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Recruitment threshold force and its changing type of motor units during voluntary contraction at various speeds in man
89
Brain Research, 372 (1986) 89-94 Elsevier BRE 11639
Recruitment Threshold Force and its Changing Type of Motor Units during Voluntary Contraction at Various Speeds in Man TSUGUTAKE YONEDA, KAZUO OISHI, SEI FUJIKURA and AYAKO ISHIDA
Department of Physiology, School of Physical Education, Juntendo University, Fujisaki, Narashino, Chiba 275 (Japan) (Accepted August 27th, 1985)
Key words: voluntary force exertion - - ballistic contraction - - ramp contraction - - isometric force - motor unit - - threshold force - - force rate
The motor unit discharges in human hand muscles were recorded during voluntary isometric contraction. Bipolar wire electrodes were inserted in the right adductor pollicis muscle (AP) and first dorsal interosseous muscle (FDI) for the recordings. Motor unit activities from these muscles were investigated when subjects exerted voluntary force to each target force at various speeds. On 27 motor units of AP and 28 motor units of FDI, ramp RTF and ballistic RTF were compared. Furthermore, RTF changes of motor units with the different force speeds were investigated. It is clear that the RTF of the motor units during ballistic contractions were lower than those during ramp contraction. The processes of motor unit RTF changes were classified into 3 types: RTF of type I motor units were relatively low and decreased slightly even when force speed increased widely; RTF of type II motor units were relatively high and decreased irregularly; and RTF of type III motor units, which appeared rarely, decreased their relatively high RTF with increases of force speed increment. It is suggested that the volitional outflow related with the force speed change to the spinal motor pool might cause the different RTF change effects in the various motor units.
INTRODUCTION The value of the exerted voluntary force corresponding to the first discharge of a single m o t o r unit which participates in the force d e v e l o p m e n t has been termed the recruitment threshold force ( R T F ) of the m o t o r unitS,IS-20. Each m o t o r unit, in the whole muscle, has different R T F . Therefore, the m o t o r units were recruited at different times during force development. In other words, m o t o r units during force development were recruited in an o r d e r based on R T F , from low to high. It has been p o i n t e d out by several workers that RTFs are related to the several physiological properties of m o t o r units, n a m e l y the size of the motoneuron13,14.20, the conduction velocity of the m o t o n e u ronl, 8, the discharge frequency 12 and the contraction timeS,16,17A9. F u r t h e r m o r e , it has been shown that the contraction time of a m o t o r unit having a high discharge frequency p r o p e r t y is smaller than that of a
low discharge frequency m o t o r unitlO, n. Therefore, R T F might be an i m p o r t a n t index to explore the mechanisms of m o t o r unit recruitment during voluntary contractio.n in a wide speed range. Even though the R T F shows the p r o p e r t i e s of a m o t o r unit, R T F s of individual m o t o r units are not a fixed index 21. According to the studies by D e s m e d t and GodauxS-7, the R T F of a m o t o r unit during rapid (ballistic) contraction is lower than that during slow r a m p contraction. D e s m e d t and G o d a u x showed that the R T F varied with voluntary force speed. The present study was u n d e r t a k e n to clarify how the force speed effects the m o t o r unit R T F change, and how the m o t o r units classified in R T F change type in hand muscles in man. MATERIALS AND METHODS Experiments were carried out on the a d d u c t o r pollicis muscle ( A P ) and the first dorsal interosseous
Correspondence: T. Yoneda, Department of Physiology, School of Physical Education, Juntendo University, Fujisaki, Narashino, Chiba 275, Japan. 0006-8993/86/$03.50 © 1986 Elsevier Science Publishers B.V. (Biomedical Division)
90 muscle (FDI) of the right hand. Subjects were healthy adult men.
Procedures Subjects sat on a chair, and their right forearm and hand was fixed as shown in Fig. 1. The subject was instructed to perform a voluntary movement with the thumb and the index finger, respectively, after the oral signal of the examiner. The subject could watch the amplitude and the time course of exerted forces on a sweep screen of a two-channel monitor oscilloscope. Three modes of force exertions were carried out as follow: (1) slow ramp contraction with the time to peak forces of 1, 2 and 5 s by visual tracking of the target force development; (2) fast ramp contractions with the time to peak forces ranging from 0.15 to 1 s without tracking but with monitoring; and (3) ballistic contractions performed as fast as possible follow-
A
ing relaxation. As for the fast ramp and ballistic contraction, target force level was set as a horizontal sweep line on the screen of the monitor scope, and subjects performed the force matching task accordingly. In the case of the AP experiment, the joint angle of the thumb was set at 20 ° . The target force level was set at 3 kg throughout the experiment. In the FDI experiment, the joint angle between the thumb and index finger was set at 40 ° . The target force level was set at 2 kg, Procedures of force exertion were the same as in the AP experiment.
