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Average muscle tension triggered by stimulation of gamma fusimotor fibers
Neuroscieace Letters, 6 {1977) 35--39 © Elsevier/North-Holland Scientific Publishers Ltd.
35
AVERAGE M U S C L E T E N S I O N T R I G G E R E D B Y STIMULATION OF GAMMA F U S I M O T O R FIBERS
SABURO HOMMA and YOSHIO NAKAJIMA
Department of Physiology, School of Medicine, Chiba University, Chiba, 280 (Japan) (Received June 15th, 1977) (Accepted June 23rd, 1977 )
SUMMARY
Average soleus muscle tension of the anesthetized cat, triggered by repetitive stimulation to a fine ventral root filament of LT, was isometrically recorded by use of blocking methods of the alpine decending impulse~ and it showed a twitch-like contraction with very rapid time coulse. Its mean time to peak and half decay time of relaxation in 12 observations was 21.7 and 26.8 msec, respectively. It was concluded that such a rapid concentration corresponds to a twitch of nuclear chain fibers. It was shown that repetitive stimulation of gamma fusimotor fibers during a pause of spindle discharges caused by an isometric extrafusal muscle contraction was sufficient to fill out the pause with impulse activity [ 1--4 ]. On the other hand, it has been noted that spindle afferent impulses follow the rhythm of the gamma fusimotor stimulation at a rate of up to ! 8 0 shocks/sec [5]. This phenomenon was called a 'driving', which has since been attributed to characteristics of static gamma fusimotor fibers in the cat [6--8] and also in the rabb|t [9--11]. Furthermore, the driving is assumed to be elicited by minute twitches of intrafusal muscle fibers. It has become clear that there exist definite relations between gamma fusimotor axons and contractile properties of intrafusal muscle fibers (see general discussion [12] ). Bessou and Pages [13] and Boyd [ 14] cinematographically recorded a displacement of intrafusal muscle fibers elicited by either static or dynamic gamma fusimotQr stimulation in cat tenuissimus. According to them, stimulation of static gamma axons innervating nuclear chain fibers elicited a rapid and large contraction, whereas that of static and/or dynamic gamma axons innervating nuclear bag fibers produced a slow and" small contraction. Stimulation of static axons innervating nuclear bag fibers,however, eliciteda more rapid and largercontraction than that of nuclear bag fibersinnervated by dynamic g a m m a axons. In our experiments, it was investigatedto obtain isometric twitch curves of h~tra~sal muscle fibers of cat soleus elicitedby electricstimulation of g a m m a
36
fusimotor fibers. The experiments were ~arned out on adult cats anesthetized with urethane and chloralose. All the hindlimb nerves on the experimental side were cut except the lateral gastrocnemius nerve. The soleus and its tendon were separated from surrounding tissues, care being taken to keep the blood supply and nerce to the muscle intact as far as possible. In order ~ record an isometric tension o f the soleus muscle, Achilles tendon was tightly connected with a steel plate on which a stre.in gauge was attached. Minimal detectable tension of the tension recording system was 1 rag. The soleus muscle was stretched 4 mm from its resting position throughout the experiments. After laminectom~, both ventral and dorsal roots from L5 to $1 were cut at their entry to the spinal cord. The ventral root of L7 was splitted into a fine filament, which was mounted on two pah-s o f silver electrodes. One pair of electrodes, which will be referred t o (A) electrodes, wa~ supplied with rectangular pulses with 0.5 msec duration at a rate of 0.8 Hz. It~ stimulus intensity was adjusted to 10 times the threshold of soleus muscle contraction. It is certain that this intensity is sufficient to stimulate gamma fusimotor axons. The soleus muscle tensions elicited by the above stimuli were recorded for 500 msec. The other pair of electrodes, situated distally to the (A) electrodes, was supplied with rectangular pulses with 0.5 msec duration and with random intervals of 2--5 reset. These electrodes will be called (B) electrodes. The soleus contractions elicited by the random rectangular pulses were tetanie and the tetanic contraction curves were smooth. Even if, however, there exist peaks in the tetanic contraction curves in relation to each random pulse, the appearance
I
100 msec
Fig. 1. A: twitch tension when the stimulus intensity was adjusted to 10 times the threshold of alpha motor fibers and the a~pha descending impulses were b~ocked by stimulation of random rectangular pulses under the other distal electrodes. The tension ~vas averaged 100 times. B: twitch tension elicited by stimulation of ventral root filament.
