ACTA NEUROBIOL. EXP. 1990, 50: 589
- 600
THE COURSE OF MOTOR UNIT TWITCH IN DEPENDENCE
ON MUSCLE STRETCHING FORCE.
STUDIES ON MEDIAL GASTROCNEMIUS MUSCLE OF THE RAT
Kazimierz GROTTEL, J a n CELICHOWSKI and Nat,alia ANISSIMOVA
Department of Neurobiology, Academy of Physical Education
10 Droga Debinska St., 61-555 Poznali, Poland and Laboratory of Motor Physiology,
Pavlov Institute of Physiology, Leningrad, USSR
Key words: motor unit, muscle stretching, twitch force, contraction time, half-relaxation time
Abstract. Studies were performed on 46 units of medial gastrocnemius muscles in 23 rats. In the examined population, three types of motor units were distinguished: fast fatigable (FF), fast resistant (FR) and
slow (S) units. The studied muscle was stretched with force gradually
increasing from 0.5 to 10 g. Most sf F F units and some of FR units
reached the highest twitch force when the muscle was stretched with
4 to 7.5 g. The remaining fast units and alniost all slow units reached
the highest twitch force a t 10 g stretching of the muscle. In some fast
units, twitch force even decreased slightly at stretching of the muscle
with 10 g force. On the other hand, contraction tiine and half-relaxation
time were getting prolonged in the whole process of stretching the muscle. Most pronounced changes in contraction tiine and half-relaxation
time look place in S type units while the least pronounced ones - in
F F type units. The prolongation of half-relaxation times in motor units
of all three types was more pronounced than the prolongation of contraction times.
INTRODUCTION
Recording the twitch force of the muscle or motor unit in isometric
conditions requires that the muscle be stretched before the test. The
stretching of the muscle may be expressed by an increase in muscle
length or by the force used for the stretching. Depending upon the dcgree of stretching, the course of the contraction is different. In studies
on motor units performed up to the present day the twitch force has
been measured in variable conditions. Usually during the experiments
muscles have been maintained in a length optimal for the contraction of
the whole muscle (8, 17 - 19, 21, 22, 29).
In these studies, the optimal length has been defined as a length of
the muscle a t which the highest muscle twitch force is registered. In
other studies the optimal length of the muscle has been determined for
contraction of its individual motor units (2, 10, 23, 24). In some experiments muscle stretching with constant, defined force has been applied,
permitting to record the highest twitch force of most of its motor units
(3, 4, 5, 20, 31). In the majority of units, the maximal twitch force has
been reached a t the length of the muscle distinct from the length which
has been optimal for the contraction of the whole muscle (27, 28, 30,
33). In conditions optimal for the contraction of the whole muscle, usually a somewhat lowered twitch force has been registered for its motor
units (30). Till now, the interrelationship has been examined mainly
between muscle length and twitch force and, ocassionally, contraction
time as well. The relation has been examined inducing a single c m traction o r maximal tetanus, either in studies on the whole muscles
(6, 7, 9, 25, 32) or in studies on motor units (1, 27, 28, 30, 33). In these
papers the moltor unit twitch force was related mainly to muscle length
(10, 25 - 28, 33). It should be mentioned that in these studies the motor
units have been divided into fast and slow ones only. In the presented
study we have examined the interrelationships between twitch force,
contraction time and half-relaxation time in the motor units of medial
gastrocnemius muscle in the rat on one hand and the force used for
stretching the muscle on the other. So far the relations have not been
studied in detail and, as far as rat motor units are considered, they have
not been examined at all. In accordance to results obtained in earlier
publications (Celichowski, in preparation; 13), we have applied a division
of the motor units into three types (FF, FR and S). The measurements
have been conducted at stretching the muscle using force up to 10 g,
since at such stretching of the studied muscle most of its motor units
have reached the maximal twitch force, as shown by preliminary observations.