Force recordings The voluntary isometric force exerted by the subject while performing the adduction or the abduction movement by the fingers, was recorded by means of a transduction of the strain gauge which was put on a stainless steel pole (Fig. 1, P; 10 mm diameter) with a trigger holder (Fig. 1, H) of thumb and index finger. The gauge signal was amplified by a carrier amplifier ( K Y O W A , DPM-350A) and led to a data recorder and stored on magnetic tape. The force signal was also led to a monitor oscilloscope separately. The recordings of motor unit discharges and 3 kg force curves of the thumb during 3 different force speeds are shown in Fig. 2.
Recording of the motor unit activity
B
B1
B2
H
Fig. 1. A: general view of hand fixation of the experiment for adductor pollicis muscle. B: hand fixation for first dorsal interosseous muscle experiment viewed from the side (B2) and from the top (B1). F, fixed belt; G, strain gauge; H, plastic trigger holder; P, plate; and S, stainless steel pole. Arrows in A and B1 indicate the direction of exerted force.
Plastic embedded fine bipolar electrodes were made from two fine polyurethane coated copper wires (50 ,urn diameter). The wires of these electrodes were the same as those which were used in Kurata's coil shaped electrode ]5. Less than 10 mm of the tips of two wires were embedded in a little acryl-resin in a parallel position. After a few millimeters of the tip was cut off by a razor blade, the electrode was inserted into the muscle via a 1/2 gauge hypodermic needle. These electrodes were selective to record the action potentials of several motor units and were capable of recording over 2 h. Action potentials of motor units were amplified by a high input impedance extracellular amplifier ( D I A Medical System Co., DPA-100E) and stored on a magnetic tape together with the force signal by a data recorder.
Measurement of R TF Force signals of the whole muscle and action po-
91 a JJ..[l I[)Ilfltllll[IJ~Ulll~I.. I1 rill []Nlli]lllilllllIlllltI .................................................
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'~,,~' Fig. 2. Serial recordings of forces and motor unit activities in adductor pollicis muscle at 3 force speeds. A, 5 s ramp contraction; 13, 0.4 s ramp contraction; C, ballistic contraction. Upper traces are motor unit electrical activities recorded by means of fine wire electrodes and lower traces are force curves. The peak forces were of the same amplitude. It was observed that the RTF of a certain motor unit 'a' which was shown in A of ramp contraction lowered with force speed increment as shown in B and C.
contraction RTFs were measured when the force exertion achieved 3 kg target force in AP and 1 kg in FDI. In Fig. 3, 23 pairs of RTF data during ramp and ballistic contractions of AP motor units and 27 pairs of RTF data of FDI motor units are shown. It is clear that RTFs during ballistic contraction were lower than those during ramp contraction. The values of many RTFs during ballistic contraction were zero, although RTFs during ramp contraction were not entirely zero.
Relationship between R TF and force speed AP motor unit. When the 3 kg isometric forces were exerted by thumb adduction at various force speeds, serial changes of RTF of AP motor units to force speeds were studied. When a certain motor unit was activated during both ballistic and ramp contraction, RTFs of the motor unit were measured at various speeds. The results derived from each series of experiments of 5 motor units among 27 motor units of 5 subjects are shown in Fig. 4. In all cases, RTFs decreased with force speed changes from low to high, and those during ballistic
A 5000-
tentials of the motor unit stored on a magnetic tape were then transferred to oscillopaper. This oscillogram was used for motor unit identification and RTF measurement. Single motor units were identified from the amplitude and shape of the action potentials in a routine manner. RTF of the motor unit was expressed as the value of the whole muscle force corresponding to the first discharge of the motor unit. RESULTS
Comparison of RTFs during ramp and ballistic contraction RTFs of motor units activated during both ramp (ramp RTF) and ballistic (ballistic RTF) contractions were compared. In AP motor units, reference RTFs were obtained during slow ramp contractions 5 kg and over at 1 kg/s force rate. Reference RTFs of FDI motor units were obtained during ramp contractions 3 kg and over at 0.6 kg/s force rate. During ballistic
B AP (N=27) /J:soo°
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Fig. 3. Comparison between ramp RTF and ballistic RTF. Ramp RTFs of AP motor units (A) were obtained from the force exertion 5 kg and over a force rate of 1 kg/s. Ramp RTFs of FDI motor units (13) were derived from the exertion 3 kg and over at 0.6 kg/s force rate. Ballistic RTFs were obtained when 3 kg forces were exerted by AP, and when 1 kg by FDI as fast as possible.
92 3000
TABLE I
Arrangement of motor units according to R TF and R TF changing type
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1000 2000 5000
Time to peak force ( msec )
Fig. 4. RTF changes of several motor units of A P during force exertions to 3 kg force level in various force speeds. RTF change processes were distinguished type I, type II and type III.
contraction were lowest. Three types of RTF change processes were distinguished: type I, relatively low RTFs lowered slightly even when force speed changed widely; type II, RTFs decreased irregularly with changes of force speed increment; and type III, relatively high RTFs decreased regularly with changes of force speed increment. Forty-one % of type I, 55%
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Values of RTFs and RTF change in type are arranged according to rank order of ramp RTF for 27 A P motor units (A) and 28 FDI motor units (B).
