms in a–d and e–g, respectively.
to each other (Fig. 1e, f and g) represent their own discharge patterns during continuous force developments at 8% MVC. Although the spike intervals of both units gradually elongate (initial elongation) and their firing once stop (decruitment) at last, both the timing and duration of the decruitment are quite different from each other. Furthermore, the unit with larger amplitude restarts its neural activity following the decruitment with a pause (re-recruitment), but that with smaller amplitude does not recover its neural activities until the end of the experiment. We could measure completely the spike interval of 57 single MU during the contraction. 10, 15, 14 and 18 MUs were observed at 2, 4, 8 and 10% MVC of target force, respectively. We plotted the spike interval trains
Fig. 2. Spike interval of the motor units (MUs) through the contraction. MU discharge pattern characterized as re-recruitment (D-REC; A) and continuous (CONT; B). At an initial period of the contraction, the elongation of the spike interval was commonly observed.
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Fig. 3. Proportion of each discharge pattern of motor unit to the number of tested motor units at every target force experiment. Three discharge patterns appeared commonly in every target experiment. D-N, D-REC and CONT means decruitment, re-recruitment and continuous discharge pattern, respectively.
3.2. Relationship between discharge pattern and recruitment threshold force Fth of single MUs distributed from 0% MVC to 9.3% MVC. Fig. 4 shows the relationship between Fth and discharge pattern at every target force. At 2% MVC of the lowest target force, Fth was not related to the discharge pattern. Although Fth distribution was broad and overlapped among each discharge pattern at 4% MVC and 8% MVC target forces, the Fth of MUs with CONT was significantly lower than that of D-N, but no difference of Fth between CONT and D-REC, and between D-REC and D-N. At 10% MVC the Fth of MUs with CONT was significantly lower than those of D-N and D-REC, but no difference of Fth between D-N and D-REC. 3.3. Relationship between initial excitation level and discharge pattern At low target force, Fth did not relate the discharge pattern. In contrast, as higher target force, discharge pattern of MU tended to depend on Fth; low Fth MUs showed CONT, high Fth MUs were D-N or D-REC. The relationship between Fth and discharge pattern is considered that discharge pattern of MU during prolonged contraction at low level was changed with excitation level at the onset of constant force. Therefore, the mean spike interval of MU at the beginning of constant contraction (MSI0) was used as the index of an initial excitation level. Fig. 5 shows the relationship between Fth and MSI0 in each type of discharge pattern. Number (%)
Fig. 4. Appearance of discharge pattern against the difference in the recruitment threshold (Fth) in every target experiment. D-N, R-REC and CONT means decruitment, re-recruitment and continuous discharge pattern, respectively. *P⬍0.05.
in each box means the appearance rate of the CONT discharge pattern against the all plots inside the box. In the box of Fth: 0–2% MVC and MSI0: 70–90 ms the appearance ratio of CONT pattern was 100%. The higher appearance ratio of CONT (the number in each box) could be seen in lower Fth and shorter MSI0. On the other hand, the ratio of the D-N and D-REC patterns are higher in the higher Fth and longer MSI0. There was no difference of the distribution of appearance ratio between the D-N and the D-REC patterns.
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Fig. 5. Relation among Fth (abscissa), MSI0 (ordinate), and discharge pattern (symbol) in all motor units (MUs) tested. The symbol of closed circle, closed triangle and open square shows the discharge pattern of decruitment (D-N), re-recruitment (D-REC) and continuous (CONT), respectively. We arbitrarily divided the abscissa and the ordinate into consecutive every 2% MVC and 20 ms, respectively. Each number in the boxes of the figure represents the appearance rate of continuous discharge pattern to all the plotted MUs in the box.
3.4. Discharge pattern of the identified single motor unit at different target force Morimoto et al. [22] have reported a “surface electrodes method” to detect activities of particular single MUs, and this method makes it possible to detect the discharge pattern of the identified single MUs at various contraction levels in different experiments. Fig. 6a and b shows the change in the mean spike interval (MSI) of two identified single MUs by using the surface method during the muscle contraction for 6 min at two different target forces. The symbols and attached bars represent mean value and standard deviation (SD) calculated from results of five different days. Each discharge pattern was highly reproducible. The Fth of MUs was 4% MVC (Fig. 6a) and 5% MVC (Fig. 6b), respectively. In the MU shown in Fig. 6a, the MSI0 was 104.9 ms and 78.3 ms at the target force of 5% MVC and 10% MVC, respectively. Regardless of the initial excitation level (MSI0), discharge pattern of the MU characterized was always CONT. In contrast, in Fig. 6b, at 5% MVC (MSI0: 117 ms) the MU discharged CONT pattern, but D-N pattern at 10% MVC (MSI0: 93.9 ms). Therefore, when MSI0 became lower at low target force, the two MUs represented different discharge patterns to each other.
