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Motor unit areas in a cat limb muscle
EXPERIMENTAL
30,
NEUROLOGY
Motor
Unit
475-483 (1971)
Areas
in a Cat
Limb
Muscle
SARAH KNOTT, D. M. LEWIS, AND J. C. LUCK l Department
of Physiology, Received
Unizlersity
of Bristol,
England
November 2, 1970; November 30, 1970
revision received
In an investigation of the areas of motor units in the flexor hallucis longus muscle of the cat, the electromyogram was recorded from the surface of the muscle with a bipolar concentric electrode. With the muscle set at the optimal length for each unit, observations were carried out on seven motor units which produced maximum isometric tensions of 0.28-22 g. The motor units were not uniformly scattered over the surface of the muscle but each had a distinct, localized territory. It is assumed that there was a similar localization in the deeper muscle layers. There was a clear correlation between the surface area from which an electromyogram could be recorded and between EMG amplitude and the maximum tension developed by different units. The distributions were not correlated with any mechanical parameter of the units. Introduction
During a study of the mechanical properties of the medial head of the flexor digitorum longus muscle of the cat (below called flexor hallucis longus or FHL),” the anatomical distribution of the muscle fibers belonging to single motor units was investigated. Previous workers have agreed that the individual muscle fibers of a unit are scattered and are intermingled with fibers of other units; Feindel, Hinshaw and Weddell in rabbit and monkey (6) and Edstrom and Kugelberg in rat (5) demonstrated this phenomenon by histological techniques, and similar results were obtained by KrnjeviC and Miledi (10) and Norris and Irwin (12) using a technique in which rat muscle was systematically penetrated with a microelectrode. There is, however, disagreement about the extent to which fibers of a single motor unit are distributed throughout a muscle. All observations in rat muscles show that the elements of a unit are found to be scattered 1 This work has been assisted by a grant from The Medical Research Council. 2The long “flexor” of the toes has two heads in the cat and the separate tendons fuse in the foot before dividing to serve all digits. The medial head has been called “flexor hallucis longus” by some workers (3). This nomenclature has been retained in this paper although other workers have used the anatomically more correct name “flexor digitorum longus” (13). 475
476
KNOTT,
LEWIS,
AND
LUCK
throughout the whole muscle. However, in man (Z), and in cat (4, 7), less direct evidence indicates that the units may be much more localized. In many of the cat experiments (7), units were isolated by eliciting minimal muscle contractions and this procedure might well have involved only a particular type of unit. Such a limitation might be very important for it has been shown that cat muscles contain a wide variety of units, whether they be classified by twitch contraction time or tetanic tension (13). The present paper presents evidence that confirms that motor units have a limited territory in the cat FHL muscle. Although only a small group of units was investigated, great care was taken to ensure that the units selected covered the full range of contraction times, tensions, and optimal lengths that had been found in a previous investigation ( 11). Methods Observations were made on seven motor units in three cats (2.2, 2.3, and 1.6 kg) anesthetised with pentobarbitone sodium (40 mg/kg), supplemented when necessary. The FHL muscle was exposed by a midline calf skin incision. To give maximal access to the muscle the medial head of gastrocnemius was excised and the remainder of triceps surae drawn laterally; finally, the fascia over the muscle was divided and removed extensively. All nerves in the back of the leg were divided except that to FHL ; the spinal roots L6 to Sl were exposed by laminectomy and cut centrally. Skin flaps were supported to allow exposed tissues to be covered with pools of liquid paraffin, the temperatures of these and of the whole animal being maintained at 37-38 C. The lower leg was fixed in a rigid position by clamping at either end of the tibia and fibula. The tendon of the FHL was cut distally and tied directly to a strain