5
1000 2000 5000
Time to peak force ( msec )
Fig. 5. RTF changes of several motor units of FDI during force exertions to 1 kg level in various force speeds. Distinguished RTF change processes were type I and type II.
R TF (ramp)
R TF (ballistic)
R TF changing
(g)
(g)
type
(A) AP 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
20 70 90 90 120 180 270 310 510 510 610 1020 1380 1400 1880 1900 1970 2050 2150 2190 2250 2260 2460 2820 2840 2950 4100
0 0 0 0 0 0 0 0 0 0 0 0 0 0 65 80 0 0 165 85 190 0 0 70 0 45 145
I I I I I I I I I I I II II II II II II II It II III II II II II II II
(B) FDI 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28
10 60 90 100 160 210 240 270 410 680 700 760 870 960 990 1020 1180 1270 1290 1360 1490 1500 1520 1540 1640 1950 2300 2630
0 0 0 0 10 0 0 0 0 0 0 0 80 0 0 75 40 30 0 0 10 10 10 75 0 20 0 60
I I I I I I I I II II II lI II II II II II II II II II II II II II II II ll
93 of type II and 4% of type III were found among 27 AP motor units as shown in Table IA. FDI motor unit. When the forces were exerted by abduction of the index finger at various force speeds, RTFs of 28 FDI motor units from 5 subjects were studied in the same way as in the AP experiment. Results of 5 motor units obtained by the same method as in Fig. 4 are shown in Fig. 5. The criteria used in Fig. 5 to distinguish the changes in the type of RTF were the same as in the AP motor unit experiment (Fig. 4). FDI motor units investigated in this experiment revealed almost the same RTF change process as those of AP motor units. Twenty eight % of type I, 71% of type II and 0% of type III were found in this experiment as shown in Table IB. Over half of the motor units measured were of type II. It is a remarkable fact that RTFs of type I motor units are very low and the range of change is very small. Relation between R T F and R T F changing type. The values of RTFs of 27 AP and 28 FDI motor units compared with their respective RTF changing type are shown in Table I. Motor units were arranged, according to RTF rank order from low to high. It appears that low RTF motor units in ramp contraction correspond to type I of RTF change. In addition, RTFs of the majority of type I and type II motor units during ballistic contraction were zero. RTFs of half of the total number of motor units investigated were classified into type II. There was no significant relation between values of RTF during ramp and ballistic contraction in type II motor units. Only one type III motor unit was found in the present experiment. DISCUSSION The purpose of the present study was to explore more fully the RTF change of motor units during voluntary force exertion at various force speeds. For this purpose, it is very important that the activity of a single motor unit must be recorded stably during voluntary contractions over a wide range of force speeds. The wire electrodes used in the present experiment were capable of leading and recording several motor unit discharges. Most of the electrodes inserted into the muscle maintained their selectivity during ramp and even ballistic contraction up to the 3 kg isometric force for over 2 h. Therefore, it seems that those
electrodes were of a suitable type for recording motor unit discharges during ballistic contraction within certain limits. It has been reported by Desmedt and Godaux 5-7 that the RTFs reduced in rapid contraction as compared with slow ramp contaction. Our results which were performed more extensively than in the Desmedt and Godaux experiments in regard to force speed institution, corresponded with their reports in principle. As shown in Fig. 3, high RTFs during ramp contraction revealed broad reduction and low RTFs revealed limited reduction when ballistic contractions were performed. The RTF change processes of the 55 motor units examined were classified into 3 types as shown in Figs. 4, 5 and Table I. Most of the motor units belonged to the type II, which revealed that the RTF change irregularly in spite of the linear change of time to peak force. It has been pointed out that afferent impulses from the sensory nerves have a crossing influence on RTF changes of the motor units; that is, a high RTF of motor unit is changed to low and low RTF to high 9. In the present study, RTF changes of most motor units constricted to zero, not in a crossing fashion but in one direction. Although the motoneuron which innervates the activated muscle fiber is exposed to many sensory input influences in the spinal motor pool, it is not possible that the RTF changes during contraction at various speeds were affected by the sensory input only. Other influencing factors must also be considered in regard to RTF changes during voluntary contraction at different speeds. It is suggested that the supraspinal outflow concerning volitional effort may influence the RTF changes. However, about one third of the motor units were classified as type I. A low RTF means that the motor unit has a chance of contributing to force development of the whole muscle force in an early phase. Furthermore, a low RTF motor unit is always recruited during force exertion of the whole muscle; no matter whether the force is large or small. It seems that such motor units must be characterized by high durability to repetitive contraction rather than for their contraction strength. It is reasonable to consider that low RTF motor units are related to the slow twitch muscle fiber type as pointed out by Burke et al. 2-4 and that they are also related to the small size moto-