MATERIAL AND METHODS
The experiments were performed on 23 adult rats of Wistar strain,
weighing on the average, 311 40 g, in pentobarbital anesthesia. Details
+
related to the administering of anesthesia, surgery, regulatilon of the
body temperature, immobilization of extremities and isolation of individual motor units were described in earlier publications (Celichowski, in
preparation; 15). Muscle fullction was taken as reflecting the function
of a single motlor unit if both twitch force and EMG record were consistent with "all or none" reaction type. Methods used to register EMG
and the electrodes used were also described earlier (14, 15).
Twitch force of the motor units was measured using inductive force
transducer in isometric conditions. After finding out that an individual
unit was stimulated (at stretching the muscle with 10 g force), sequential
twitch records were obtained, stretching the muscle with increasing force, according to the sequence 0.5 - 1 -- 2 - 3 - 4 - 5 - 7.5 - 10 g.
Subsequently, the sag test was performed (stimulation of the motor unit
with a sequence of stimuli at 40 Hz frequency and 500 ms duration),
which permitted to divide the units into fast and slow ones. Finally, the
unit was subjected to fatigue test (stimulation of the unit with 330 ms
lasting bursts of stimuli a t 40 Hz frequency and repeated every one
second, for a total of 4 min). Results of the fatigue test allowed to calculate the fatigue index and to divide fast motor units into resistant to
fatigue, (FR) and nonresistant ones (FF) (4, 13, Celichowski, in preparation). The way in which twitch force, contraction time, half-relaxation
time were measured and fatigue index calculated were described in detail in other papers (12, 13).
In the presented study, we have calculated the means of investigated
properties and their standard deviations. The significance of differences
between the means was calculated using t-Student test.
RESULTS
For three animals the relation was investigated between the muscle
length increment and the force with which the muscle was stretched.
This relationship is exemplified in Fig. 1.
Out of 46 motor units studied, 23 were classified as F F type, 12 units
as FR type and 11 as S type. The mean values of twitch force, contraction time, half-relaxation time and of fatigue index are given in
Table I.
Examples of records of motor unit twitches for all three types of
units, obtained during the increasing stretching of the muscle, are presented in Fig. 2. Increasing force of stretching the muscle was paralleled
by increasing motor unit twitch force and increasing duration of its
course (both contraction time and half-relaxation time).
nm
-.:
I
O A 2 3 4 5
75
?,J
0
MS
Fig. 1. Relationships between muscle
stretching force (MS) a n d its length
(L) increment. The measurements wer e collected durlng stretching t h e muscle w i t h increasing force. Muscle
stretching force equal to 1 g w a s used
to stretch t h e muscle w h e n its original length (0) w a s measured.
Twitch force
The relationships between the twitch force of motor units (expressed
in percentage) and muscle stretching is presented in Fig. 3A and B separately for different types of units. Increasing stretching of the muscle
induced an increase in twitch force to its highest value (i.e. 100°/o) in
most of investigated motor units.
Mean values and thcir standard deviations of principal properties of studied
motor units of three types. Testing was performed when the muscle was
stretched with 10 g force. TwF,twitch force; CT,contraction time; HRT,half-relaxation time; FI, fatigue index. The same abbreviations were also used in
Fig. 5.
-
Motor u r ~ i ttype
TwF
(9)
CT
(111s)
13 RT
FI
(ms)
In the extreme case among investigated F F units (marginal curve
delimiting F F type unit area at the left hand side, Fig. 3 4 , already at
stretching the muscle with 4 g force, the twitch force of the unit reached
its maximum. In other units - this maximum was reached a t stretching
the muscle with 5 or 7.5 g force. Further stretching of the muscle (with
force from 7.5 up to 10 g) in experiments on the part of F F type units
IFF
FR
S
Fig. 2. Twitch courses in FF, FR and S type motor units recorded during stretching
the muscle with increasing force. Sequential records for each unit are placed in
separate columns. Numbers to the left relate to records in all three columns and
indicate the force used to stretch t h e muscle a t the time of recording.