gauge (Ether U.F.l) which was mounted on a micrometer, thus allowing movement relative to the muscle origin. Isometric twitches and fused tetani (300-msec duration) of the whole muscle and some of its component motor units were measured over a range of muscle lengths to determine the optimal length ( 11). Single units were obtained by splitting the cut ventral roots (usually L7) with fine forceps, examining the subdivisions until the antidromic action potential evoked from the muscle nerve was seen to be single by all-or-none behavior when the stimulus was held constant at threshold intensity. To confirm this as single, care was taken to test for all-or-none behavior of the unit at threshold by observing muscle twitch, electromyogram (EMG) with belly-tendon leads and the antidromic response in the ventral root filament. The muscle was fixed at its optimal length for measurements of motor unit EMG, which was made with a bipolar concentric needle electrode (outside diameter 0.4 mm) which had been ground flat at the tip to give uniform contact with the muscle surface. The limb was orientated to expose as great an area of muscle as possible ; the medial two-thirds of the surface
MOTOR
UNIT
477
was exposed in a horizontal plane while the lateral third sloped downward. The electrode was held in a micromanipulator one axis of which was arranged parallel to the muscle surface, another at right angles to the long axis of the muscle, and the third normal to the surface. Initially, the muscle surface was mapped with a l-mm grid, at each point the electrode being lowered onto the surface until the EMG was maximal. Finally, the regions of activity were explored in greater detail transversely across the muscle. Results
Details of the mechanical properties of the units are shown in Table 1. Contraction times for the units ranged 17-40 msec and isometric twitch tensions 0.28-22 g. The whole muscles had contraction times of 20 msec and developed maximal twitches of 325, 390, and 225 g (A, B, C, respectively). The optimal muscle lengths for the unit isometric twitches were from 4.5 mm longer to 1 mm shorter than the optimal lengths for whole muscle contractions. Figure 1 shows the distribution of EMG in response to single stimuli obtained from the seven units. The black areas are those in which sharp, large-amplitude potentials were recorded. In the other shaded areas the potentials were of small amplitude and were rounded. Typical potentials are inserted in the diagram for unit Bl. Figure 1 also shows the arrangement of tendon (black) and muscle fibers (dotted) with a median raphe and terminal aponeurosis. The lengths of the muscle fibers in FHL vary between 2 and 4 cm. The maximum peak to peak amplitude of the EMG of the units and their estimated areas (as fractions of the total muscle surface area) are presented in Table 1 : These two variables are plotted against unit tension in Fig. 2A and B, respectively. In the double logarithmic plots used, linear regression lines could be fitted with a significance greater than 0.01, with slopes of 0.94 (voltage on tetanic tension, r = 0.91) and 0.44 (area on tension, r = 0.90). A similar correlation was found between log area and log voltage (regression coefficient = 1.92, r = 0.92). The relationship of the three variables could be expressed by the multiple regression equation (R = 0.93) : Log tension = 0.78 log area + 0.55 log voltage + 0.092. Similar correlations were found when twitch rather than tetanic tensions were used but the significance was somewhat less. Figure 3 shows in detail the EMG potentials recorded in a transverse exploration of three typical units. The potentials, including those in the troughs, were sharp and are included in the black-shaded areas of Fig. 1. Potentials in the stippled areas were too small to be distinguished from zero on the ordinate scale used in Fig. 3. In two casesthe EMG could be recorded for a sufficient distance along
478
KNOTT,
LEWIS,
AND
LUCK
,’ B 1 13
$1 ,‘\I’ ‘! (‘,(//S I \\ ‘, 1 ‘,, I,‘, \ ‘I ’ \‘$ \
1 cm
[
~
B
1 c3
1. Each figure shows the area frown which the EMG of one motor unit was recorded. Black area, sharp potentials ; stippled area, rounded potentials ; white area. no potentials: typical potentials with Bl. Diagram to right of Bl is the arrangement FIG.
of tendon
(black)
and muscle
fibers
(lines).