94 n e u r o n as pointed out by H e n n e m a n and colleagues TM 14,19. Type III motor units changed their R T F regurlarly according to speed changes, however they were found only rarely. The neuronal variation of voluntary effort might cause the various changes of the motor unit activities. We cannot overlook the possibility that the type III R T F change of motor unit might be one of the manifestations of n e u r o n a l activities. In such a case, this rare appearance of type III R T F change of motor unit would be significant. Looking back at the R T F test in this study, the first discharged action potential of a motor unit was related to the force of a whole muscle in only one series of force speed changes (Figs. 4 and 5). In order to describe the R T F changing type of motor units, it is
REFERENCES 1 Borg, J., Grimby, L. and Hannerz, L., Axonal conduction velocity and voluntary discharge properties of individual short toe extensor motor units in man, J. Physiol. (London), 277 (1978) 143-152. 2 Burke, R.E., Levine, D.N., Zajac, F.E., Tsairis, P., and Engel, W.K., Mammalian motor units; physiological histochemical correlation in three types in cat gastrocnemius, Science, 174 (1971) 709-712. 3 Burke, R.E., Levine, D.N., Tsairis, P. and Zajac, F.E., Physiological types and histochemical profiles in motor units of the cat gastrocnemius, J. Physiol. (London), 234 (1973) 723-748. 4 Burke, R.E., Levine, P.N., Salcman, M. and Tsairis, P., Motor units in cat soleus muscle; physiological, histochemical and morphological characteristics, J. Physiol. (London), 238 (1974) 503-514. 5 Desmedt, J.E. and Godaux, E., Fast motor units are not preferentially activated in rapid voluntary contraction in man, Nature (London), 267 (1977) 717-719. 6 Desmedt, J.E. and Godaux, E., Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle, J. Physiol. (London), 267 (1977) 673-693. 7 Desmedt, J.E. and Godaux, E., Ballistic contractions in fast or slow human muscles: discharge patterns of single motor units, J. Physiol. (London), 285 (1978) 185-196. 8 Freund, H.-J., Buedingen, H.-J. and Dietz, V., Activity of single motor units from human forearm muscles during voluntary isometric contraction, J. Neurophysiol., 38 (1975) 933-946. 9 Garnett, R. and Stephens, J.A., Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man, J. Physiol. (London), 311 (1981) 463-472. 10 Grimby, L. and Hannerz, J., Firing rate and recruitment order of toe extensor motor units in different modes of voluntary contraction, J. Physiol. (London), 264 (1977) 865-879.
neccessary to obtain many R T F data at each speed in many series of force speed changes. Therefore, it is uncertain whether each R T F change of a motor unit (Figs. 4, 5 and Table I) is inherent to that particular motor unit or not in this stage. F u r t h e r research is proposed to clarify the exact nature of these phenomena. Nevertheless, the present results indicated that RTFs might well be quite variable even at the same force amplitude if the forces are exerted at various speeds. The p h e n o m e n o n which has been pointed out previously by Desmedt and Godaux 5-7 was further clarified by a precise observation in this experiment.
11 Grimby, L., Hannerz, J. and Hedman, B., Contraction time and voluntary discharge properties of individual short toe extensor motor units, J. Physiol. (London), 289 (1979) 191-201. 12 Hannerz, J,, Discharge patterns of motor units in relation to recruitment order in voluntary contraction, Acta Physiol. Scand., 91 (1974) 374-384. 13 Henneman, E., Relation between size of neurons and their susceptibility to discharge, Science, 126 (1957) 1345-1347. 14 Henneman, E., Somjen, G. and Carpenter, D.O., Functional significance of cell size in spinal motoneurons, J. Neurophysiol., 28 (1965) 560-580. 15 Kurata, H., Ogawa, Y. and Masuda, M., Characteristics of single human motor units during various modes of contraction, Jikeikai Med. J., 27 (1980) 19t-202. 16 Milner-Brown, H.S., Stein, R.B. and Yemm, R.R., The contractile properties of human motor units during voluntary isometric contractions, J. Physiol. (London), 228 (1973) 285-306. 17 Milner-Brown, H.S., Stein, R.B. and Yemm, R.R., The orderly recruitment of human motor units during voluntary isometric contraction, J. Physiol. (London), 230 (1973) 350-370. 18 Milner-Brown, H.S., Stein, R.B. and Yemm, R.R., Changes in firing rate of human motor units during linearly changing voluntary contraction, J. Physiol. (London), 230 (1973) 371-390. 19 Somjen, G., Carpenter, D.O. and Henneman, E., Responses of motoneurons of different size to graded stimulation of supraspinal center of the brain, J. Neurophysiol., 28 (1965) 958-965. 20 Stephens, J.A. and Usherwood, T.P., The mechanical properties of human motor units with special reference to their fatiguability and recruitment threshold, Brain Research, 125 (1977) 91-97. 21 Tanji, J. and Kato, M., Recruitment of motor unit in voluntary contraction of a finger muscle in man, Exp. Neurol., 40 (1973) 753-770.