Fig. 3. A, course of changes of twitch force (TwF) i n motor units of various type,
recorded during stretching the muscle with increased force (MS). The highest recorded twitch force was taken as 100°/o TwF. Each point represents the mean value and its standard deviation. F F type units a r e marked in filled circles, FR units
in open circles, S in crosses. B, areas between marginal (on the axis marked by
dotted line) curves of dependence of twitch force upon muscle stretching force,
separately for each of the distinguished types of motor unlts.
induced a decrease in their twitch force by 2 to 8% (n = lo), or the
units maintained the maximal twitch force (n = 3). In the remaining
10 FF type motor units the maximal twitch force was recorded at stretching the muscle with 10 g force.
In FR group, the marginal motor unit reached its maximal twitch
forte also a t 4 g stretching of the muscle, in 4 other cases, - at 5 or
7.5 g stretching. At,still higher stretching of the muscle, i.e. a t stretching with 10 g force, the twitch force of one of the units decreased by
4"o. In the remaining 7 units of FR type the highest twitch force was
reached when the muscle was stretched with 10 g force.
The twitch force of slow motor units reached usually its maximal
value at the strongest stretching, applied i.e. 10 g (Fig. 3A and B). .In
only two of the units the highest twitch,force values were reached
already at s t r e t c h i ~ gthe muscle with 7.5 g force. O n the other hand,
still stronger stretching of the muscle (with 10 g force) did not induce
a decrease in twitch force in these two units.
Differences in twitch force values between motor units of various
types at'stretching the muscle with force ranging from 0.5 t;o 10 g (Fig.
3A) proved insignificant.
In 5 muscles i n which more than 1 motor unit was examined (2 - 6),
the course of curves of dependence between twitch force and muscle
stretching was analysed for motor units of various types. Usually also
in a single muscle twitch the force of fast motor units reached higher
relative values (in percentage) in sequential points of increasing stretching than did slow units (Fig. 4). However, no relations were detected
between'the values of twitch force (expressed in grams) of units and the
100
%
Cli
3 50
b
Fig. 4. Course of changes in twich
force in 6 individual motor units of
the same muscle. The curves were
drawn similarly to those in Fig. 3.
Numbers in the Figure denote motor
unit twitch force in grams (tested a t
10 g muscle stretching force). Symbols
indicating types of motor units are
identical to those of Fig. 3A.
0
0
0 1 2 3 4 5
MS
75
10
9
100 -
75-.-1
ti
%
C
Fig. 5. Relative changes in contraction
times (CT) of m o t ~ runits in each of
three types (mean f SD) in function
of tnuscle stretching. Symbols identical to those of Fig. 3 A. The longest
contraction time was accepted as 100%
(always a t 10 g stretching force).
I
50
0 1 2 3 4 5
MS
7.5
10
9
course of twitch force changes during the stretching of the muscle
(Fig. 4).
~ontractio?ttime
The relationship between the cointraction time of motor units of various type and the stretching of the muscle is presented in Fi,g. 5. In the
course of the entire process of stretching the muscle contraction time was
becoming prolonged in all types of units. Contraction time in FF units
showed, on the average, the least pronounced alterations when the muscle was stretched with force increasing from 0.5 to 10 g, while contraction time of slow units showed greatest alterations. In all units, an increase in contraction time was greater when the muscle stretching force
increased from 0.5 to 5 g than in the remaining portion of the experiment. Significant differences (p 0.05) were detected when contraction
times expressed in percentages were compared between FF, and S type
units at stretching the muscle with the force up to 5 g.
<
Relation between half-relaxation time and muscle stretching is prcsented in Fig. 6. Increasing stretching of the muscle induced also a prolongation of half-relaxation times in units of any type. The greatest increase in the half-relaxation time upon stretching the muscle within the
studied range took place in S type motor ulnits, the smallest - in FF
type units. Similarly to contraction time, half-relaxation time was getting prolonged, particularly in the earlier part of the experiment, i.e.
upon stretching the muscle with force increasing up to 5 g, in all three
0 1 2 3 4 5
hf!3
10
7.5
Q
Fig. 6. Relative changes in half-relaxation times (HRT, mean i SD) in
motor units of three types. For symbol explanation see Fig. 3-4. The longest half-relaxation time was taken as
1000/o (always at 10 g stretching force).