37 of the peaks must be random. The stimulus in~nsity of the random rectangular pulses was adjusted such that the alpha descending impulses elicited by the (A) electrodes, which elicit the twitch contractions, are blocked under the (B) electrodes. Since the intensity of the (B) electrodes was not strong enough to block gamma efferent impulses, the gamma descending impulses can pass under the (B) electrodes and elicit twitch contractions of the intrafusal muscle fibers in soleus muscle. Based on the methods stated above, the soleus muscle tensions were isometrically recorded and averaged for 500 msec, triggered by the 0.8 Hz pulses of the (A) electrodes. The averaging of the tension showed a twitch-like contraction with very rapid time course as shown in Fig. 1A. Fig. 1B shows a twitch tension of soleus extrafusal muscle contraction elicited by the (A) electrodes without block by the (B) electrodes. Time to peak and half decay time of relaxation was 71.0 and 128.6 msec, respectively. Thougb it is not clear how many alpha efferent fibers this ventral filament consists of, the maximum tension of Fig. 1B was 3.2 g° Fig. 1A shows a tension curve obtained from 100 times averaging by gamma efferent impulses. Time to peak and half decay time of relaxation was 17.1 and 31.4 msec, respectively. The time ~ourse is very rapid and the peak tension (61.3 mg) is very small as compared with those of the extrafusal contraction. It was assumed from these results that the contraction curve is that of intrafusal muscle fibers. In this particular case, a slow and small contraction is seen following the rapid contraction. The contraction curve apparently suggests that it is composed of two components of different time courses. However, such slow and small contraction could not be recorded in all cases. In measur;mg the time to peak and half decay time, the latter could not often be measured when accompanied with slow contraction. The results of the experiments are shown in Table I. It is obvious from Table I i~,hat the time course and the peak tension of the intrafusal muscle fibers are rap~d and small, respectively, as compared with those of extrafusal muscle fibers. S:ince it was occasion'~y difficult to block the twitch contraction completely under the (B) electrodes, Flaxedil ® was intravenously injected in a dose of about 3 mg/kg in order to complete the block by the (B) electrodes. Results of intrafusal muscle contraction under the Flaxedil ~ administration are 'also shown in Table I. It is clear that the Flaxedil ® does not affect the contraction curve of intrafusal muscle fibers. Minimum tension of the intrafusal muscle contractions lies between 7.7 and 81.~ rag. This variation of recorded tension may result from the difference in number of gamma efferent fibers stimulated in each case. Bessou and Pages [13] and Boyd [14] cinemato~aphical!y measured the time course o£ the displacement accompanied with the contractions of intrafusal muscle fibers in cat tenuissimus. They showed that the time course and the displacement of nuclear chain fibers are rapid and large, respectively. It was noticed that the time to peak and relaxation time were 40 and 80 rnsec, respectively.
38 TABLE I Peak tension (rag)
Time to peak (reset)
Half decay time (msec)
Duration at half tension (n~c)
Without Flaxedfl ® 1
7.7
26.5
--
--
2
8.7
22.1
3
9.2
17.6
26.5 26.5
38.2 38.2
4
17.4
23.5
--
--
5
22.0 25.6 45.7
26.5 27.6 25.6
--
--
41.6 30.6
54.4 52.9
28.8 58.8 61.3 65.0 81.3 36.0 ± 25.4
17.1 20.0 17.1 16.6 20.0 21.7 ± 4.2
11.4 28.6 31.4 15.7 28.6 26.8 ± 8.8
6
7 With Flaxedil ® 1 2 3a 4 5 Mean ± SD
20.0 42.9 42.9 ~ 24.3 37.1 39.9 ± 11.4
a See Fig. 1.