Brain Research, 372 (1986) 89-94 Elsevier BRE 11639
Recruitment Threshold Force and its Changing Type of Motor Units during Voluntary Contraction at Various Speeds in Man TSUGUTAKE YONEDA, KAZUO OISHI, SEI FUJIKURA and AYAKO ISHIDA
Department of Physiology, School of Physical Education, Juntendo University, Fujisaki, Narashino, Chiba 275 (Japan) (Accepted August 27th, 1985)
Key words: voluntary force exertion - - ballistic contraction - - ramp contraction - - isometric force - motor unit - - threshold force - - force rate
The motor unit discharges in human hand muscles were recorded during voluntary isometric contraction. Bipolar wire electrodes were inserted in the right adductor pollicis muscle (AP) and first dorsal interosseous muscle (FDI) for the recordings. Motor unit activities from these muscles were investigated when subjects exerted voluntary force to each target force at various speeds. On 27 motor units of AP and 28 motor units of FDI, ramp RTF and ballistic RTF were compared. Furthermore, RTF changes of motor units with the different force speeds were investigated. It is clear that the RTF of the motor units during ballistic contractions were lower than those during ramp contraction. The processes of motor unit RTF changes were classified into 3 types: RTF of type I motor units were relatively low and decreased slightly even when force speed increased widely; RTF of type II motor units were relatively high and decreased irregularly; and RTF of type III motor units, which appeared rarely, decreased their relatively high RTF with increases of force speed increment. It is suggested that the volitional outflow related with the force speed change to the spinal motor pool might cause the different RTF change effects in the various motor units.
INTRODUCTION The value of the exerted voluntary force corresponding to the first discharge of a single m o t o r unit which participates in the force d e v e l o p m e n t has been termed the recruitment threshold force ( R T F ) of the m o t o r unitS,IS-20. Each m o t o r unit, in the whole muscle, has different R T F . Therefore, the m o t o r units were recruited at different times during force development. In other words, m o t o r units during force development were recruited in an o r d e r based on R T F , from low to high. It has been p o i n t e d out by several workers that RTFs are related to the several physiological properties of m o t o r units, n a m e l y the size of the motoneuron13,14.20, the conduction velocity of the m o t o n e u ronl, 8, the discharge frequency 12 and the contraction timeS,16,17A9. F u r t h e r m o r e , it has been shown that the contraction time of a m o t o r unit having a high discharge frequency p r o p e r t y is smaller than that of a
low discharge frequency m o t o r unitlO, n. Therefore, R T F might be an i m p o r t a n t index to explore the mechanisms of m o t o r unit recruitment during voluntary contractio.n in a wide speed range. Even though the R T F shows the p r o p e r t i e s of a m o t o r unit, R T F s of individual m o t o r units are not a fixed index 21. According to the studies by D e s m e d t and GodauxS-7, the R T F of a m o t o r unit during rapid (ballistic) contraction is lower than that during slow r a m p contraction. D e s m e d t and G o d a u x showed that the R T F varied with voluntary force speed. The present study was u n d e r t a k e n to clarify how the force speed effects the m o t o r unit R T F change, and how the m o t o r units classified in R T F change type in hand muscles in man. MATERIALS AND METHODS Experiments were carried out on the a d d u c t o r pollicis muscle ( A P ) and the first dorsal interosseous
Correspondence: T. Yoneda, Department of Physiology, School of Physical Education, Juntendo University, Fujisaki, Narashino, Chiba 275, Japan. 0006-8993/86/$03.50 © 1986 Elsevier Science Publishers B.V. (Biomedical Division)
90 muscle (FDI) of the right hand. Subjects were healthy adult men.
Procedures Subjects sat on a chair, and their right forearm and hand was fixed as shown in Fig. 1. The subject was instructed to perform a voluntary movement with the thumb and the index finger, respectively, after the oral signal of the examiner. The subject could watch the amplitude and the time course of exerted forces on a sweep screen of a two-channel monitor oscilloscope. Three modes of force exertions were carried out as follow: (1) slow ramp contraction with the time to peak forces of 1, 2 and 5 s by visual tracking of the target force development; (2) fast ramp contractions with the time to peak forces ranging from 0.15 to 1 s without tracking but with monitoring; and (3) ballistic contractions performed as fast as possible follow-
A
ing relaxation. As for the fast ramp and ballistic contraction, target force level was set as a horizontal sweep line on the screen of the monitor scope, and subjects performed the force matching task accordingly. In the case of the AP experiment, the joint angle of the thumb was set at 20 ° . The target force level was set at 3 kg throughout the experiment. In the FDI experiment, the joint angle between the thumb and index finger was set at 40 ° . The target force level was set at 2 kg, Procedures of force exertion were the same as in the AP experiment.
Force recordings The voluntary isometric force exerted by the subject while performing the adduction or the abduction movement by the fingers, was recorded by means of a transduction of the strain gauge which was put on a stainless steel pole (Fig. 1, P; 10 mm diameter) with a trigger holder (Fig. 1, H) of thumb and index finger. The gauge signal was amplified by a carrier amplifier ( K Y O W A , DPM-350A) and led to a data recorder and stored on magnetic tape. The force signal was also led to a monitor oscilloscope separately. The recordings of motor unit discharges and 3 kg force curves of the thumb during 3 different force speeds are shown in Fig. 2.