<
types of units. Significant differences (p 0.05) were noted between
relative values of half-relaxation times between F F and S type units,
upon stretching the muscle with force increasing up to 2 g.
Comparisons were made also between relative values (in percentages) of contraction times on one hand and half-relaxation times on the
other, separately for each of all three studied types of motor units. Values of the two compared properties in F F units differed significantly
from each other upon stretching the muscle with force
to 5 g, in
FR units - with force up to 3 g, in S units
with force up t~ 7.5 g.
-
DISCUSSION
Multiple studies on the twitch of entire muscle and motor units indicate that the twitch force registered during stretching the muscle
(during increase in its length) increases originally and, after reaching
a certain value, gradually decreases (6, 9, 26 - 28, 33). The studies were
usually performed by progressive stretching the muscle each time by the
same unit of length (9, 27, 33). In this study we have examined changes
in the twitch force of motor units, defining the force with which, the
muscle was stretched. This way of testing provides more dependable
control of a degree of muscle stretching examining motor units. This is
particularly important when the muscle is stretched with gradually increasing force. At the beginning, stretching the muscle with a unit of
force has resulted in a relatively marked increase in its length, while
further stretching has lead to a still lower increase in muscle length per
increase in the unit of force (Fig. I), (7, 33). The discussed results relate
to records made during stretching the muscle with force increasing from
0.5 to 10 g. The upper limit of testing, equal to 10 g, reflects the force
of stretching the muscle at which the twitch force of most motor units
reaches its highest value. In such muscle load, the twitch force of some
fast units begins even to decrease. However, the decrease is slight and
amounts up to 8O/d. At stretching the muscle with 10 g force, a t the
average, a higher twitch force is reached in motor units of any type,
as compared to stretching the muscle with 7.5 g force. The difference
is also inconsiderable, amounting from 3O/o to 7010 for FF and S type
units, respectively. Thus, stretching the medial gastrocnemius muscle
of the rat with 10 g force may be thought optimal for testing the units
of the muscle.
In the presented experiments we have noted that among the distinguished three types of motor units, the twitch force of FF type motor
units is the earliest to reach maximal values and the twitch force of
S units is the last one to reach maximal values during a gradual increase
in stretching force up to 10 g. Similar results hqve been obtained by
other authors (1, 33). The results indicate that FF type motor units are
adjusted to work in conditions of lower extending of the muscle (at its
shorter length) than FR and S type units. This fact may have a functional importance. During normal movement, the slow motor units are first
recruited into contraction (16). The muscle is then extended, (i.e. it has
its greatest length). In the extended muscle slow motor units work
in optimal length colnditions. In the course of contractioln the slow motor
units start the shortening of the muscle and then, with some delay (upon
certain shortening of the muscle), fast motor units become involved.
However, the latter do not reach the maximal values of their force until the belly of the muscle becomes shortened. Stephens et al. (33) have
related the differeince between fast and slow motor units in their optimal muscle length to differences in absolute values of twitch force between fast and slow units. In the experiments presented in this study
much higher twitch forces have been obtained for FF type units than for
the remaining ones. On the other hand, twitch forces expressed in percentages for various extent of muscle stretching have not, differed from
each other so significantly. The absence of statistical significance of the
differences may reflect a low number of examined units and, in part,
individual differences between motor units of even the same type within a given muscle. The latter factor may reflect, e.g. the position of
muscle fibers of the studied units within the cross-section of the muscle,
length of the fibres or other properties.
In all motor units, contraction time and half-relaxation time have
become prolonged upon stretching the muscle. This has taken place
even if the twitch force of some units was becoming constant or has
been decreasing at the end of stretching. These observations confirm the
results of twitch studies on muscles and motor units by other authors
(6, 26, 32 - 34). In FF units, contraction time and half-relaxation time
became only slightly, while in S units, markedly prolonged. Changes in
half-relaxation times in units of all three types have been more evident
than corresponding changes in contraction times. The latter observation
has also corroborated the results of other authors on colntsactions of
muscles and motor units (6, 26, 33).