Our results of isometric contraction curves showed a time to peak and a half decay time of relaxation being about 21.7 and 26.8 msec, respectively, and are considerably short as compared with those of Bessou and Pages [13] and Boyd [ 14]. The driving, as mentioned above, which was assumed to be elicited by minute twitches of intmfusal muscle fibers will be achieved by such a short twitch contraction as shown in Fig. 1A. Since the displacement of nuclear chain fibers large in tenuissimus muscle according to Bessou a n d Pages [13] Boyd [14], it ~ be v ~ d to c0nclude that the large displacemen~ of nuclear c h ~ fibers was predominatly recorded a~ a large tension in this inves. • tigation. .... It was concluded that average tension triggered b y repetitive stimulation of the ventral root ~ a m e n t as shown i n Fig. 1A corresponds to a twitch contraction of nuclear c h ~ fibers elicited by static gamma fusimotor fibers. REFERENCES 1 Matthews, B.H.C., Nerve endings in mamraalian muscle, J. Physiol., 78 (1933) 1--53. 2 Leksell, L., Th~ action potential and excitatory effects of the small ventral root fibers to skeletal muscle, Acta physiol, stand,, I0, Supp|. 31 (1945~ 1--81. 3 Hun~, CICi ~ d r ~ e p t 0 r discharges during muscle contraction. J. ~ y s i o l . , 113 (1951) ~298--315, i / 4 o : efferent small-nerve fibers to mammalian muscle spindles, Multiple spindle innervation and activity durivg contraction, J. Physiol., 113 (1951) 283--297.
39 5 Kuffler, S.W., Hunt, C.C. and Quilliam, J.P., Function of medullated small-nerve fibers in mammalian ventral roots;efferent muscle spindle innervation, J. Neurophysiol., 14 (1951) 29--54. 6 Crowe, A. and Matthews, P.B.C., The effects of stimulation of static and dynamic fusimotor fibers on the response to stretching ~f the primary end~n~ of muscle spindles, J. Physiol., 174_(1964) 109--131. 7 Brown, M.C., Crowe, A. and Matthews, P.B.C., Observations on fusimotor fibers of tibialis posterior muscle of the cat, J. Physiol., 177 (1965) 140--159. 8 Lennerstrand, G. and Thoden, U., Position and velocity sensitivity of musc|e spindles in the cat. HI. Static fusimotor single-fiber activation of primary and secondary endings, Acta physiol, scnad., 74 (1968) 30--49. 9 Emonet-Ddnand, F., Laporte, Y. and Pages, B., Fibres fusimotorices statique et fusimotorices dynamique chez ]e lapin, Arch. ital. Biol., 104 (1966) 195--213. 10 Bessou, P. and Pages, B., A method of analysing the response of spindle primary endings to fusimotor stimulation, J. Physiol., 196 (1968) 37--45. 11 Bea~ou, P., Laporte,Y. and Pages, B., Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibers, J. Physiol., 196 (1968) 47--63. 12 Homma, S., Understanding the stretch reflex. In S. Hornma (Ed.), Progress in Brain Research Vol. 44, Elsevier, Amsterdam, 1976, pp. 107--109. 13 Bessou, P. and Pages, B., Cinematographic analysi~ of.contractile events produced in intrafusal muscle fibers by stimulation of static'a~d dynamic fusimotor axons, J. Physiol., 252 (1975) 397--427. 14 Boyd, I.A.j The response of fast and slow nuclear bag fibers and nuclear chain fibers in isolated cat muscle spindles t o fusimotor stimulation, and the effects of intrafusal contraction on the sensory ending, QuaY. J. exp. Physiol., 61 (1976) 203--254.