Recording of the motor unit activity
B
B1
B2
H
Fig. 1. A: general view of hand fixation of the experiment for adductor pollicis muscle. B: hand fixation for first dorsal interosseous muscle experiment viewed from the side (B2) and from the top (B1). F, fixed belt; G, strain gauge; H, plastic trigger holder; P, plate; and S, stainless steel pole. Arrows in A and B1 indicate the direction of exerted force.
Plastic embedded fine bipolar electrodes were made from two fine polyurethane coated copper wires (50 ,urn diameter). The wires of these electrodes were the same as those which were used in Kurata's coil shaped electrode ]5. Less than 10 mm of the tips of two wires were embedded in a little acryl-resin in a parallel position. After a few millimeters of the tip was cut off by a razor blade, the electrode was inserted into the muscle via a 1/2 gauge hypodermic needle. These electrodes were selective to record the action potentials of several motor units and were capable of recording over 2 h. Action potentials of motor units were amplified by a high input impedance extracellular amplifier ( D I A Medical System Co., DPA-100E) and stored on a magnetic tape together with the force signal by a data recorder.
Measurement of R TF Force signals of the whole muscle and action po-
91 a JJ..[l I[)Ilfltllll[IJ~Ulll~I.. I1 rill []Nlli]lllilllllIlllltI .................................................
--~
E5
% C
'~,,~' Fig. 2. Serial recordings of forces and motor unit activities in adductor pollicis muscle at 3 force speeds. A, 5 s ramp contraction; 13, 0.4 s ramp contraction; C, ballistic contraction. Upper traces are motor unit electrical activities recorded by means of fine wire electrodes and lower traces are force curves. The peak forces were of the same amplitude. It was observed that the RTF of a certain motor unit 'a' which was shown in A of ramp contraction lowered with force speed increment as shown in B and C.
contraction RTFs were measured when the force exertion achieved 3 kg target force in AP and 1 kg in FDI. In Fig. 3, 23 pairs of RTF data during ramp and ballistic contractions of AP motor units and 27 pairs of RTF data of FDI motor units are shown. It is clear that RTFs during ballistic contraction were lower than those during ramp contraction. The values of many RTFs during ballistic contraction were zero, although RTFs during ramp contraction were not entirely zero.
Relationship between R TF and force speed AP motor unit. When the 3 kg isometric forces were exerted by thumb adduction at various force speeds, serial changes of RTF of AP motor units to force speeds were studied. When a certain motor unit was activated during both ballistic and ramp contraction, RTFs of the motor unit were measured at various speeds. The results derived from each series of experiments of 5 motor units among 27 motor units of 5 subjects are shown in Fig. 4. In all cases, RTFs decreased with force speed changes from low to high, and those during ballistic
A 5000-
tentials of the motor unit stored on a magnetic tape were then transferred to oscillopaper. This oscillogram was used for motor unit identification and RTF measurement. Single motor units were identified from the amplitude and shape of the action potentials in a routine manner. RTF of the motor unit was expressed as the value of the whole muscle force corresponding to the first discharge of the motor unit. RESULTS
Comparison of RTFs during ramp and ballistic contraction RTFs of motor units activated during both ramp (ramp RTF) and ballistic (ballistic RTF) contractions were compared. In AP motor units, reference RTFs were obtained during slow ramp contractions 5 kg and over at 1 kg/s force rate. Reference RTFs of FDI motor units were obtained during ramp contractions 3 kg and over at 0.6 kg/s force rate. During ballistic
B AP (N=27) /J:soo°
4000.
'°°°l FDi (N,28)
I__
/,000
I 3000
-3000
3000-
2000
1000
20110
-I~
0
B(:illilttic
.3000
Romp
I000
1000
0
0
lklllkltic
Ramp
Fig. 3. Comparison between ramp RTF and ballistic RTF. Ramp RTFs of AP motor units (A) were obtained from the force exertion 5 kg and over a force rate of 1 kg/s. Ramp RTFs of FDI motor units (13) were derived from the exertion 3 kg and over at 0.6 kg/s force rate. Ballistic RTFs were obtained when 3 kg forces were exerted by AP, and when 1 kg by FDI as fast as possible.
92 3000
TABLE I
Arrangement of motor units according to R TF and R TF changing type
Ill
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--<>
7'- r- <3
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Unit no. /
9
/
,/
t
:/
II/
e-
/
l OOC
k/
O~
0
500
1000 2000 5000
Time to peak force ( msec )
Fig. 4. RTF changes of several motor units of A P during force exertions to 3 kg force level in various force speeds. RTF change processes were distinguished type I, type II and type III.
contraction were lowest. Three types of RTF change processes were distinguished: type I, relatively low RTFs lowered slightly even when force speed changed widely; type II, RTFs decreased irregularly with changes of force speed increment; and type III, relatively high RTFs decreased regularly with changes of force speed increment. Forty-one % of type I, 55%
1500
I ! / . '• v
8 ~1ooo
/
0
8
Values of RTFs and RTF change in type are arranged according to rank order of ramp RTF for 27 A P motor units (A) and 28 FDI motor units (B).