Fig. 6. Discharge pattern of identified motor units (MUs) at various target force. Symbol and attached bar means the mean value and its standard deviation of 5 mean values obtained from five different experimental trials at the same target performed at different days. (A) MU fired continuously even at every target force, i.e., at different MSI0. Fth of the MU was 4% MVC. (B) MU represented the different discharge pattern under the different target force experiments. At 5% MVC or low value in MSI0, MU decruited, but at 10% MVC or high value in MSI0 MU fired continuously through the experiment.
4. Discussion 4.1. Discharge pattern of motor unit during low level contraction In the present study, we found the characteristic discharge behaviors in MUs from the m. vastus medialis during the submaximal constant isometric contraction (⬍10% MVC) i.e., the initial elongation in the spike interval and the following discharge pattern was able to divide the total discharge pattern into three categories. All the tested MUs showed the elongation of the spike
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interval at the initial phase (⬍6 min) of the prolonged contraction. Also, the initial elongation of spike interval (or decrease of firing rate) have been reported during the sustained contraction at the force of 10% MVC and over. The mechanisms of the initial elongation are still uncertain [4–6,10,16,19,27,28]. One of the possible mechanisms of the elongation is considered from the disfacilitation of the spinal αmotoneuron elicited indirectly by the changes in contracting properties of the muscle fiber(s) [4,5,16]. The potentiation in the force of muscle fiber(s) could compensate the decrease of the developed force of the MU resulted from the elongation of the spike interval. There was difference between the present results and the results at more than 10% MVC. Below 10% MVC in the present conditions, there could not be seen only the continuously discharged MUs but also the decruitment and the re-recruitment MUs. Our preliminary data indicated the simultaneous occurrence of the initial elongation and the recruitment of other MUs during the low level contraction [13,14]. The decruitment following the initial elongation, the re-recruitment following the decruitment and the recruitment of other MUs were considered to be the unique MU activities to control the constant force at low level contraction. The present decruitment and re-recruitment discharge pattern could be considered in relation with the rotational activity reported by Fellentin et al. [8]. They observed rotational activity among MUs on the m. biceps brachii during the fatiguing contraction at 10% MVC but at not 40% MVC. Extensive investigation is necessary to understand the rotation of MUs, such as the instant of rotation among MUs, the characteristics in the relationship between the decruitment MU and recruitment MU which works compensatory. 4.2. Possible factors influenced the discharge pattern In our previous study [12], we observed that the MU discharge pattern did not relate to Fth under the target force set at just above the recruitment threshold of the objective MU. Also, we could elucidate the difference of Fth only between CONT and D-N at the target force of ⭐8% MVC. However, at the 10% MVC experiment, it appeared as a significant difference in Fth distribution between DN and CONT MU populations, and between D-REC and CONT MU populations (cf. Fig. 4). This distinct relation in the 10% MVC experiment was considered to be provided from the extent in the difference between the target force and the Fth because that the large extent produced the large difference in MSI0 among MUs. As shown in Fig. 5, CONT MU distributed mainly in the range of shorter MSI0 and there was intermingled distribution among three discharge pattern MUs above 110 ms of MSI0. When the consideration was constructed from two
parameters, Fth and MSI0, together, the MU with low Fth and with short MSI0 had the tendency to discharge continuously during the submaximal contraction (CONT MU). Two MUs represented the same discharge pattern of CONT at short MSI0. But, at longer MSI0, two MUs discharged in different patterns to each other, one (A) fired continuously and the other (B) decruited. In conclusion, during submaximal contraction at 10% MVC or below, the behavior of MUs show continuous discharge and unique characteristics following the elongation of spike interval at initial contraction, i.e. decruitement (D-N) and re-recruitment following the decruitment (D-REC). The MU with high initial excitation level tended to discharge continuously, but individual MU represents an intrinsic discharge pattern at not that high excitation level.
Acknowledgements I would like to thank Dr Watanabe, MD, PhD (The University of Jikei, School of Medicine) for variable comments on a draft of the manuscript.
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Mifuyu Kamo received a MSc degree in eduction from Yokohama National University. Since 1987 she has worked on the motor unit activity by use of fine wire electrodes and surface eletrodes in the Department of Applied (Exercise) Physiology at Yokhama National University. She is currently working to complete her PhD on behaviour of motor units during submaximal voluntary contraction. Her interest is the mechanism to maintain the development force constantly at the inhibitory phase in motor unit activity during the intital period of the submaximal prolonged contraction. Shigeru Morimoto was born in Japan in 1951. He received his MD degree from the Department of Physiology, The Jikei University, School of Medicine in 1983. In 1984 he was a lecturer of the Department of Physiology, The Jikei University, School of Medicine. In 1985, he started work at the Department of Applied (Exercise) Physiology, Faculty of Education, Yokhama National University. From 1997 to date he has been a professor of the Department of Applied (Exercise) Physiology, Faculty of Education and Human Science. His current research interests focus on the reconstruction of surface myoelectric signals from wave form of the motor unit action potential.