35
AVERAGE M U S C L E T E N S I O N T R I G G E R E D B Y STIMULATION OF GAMMA F U S I M O T O R FIBERS
SABURO HOMMA and YOSHIO NAKAJIMA
Department of Physiology, School of Medicine, Chiba University, Chiba, 280 (Japan) (Received June 15th, 1977) (Accepted June 23rd, 1977 )
SUMMARY
Average soleus muscle tension of the anesthetized cat, triggered by repetitive stimulation to a fine ventral root filament of LT, was isometrically recorded by use of blocking methods of the alpine decending impulse~ and it showed a twitch-like contraction with very rapid time coulse. Its mean time to peak and half decay time of relaxation in 12 observations was 21.7 and 26.8 msec, respectively. It was concluded that such a rapid concentration corresponds to a twitch of nuclear chain fibers. It was shown that repetitive stimulation of gamma fusimotor fibers during a pause of spindle discharges caused by an isometric extrafusal muscle contraction was sufficient to fill out the pause with impulse activity [ 1--4 ]. On the other hand, it has been noted that spindle afferent impulses follow the rhythm of the gamma fusimotor stimulation at a rate of up to ! 8 0 shocks/sec [5]. This phenomenon was called a 'driving', which has since been attributed to characteristics of static gamma fusimotor fibers in the cat [6--8] and also in the rabb|t [9--11]. Furthermore, the driving is assumed to be elicited by minute twitches of intrafusal muscle fibers. It has become clear that there exist definite relations between gamma fusimotor axons and contractile properties of intrafusal muscle fibers (see general discussion [12] ). Bessou and Pages [13] and Boyd [ 14] cinematographically recorded a displacement of intrafusal muscle fibers elicited by either static or dynamic gamma fusimotQr stimulation in cat tenuissimus. According to them, stimulation of static gamma axons innervating nuclear chain fibers elicited a rapid and large contraction, whereas that of static and/or dynamic gamma axons innervating nuclear bag fibers produced a slow and" small contraction. Stimulation of static axons innervating nuclear bag fibers,however, eliciteda more rapid and largercontraction than that of nuclear bag fibersinnervated by dynamic g a m m a axons. In our experiments, it was investigatedto obtain isometric twitch curves of h~tra~sal muscle fibers of cat soleus elicitedby electricstimulation of g a m m a
36
fusimotor fibers. The experiments were ~arned out on adult cats anesthetized with urethane and chloralose. All the hindlimb nerves on the experimental side were cut except the lateral gastrocnemius nerve. The soleus and its tendon were separated from surrounding tissues, care being taken to keep the blood supply and nerce to the muscle intact as far as possible. In order ~ record an isometric tension o f the soleus muscle, Achilles tendon was tightly connected with a steel plate on which a stre.in gauge was attached. Minimal detectable tension of the tension recording system was 1 rag. The soleus muscle was stretched 4 mm from its resting position throughout the experiments. After laminectom~, both ventral and dorsal roots from L5 to $1 were cut at their entry to the spinal cord. The ventral root of L7 was splitted into a fine filament, which was mounted on two pah-s o f silver electrodes. One pair of electrodes, which will be referred t o (A) electrodes, wa~ supplied with rectangular pulses with 0.5 msec duration at a rate of 0.8 Hz. It~ stimulus intensity was adjusted to 10 times the threshold of soleus muscle contraction. It is certain that this intensity is sufficient to stimulate gamma fusimotor axons. The soleus muscle tensions elicited by the above stimuli were recorded for 500 msec. The other pair of electrodes, situated distally to the (A) electrodes, was supplied with rectangular pulses with 0.5 msec duration and with random intervals of 2--5 reset. These electrodes will be called (B) electrodes. The soleus contractions elicited by the random rectangular pulses were tetanie and the tetanic contraction curves were smooth. Even if, however, there exist peaks in the tetanic contraction curves in relation to each random pulse, the appearance
I
100 msec
Fig. 1. A: twitch tension when the stimulus intensity was adjusted to 10 times the threshold of alpha motor fibers and the a~pha descending impulses were b~ocked by stimulation of random rectangular pulses under the other distal electrodes. The tension ~vas averaged 100 times. B: twitch tension elicited by stimulation of ventral root filament.