As evident from respective literature, the muscles of extremities remain in the length close to the optimal one for contraction during their
normal activity (1, 7, 9, 26). Changes in muscle stretching during changes
in angles of joints a t which the muscle acts lead probably not only to
changes in the twitch force of motor units but probably induce changes
in contraction and relaxation times as well. The latter changes, in turn,
may affect the course of unfused tetani (34). Motor units usually work
in such unfused tetani (11) and the degree to which the tetanus is fused
(and, in effect tetanic tension) depends, apart from the frequency of
motoaeurone firing, upon cointraction and relaxation times. Thus, the
twitch force of the muscle during its normal activity should be considered to represent not only the net result of a number of functioning
motor units and frequencies of their contractions. Undoubtedly, the original stretching of the muscle, dependent upon angular position of the
extremity, may also affect the original twitch force.
This investigation was partly supported by Project R P 111-52.V.3.4.
REFERENCES
1. BAGUST, J., KNOTT, S., LEWIS, D. M., LUCK, J. C. and WESTERMAN,
R. A. 1973. Isometric contractions of motor units in a fast twitch muscle
of the cat. J. Physiol. 231: 87 - 104.
2. BAGUST, J., LEWIS, D. M. and LUCK, J. C. 1974. Post-tetanic effects i n motor units of fast and slow twitch muscle of the cat. J. Physiol. 237: 115 121.
3. BURKE, R. E. 1967. Motor units types of cat triceps surae muscle. J. Physiol.
193: 141 - 160.
4 BURKE, R. E., LEVINE, D. M., TSAIRIS, P. and ZAJAC, I?. E. 1973. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J. Physiol. 234: 723 - 748.
5. CLAMAN, H.P. and ROBINSON, A. J. 1985. A comparison of elecromyographic
and mechanical fatlgue properties In motor units of the cat hindlimb.
Brain Res. 327: 203 - 219.
6. CLOSE, R. I. 1964. Dynamic properties of fast and slow skeletal muscles of
the rat during development. J . Physiol. 173: 74 - 95.
7. CLOSE, R. I. 1972. Dynamic properties of mammalian skeletal muscles. Physiol.
Rev. 52: 129 - 197.
8. GARDINER, P. F. and OLHA, A. E. 1987. Contractile and electromyographic
9.
10.
11.
12.
13.
14.
characteristics of rat plantaris motor unit types d u r h g fatigue in situ.
J. Physiol. 385: 13 - 34.
GOSLOW, G. E., CAMERON, W. E. and STUART, D. G. 1977. Ankle flexor
muscles in the cat: length-active tension and muscle unit properties as
related to locomotion. J. Morphol. 153: 23 - 28.
GOSLOW, G. E., CAMERON, W. E. and STUART, D. G. 1977. The fast twitch
motor units of cat ankle flexors. 1. Tripartite classification on basis of fatiguability. Brain Res. 134: 35 - 46.
GRIMBY, L., HANNERZ, J. and HEDMAN, B. 19r19. Colltraction time and voluntary discharge properties of individual short toe extensor motor units
in man. J. Physiol. 289: 191 - 201.
GROTTEL, K. and CELICHOWSKI, J. 1988. Contraction time and contraction
delay of motor units in rat's medial gastrocnemius muscle. Biol. Sport
5 (4): 285 - 295.
GROTTEL, K. and CELICHOWSKI, J. 1990. Division of motor units in medial
gastrocnemius muscle of the rat in the light of variability of their principal properties. Acta Neurobiol. Exp. 50: 571.
GROTTEL, K., CELICHOWSKI, J. and KOWALSKI, K. 1986. Spatial analysis
of motor unit potentials of the rat medial gastrocnemius. Acta Physiol. Pol.
37: 219
q
- 227.
15. GROTTEL, K., CELICHOWSKI, J. and KOWALSKI, K. 1988. Twitch force and
16.
17.
action potentials of single motor units in medial gastrocnemius muscle of
the rat. Acta Neurobiol. Exp. 48: 7 1 - 81.
HENNEMAN, E., SOMJEN, G. and CARPENTER, D. 0. 1965. Functional significance of cell size in sp~inalmotoneurones. J. Neurophysiol. 28: 560 - 580.