5
1000 2000 5000
Time to peak force ( msec )
Fig. 5. RTF changes of several motor units of FDI during force exertions to 1 kg level in various force speeds. Distinguished RTF change processes were type I and type II.
R TF (ramp)
R TF (ballistic)
R TF changing
(g)
(g)
type
(A) AP 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
20 70 90 90 120 180 270 310 510 510 610 1020 1380 1400 1880 1900 1970 2050 2150 2190 2250 2260 2460 2820 2840 2950 4100
0 0 0 0 0 0 0 0 0 0 0 0 0 0 65 80 0 0 165 85 190 0 0 70 0 45 145
I I I I I I I I I I I II II II II II II II It II III II II II II II II
(B) FDI 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28
10 60 90 100 160 210 240 270 410 680 700 760 870 960 990 1020 1180 1270 1290 1360 1490 1500 1520 1540 1640 1950 2300 2630
0 0 0 0 10 0 0 0 0 0 0 0 80 0 0 75 40 30 0 0 10 10 10 75 0 20 0 60
I I I I I I I I II II II lI II II II II II II II II II II II II II II II ll
93 of type II and 4% of type III were found among 27 AP motor units as shown in Table IA. FDI motor unit. When the forces were exerted by abduction of the index finger at various force speeds, RTFs of 28 FDI motor units from 5 subjects were studied in the same way as in the AP experiment. Results of 5 motor units obtained by the same method as in Fig. 4 are shown in Fig. 5. The criteria used in Fig. 5 to distinguish the changes in the type of RTF were the same as in the AP motor unit experiment (Fig. 4). FDI motor units investigated in this experiment revealed almost the same RTF change process as those of AP motor units. Twenty eight % of type I, 71% of type II and 0% of type III were found in this experiment as shown in Table IB. Over half of the motor units measured were of type II. It is a remarkable fact that RTFs of type I motor units are very low and the range of change is very small. Relation between R T F and R T F changing type. The values of RTFs of 27 AP and 28 FDI motor units compared with their respective RTF changing type are shown in Table I. Motor units were arranged, according to RTF rank order from low to high. It appears that low RTF motor units in ramp contraction correspond to type I of RTF change. In addition, RTFs of the majority of type I and type II motor units during ballistic contraction were zero. RTFs of half of the total number of motor units investigated were classified into type II. There was no significant relation between values of RTF during ramp and ballistic contraction in type II motor units. Only one type III motor unit was found in the present experiment. DISCUSSION The purpose of the present study was to explore more fully the RTF change of motor units during voluntary force exertion at various force speeds. For this purpose, it is very important that the activity of a single motor unit must be recorded stably during voluntary contractions over a wide range of force speeds. The wire electrodes used in the present experiment were capable of leading and recording several motor unit discharges. Most of the electrodes inserted into the muscle maintained their selectivity during ramp and even ballistic contraction up to the 3 kg isometric force for over 2 h. Therefore, it seems that those
electrodes were of a suitable type for recording motor unit discharges during ballistic contraction within certain limits. It has been reported by Desmedt and Godaux 5-7 that the RTFs reduced in rapid contraction as compared with slow ramp contaction. Our results which were performed more extensively than in the Desmedt and Godaux experiments in regard to force speed institution, corresponded with their reports in principle. As shown in Fig. 3, high RTFs during ramp contraction revealed broad reduction and low RTFs revealed limited reduction when ballistic contractions were performed. The RTF change processes of the 55 motor units examined were classified into 3 types as shown in Figs. 4, 5 and Table I. Most of the motor units belonged to the type II, which revealed that the RTF change irregularly in spite of the linear change of time to peak force. It has been pointed out that afferent impulses from the sensory nerves have a crossing influence on RTF changes of the motor units; that is, a high RTF of motor unit is changed to low and low RTF to high 9. In the present study, RTF changes of most motor units constricted to zero, not in a crossing fashion but in one direction. Although the motoneuron which innervates the activated muscle fiber is exposed to many sensory input influences in the spinal motor pool, it is not possible that the RTF changes during contraction at various speeds were affected by the sensory input only. Other influencing factors must also be considered in regard to RTF changes during voluntary contraction at different speeds. It is suggested that the supraspinal outflow concerning volitional effort may influence the RTF changes. However, about one third of the motor units were classified as type I. A low RTF means that the motor unit has a chance of contributing to force development of the whole muscle force in an early phase. Furthermore, a low RTF motor unit is always recruited during force exertion of the whole muscle; no matter whether the force is large or small. It seems that such motor units must be characterized by high durability to repetitive contraction rather than for their contraction strength. It is reasonable to consider that low RTF motor units are related to the slow twitch muscle fiber type as pointed out by Burke et al. 2-4 and that they are also related to the small size moto-