37 of the peaks must be random. The stimulus in~nsity of the random rectangular pulses was adjusted such that the alpha descending impulses elicited by the (A) electrodes, which elicit the twitch contractions, are blocked under the (B) electrodes. Since the intensity of the (B) electrodes was not strong enough to block gamma efferent impulses, the gamma descending impulses can pass under the (B) electrodes and elicit twitch contractions of the intrafusal muscle fibers in soleus muscle. Based on the methods stated above, the soleus muscle tensions were isometrically recorded and averaged for 500 msec, triggered by the 0.8 Hz pulses of the (A) electrodes. The averaging of the tension showed a twitch-like contraction with very rapid time course as shown in Fig. 1A. Fig. 1B shows a twitch tension of soleus extrafusal muscle contraction elicited by the (A) electrodes without block by the (B) electrodes. Time to peak and half decay time of relaxation was 71.0 and 128.6 msec, respectively. Thougb it is not clear how many alpha efferent fibers this ventral filament consists of, the maximum tension of Fig. 1B was 3.2 g° Fig. 1A shows a tension curve obtained from 100 times averaging by gamma efferent impulses. Time to peak and half decay time of relaxation was 17.1 and 31.4 msec, respectively. The time ~ourse is very rapid and the peak tension (61.3 mg) is very small as compared with those of the extrafusal contraction. It was assumed from these results that the contraction curve is that of intrafusal muscle fibers. In this particular case, a slow and small contraction is seen following the rapid contraction. The contraction curve apparently suggests that it is composed of two components of different time courses. However, such slow and small contraction could not be recorded in all cases. In measur;mg the time to peak and half decay time, the latter could not often be measured when accompanied with slow contraction. The results of the experiments are shown in Table I. It is obvious from Table I i~,hat the time course and the peak tension of the intrafusal muscle fibers are rap~d and small, respectively, as compared with those of extrafusal muscle fibers. S:ince it was occasion'~y difficult to block the twitch contraction completely under the (B) electrodes, Flaxedil ® was intravenously injected in a dose of about 3 mg/kg in order to complete the block by the (B) electrodes. Results of intrafusal muscle contraction under the Flaxedil ~ administration are 'also shown in Table I. It is clear that the Flaxedil ® does not affect the contraction curve of intrafusal muscle fibers. Minimum tension of the intrafusal muscle contractions lies between 7.7 and 81.~ rag. This variation of recorded tension may result from the difference in number of gamma efferent fibers stimulated in each case. Bessou and Pages [13] and Boyd [14] cinemato~aphical!y measured the time course o£ the displacement accompanied with the contractions of intrafusal muscle fibers in cat tenuissimus. They showed that the time course and the displacement of nuclear chain fibers are rapid and large, respectively. It was noticed that the time to peak and relaxation time were 40 and 80 rnsec, respectively.
38 TABLE I Peak tension (rag)
Time to peak (reset)
Half decay time (msec)
Duration at half tension (n~c)
Without Flaxedfl ® 1
7.7
26.5
--
--
2
8.7
22.1
3
9.2
17.6
26.5 26.5
38.2 38.2
4
17.4
23.5
--
--
5
22.0 25.6 45.7
26.5 27.6 25.6
--
--
41.6 30.6
54.4 52.9
28.8 58.8 61.3 65.0 81.3 36.0 ± 25.4
17.1 20.0 17.1 16.6 20.0 21.7 ± 4.2
11.4 28.6 31.4 15.7 28.6 26.8 ± 8.8
6
7 With Flaxedil ® 1 2 3a 4 5 Mean ± SD
20.0 42.9 42.9 ~ 24.3 37.1 39.9 ± 11.4
a See Fig. 1.