JAMI, L., MURTHY, K. S. K., PETIT, J . and ZYTNICKI, D. 1982. Distribution
of physiological types of motor units in the cat peroneus tertius muscle.
Exp. Brain Res. 48: 177 184.
KERNELL, D., DUCATI, A. and SJOHOLM, H. 1975. Properties of motor units
i n the first deep lumbrical muscle of the cat's foot. Brain Res. 98: 37 55.
KERNELL, D., EERBEEK, 0. and VERHEY, B. A. 1983. Motor unit categorization on 'basis of contractile properties: a n experimental analysis of the
compositon of the cat's m. peroneus longus. Exp. Brain Res. 50: 211 -219.
KERNELL, D. and MONSTER, A. W. 1982. Motoneurone properties and motor
fatigue. An intracellular study of gastrocnemius motoneurones of the cat.
Exp. Brain Res. 46: 197 - 204.
KERNELL, D. and SJOHOLM, H. 1975. Recruitment and firing rate modulation of motor unit tension in a small muscle of the cat's foot. Brain Res.
-
18.
19.
20.
21.
-
98: 57 - 72.
22. KERNELL, D., VERHEY, B. A. and EERBEEK, 0 . 1985. Neuronal and muscle
unit properties a t different rostro-caudal levels of cat's motoneurone pool.
Brain Res. 335: 71 - 79.
23. KUGELBERG, E. 1973. Histochemical composition, contraction speed and fatiguability of rat soleus motor units. J . Neurol. Sci. 20: 177 - 198.
24. KUGELBERG, E. and LINDEGREN, B. 1979. Transmission and contraction fa-
tigue of rat motor units in relation to succinate dehydrogenase activity of
motor unit fibres. J. Physiol. 288: 285 300.
-
5
- Acta Neurobiol.
Exp. 6190
LEV-TOV, A., PRATT, C. A. a n d BURKE, R. E. 1988. T h e motor-unit population of t h e cat tenuissimus muscle. J. Neurophysiol. 59: 1128 1142.
LEWIS, D. M. 1981. The physiology of motor units i n mammalian skeletal
muscle. In Handbook of behavioral neurobiology. Plenum Press, New York,
p. 1 67.
LEWIS, D. M. and LUCK, J. C. 1968. Effect of in,itial length on the tension
develo~pedb y motor units i n flexor hallucis longus muscle of t h e cat. J. Physi01. 197: 42 - 43P.
LEWIS, D. M., LUCK, J. C. and KNOTT, S. A. 1972. A comparison of i s m e tric contractions of the whole muscle with those of motor units in a fasttwitch muscle of t h e cat. Exp. Neurol. 37: 68 - 85.
LEWIS, D. M.,PARRY, D. J. and ROWLERSON, A. 1982. Isometric contractions
of motor units a n d imrnunochemistry of mouse soleus muscle. J. Physiol.
325: 393 401.
McDONAGH, J. C., BINDER, M. D., REINKING, R. M. a n d STUART, D. G.
1980. Tetrapartite classification of motor units of cat tibialis posterior.
J. Neurophysiol. 44: 696 712.
OLSON, C. B. a n d SWETT, C. P. 1971. Effect of prior activity on properties of
different types of motor units. J. Neurophysiol. 34: 1 - 16.
RACK, P. M. H. and WESTBURY, D. R. 1969. The effects of length a n d stimulus rate o n tension i n the isometric cat soleus muscle. J. Physiol. 204: 443 460.
STEPHENS, J. A., REINKING, R. M. and STUART, D. G. 1975. The motor
units of cat medial gastrocnemius: electrical and mechanical properties a s
a function of muscle length. J. Morphol. 146: 495 - 512.
WALLINGA de JONGE, W., BOOM, H. B. K., BOON, K. L., GRIEP, P. A. M.
a n d LAMMEREE, G. C. 1980. Force development of fast and slow skeletal
muscle a t different muscle lengths. Am. J. Physiol. 239: C98 - C104.
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Accepted 30 May 1990