94 n e u r o n as pointed out by H e n n e m a n and colleagues TM 14,19. Type III motor units changed their R T F regurlarly according to speed changes, however they were found only rarely. The neuronal variation of voluntary effort might cause the various changes of the motor unit activities. We cannot overlook the possibility that the type III R T F change of motor unit might be one of the manifestations of n e u r o n a l activities. In such a case, this rare appearance of type III R T F change of motor unit would be significant. Looking back at the R T F test in this study, the first discharged action potential of a motor unit was related to the force of a whole muscle in only one series of force speed changes (Figs. 4 and 5). In order to describe the R T F changing type of motor units, it is
REFERENCES 1 Borg, J., Grimby, L. and Hannerz, L., Axonal conduction velocity and voluntary discharge properties of individual short toe extensor motor units in man, J. Physiol. (London), 277 (1978) 143-152. 2 Burke, R.E., Levine, D.N., Zajac, F.E., Tsairis, P., and Engel, W.K., Mammalian motor units; physiological histochemical correlation in three types in cat gastrocnemius, Science, 174 (1971) 709-712. 3 Burke, R.E., Levine, D.N., Tsairis, P. and Zajac, F.E., Physiological types and histochemical profiles in motor units of the cat gastrocnemius, J. Physiol. (London), 234 (1973) 723-748. 4 Burke, R.E., Levine, P.N., Salcman, M. and Tsairis, P., Motor units in cat soleus muscle; physiological, histochemical and morphological characteristics, J. Physiol. (London), 238 (1974) 503-514. 5 Desmedt, J.E. and Godaux, E., Fast motor units are not preferentially activated in rapid voluntary contraction in man, Nature (London), 267 (1977) 717-719. 6 Desmedt, J.E. and Godaux, E., Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle, J. Physiol. (London), 267 (1977) 673-693. 7 Desmedt, J.E. and Godaux, E., Ballistic contractions in fast or slow human muscles: discharge patterns of single motor units, J. Physiol. (London), 285 (1978) 185-196. 8 Freund, H.-J., Buedingen, H.-J. and Dietz, V., Activity of single motor units from human forearm muscles during voluntary isometric contraction, J. Neurophysiol., 38 (1975) 933-946. 9 Garnett, R. and Stephens, J.A., Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man, J. Physiol. (London), 311 (1981) 463-472. 10 Grimby, L. and Hannerz, J., Firing rate and recruitment order of toe extensor motor units in different modes of voluntary contraction, J. Physiol. (London), 264 (1977) 865-879.
neccessary to obtain many R T F data at each speed in many series of force speed changes. Therefore, it is uncertain whether each R T F change of a motor unit (Figs. 4, 5 and Table I) is inherent to that particular motor unit or not in this stage. F u r t h e r research is proposed to clarify the exact nature of these phenomena. Nevertheless, the present results indicated that RTFs might well be quite variable even at the same force amplitude if the forces are exerted at various speeds. The p h e n o m e n o n which has been pointed out previously by Desmedt and Godaux 5-7 was further clarified by a precise observation in this experiment.
11 Grimby, L., Hannerz, J. and Hedman, B., Contraction time and voluntary discharge properties of individual short toe extensor motor units, J. Physiol. (London), 289 (1979) 191-201. 12 Hannerz, J,, Discharge patterns of motor units in relation to recruitment order in voluntary contraction, Acta Physiol. Scand., 91 (1974) 374-384. 13 Henneman, E., Relation between size of neurons and their susceptibility to discharge, Science, 126 (1957) 1345-1347. 14 Henneman, E., Somjen, G. and Carpenter, D.O., Functional significance of cell size in spinal motoneurons, J. Neurophysiol., 28 (1965) 560-580. 15 Kurata, H., Ogawa, Y. and Masuda, M., Characteristics of single human motor units during various modes of contraction, Jikeikai Med. J., 27 (1980) 19t-202. 16 Milner-Brown, H.S., Stein, R.B. and Yemm, R.R., The contractile properties of human motor units during voluntary isometric contractions, J. Physiol. (London), 228 (1973) 285-306. 17 Milner-Brown, H.S., Stein, R.B. and Yemm, R.R., The orderly recruitment of human motor units during voluntary isometric contraction, J. Physiol. (London), 230 (1973) 350-370. 18 Milner-Brown, H.S., Stein, R.B. and Yemm, R.R., Changes in firing rate of human motor units during linearly changing voluntary contraction, J. Physiol. (London), 230 (1973) 371-390. 19 Somjen, G., Carpenter, D.O. and Henneman, E., Responses of motoneurons of different size to graded stimulation of supraspinal center of the brain, J. Neurophysiol., 28 (1965) 958-965. 20 Stephens, J.A. and Usherwood, T.P., The mechanical properties of human motor units with special reference to their fatiguability and recruitment threshold, Brain Research, 125 (1977) 91-97. 21 Tanji, J. and Kato, M., Recruitment of motor unit in voluntary contraction of a finger muscle in man, Exp. Neurol., 40 (1973) 753-770.