Our results of isometric contraction curves showed a time to peak and a half decay time of relaxation being about 21.7 and 26.8 msec, respectively, and are considerably short as compared with those of Bessou and Pages [13] and Boyd [ 14]. The driving, as mentioned above, which was assumed to be elicited by minute twitches of intmfusal muscle fibers will be achieved by such a short twitch contraction as shown in Fig. 1A. Since the displacement of nuclear chain fibers large in tenuissimus muscle according to Bessou a n d Pages [13] Boyd [14], it ~ be v ~ d to c0nclude that the large displacemen~ of nuclear c h ~ fibers was predominatly recorded a~ a large tension in this inves. • tigation. .... It was concluded that average tension triggered b y repetitive stimulation of the ventral root ~ a m e n t as shown i n Fig. 1A corresponds to a twitch contraction of nuclear c h ~ fibers elicited by static gamma fusimotor fibers. REFERENCES 1 Matthews, B.H.C., Nerve endings in mamraalian muscle, J. Physiol., 78 (1933) 1--53. 2 Leksell, L., Th~ action potential and excitatory effects of the small ventral root fibers to skeletal muscle, Acta physiol, stand,, I0, Supp|. 31 (1945~ 1--81. 3 Hun~, CICi ~ d r ~ e p t 0 r discharges during muscle contraction. J. ~ y s i o l . , 113 (1951) ~298--315, i / 4 o : efferent small-nerve fibers to mammalian muscle spindles, Multiple spindle innervation and activity durivg contraction, J. Physiol., 113 (1951) 283--297.
39 5 Kuffler, S.W., Hunt, C.C. and Quilliam, J.P., Function of medullated small-nerve fibers in mammalian ventral roots;efferent muscle spindle innervation, J. Neurophysiol., 14 (1951) 29--54. 6 Crowe, A. and Matthews, P.B.C., The effects of stimulation of static and dynamic fusimotor fibers on the response to stretching ~f the primary end~n~ of muscle spindles, J. Physiol., 174_(1964) 109--131. 7 Brown, M.C., Crowe, A. and Matthews, P.B.C., Observations on fusimotor fibers of tibialis posterior muscle of the cat, J. Physiol., 177 (1965) 140--159. 8 Lennerstrand, G. and Thoden, U., Position and velocity sensitivity of musc|e spindles in the cat. HI. Static fusimotor single-fiber activation of primary and secondary endings, Acta physiol, scnad., 74 (1968) 30--49. 9 Emonet-Ddnand, F., Laporte, Y. and Pages, B., Fibres fusimotorices statique et fusimotorices dynamique chez ]e lapin, Arch. ital. Biol., 104 (1966) 195--213. 10 Bessou, P. and Pages, B., A method of analysing the response of spindle primary endings to fusimotor stimulation, J. Physiol., 196 (1968) 37--45. 11 Bea~ou, P., Laporte,Y. and Pages, B., Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibers, J. Physiol., 196 (1968) 47--63. 12 Homma, S., Understanding the stretch reflex. In S. Hornma (Ed.), Progress in Brain Research Vol. 44, Elsevier, Amsterdam, 1976, pp. 107--109. 13 Bessou, P. and Pages, B., Cinematographic analysi~ of.contractile events produced in intrafusal muscle fibers by stimulation of static'a~d dynamic fusimotor axons, J. Physiol., 252 (1975) 397--427. 14 Boyd, I.A.j The response of fast and slow nuclear bag fibers and nuclear chain fibers in isolated cat muscle spindles t o fusimotor stimulation, and the effects of intrafusal contraction on the sensory ending, QuaY. J. exp. Physiol., 61 (1976) 203--254.