the muscle surface to enable a measurement of the muscle fiber conduction velocity to be made. The plots of total latency from these measurements are shown in Fig. 4. A third unit could be followed with less certainty, but limits of conduction velocity could be determined and are shown in Table 1. Discussion
In these experiments limited measurements of the EMG have been made by recording activity from the surface of the muscle. As shown in Fig. 3, maxima and minima could be recorded in a reproducible fashion and would indicate that the electrode recorded potentials at only a short range of about
MOTOR
UNIT
479
1-2 mm. Further evidence to support this assumption was the fact that when a normal, pointed needle electrode was pushed into the muscle through an area with large EMG potentials, the size of these potentials was reduced at a depth of 2-3 mm from the surface, that is about half the thickness of the muscle. These observations were not made systematically and were done only terminally in each experiment because of the danger of damage to vessels and nerves. This evidence indicates that activity was limited to bundles of fibers perhaps corresponding to the fasciculae of fibers (diameter 0.5-l mm) which can easily be seen on inspection of the muscle surface. The fact that the potentials could be traced along the course of these fasciculae with consistent changes of latency reinforce this conclusion. The slope of the lines in Fig. 4 were 3.6 and 2.7 m/set and these may be compared with previous conduction velocity measurements of 3.66 (SD -t- 0.35) m/set obtained from heterogeneous fasciculae in this muscle (3). From Table 1 it can be seen that the conduction velocity of unit Al falls outside this range. However, Buller, Lewis and Ridge (3) measured to the beginning of the compound muscle action potential, and their estimates of conduction velocity would refer only to the fastest-conducting fibers in the bundles. Unit Al had a long contraction time and the conduction velocity of its fibers falls within the range found for a slow-contracting muscle (soleus) of 2.95 -t 0.076 m/set (3). A correlation between tension and EMG has been reported previously by Appleberg and Emonet-D&and (1) using belly-tendon electrodes which would record potentials from large areas. The present methods have allowed activity to be recorded from a restricted area of the muscle and it has been found that the maximum EMG within the territory of a unit varies from one unit to another, increasing with the tension of the unit. One explanation of this finding might be that the proportion of fibers within the territory innervated by a nerve was not constant. The largest units would have the highest density of innervation. Thus, the nerves of large motor units would not only branch more widely in a muscle but also more frequently, therefore innervating a greater proportion of muscle fibers. If it could be assumed that the depth of the unit territories in the muscle was not greatly different from the measured width, then the region from which potentials were mapped would be proportional to the cross-sectional area of the unit territory. Errors due to this assumption would be likely to be less than the differences between unit areas. Thus, the results fit the expectation that the tension developed by the unit was function of both the cross-sectional area and the density of fibers within the area. Apart from the correlation with muscle tension, there was no indication that unit distribution determined other mechanical properties. It is true that the slower units (time of peak twitch tension more than 30 msec) had
Al A2 A3 Bl Cl c2 c3
Unit
98 90 90 86 89
69
NITW velocity Wsec)
f4.5 +4.0 -0.5 f4.0 f3.0 -1.0 +1.5
Opt. length cf. whole muscle (mm)
SUMMARY
0.28 1.3 22 1.6 0.44 16 2.0
(Ed
Twitch
OF DATA Tension
1.0 6.1 83 22 1.4 33 9.8
(9)
Tetanus
ON MECHANICAL
TABLE
3.6 4.6 3.8 14 3.1 2.1 4.9
Tetanus/ twitch
PROPERTIES
1
40 28 17 28 32 18 21
Contraction time (msec)
OF MOTOR
90 4.50 3,000 350 2.5 2,000 600
Maximum EMG bcv)
UNITS
area 0.1 0.2 0.35 0.35 0.05 0.5 0.2
Unit
3.6
4 to 6
2.7
Muscle fiber velocity (m/see)
x
z i?
5
ii < 3
“=r
2
MOTOR
.
481
UNIT
.
.
10'
'
1
3
lelanic
10
. .-
'
Trnsm
0.01+---
100
30
.
30 letanic
(9)
.
.
-
100
Tenston (a)
FIG. 2. Plots of tetanic tension against maximum EMG amplitude (A) and fractional surface area of the whole muscle (B) for the single motor units. Logarithmic scales used on all axes.
limited areas, but the slow units were always small ones and, therefore, this correlation would be expected to follow. Tetanus/twitch ratios might be expected to be large if the unit were situated far from the common tendon and acted through a relatively large series compliance. That this is not so is illustrated by unit Bl, which, although it had a high ratio of 14, had some of its fibers inserted directly into the final tendon. Similarly, unit A 1 was situated far from the tendon but had a normal tetanus/twitch ratio. The optimal length for a unit twitch tension might also be expected to vary with unit size and distance from the tendon. However, unit A2 had . A3 ? a c; g
o-3- /\ 7, 0.3-
_
2
_ /
B1
‘i.., ,W.l\*,*j*’ C Ok ., = s 0.3 - .-.? i : ,,/ \l\.Pr\ ,”
O/i
\
c2
SE
0’
. .
/
, 0.2
hnsverse
\./
o-4
O-6 distance
(cm)
3. EMG amplitude (peak-to-peak values) recorded from three motor units (A3, Bl, CT!) at 0.5-mm steps transversely across the muscle. FIG.
482
KNOTT,
Longitudinal
LEWIS,
AND
Distance
LTJCK
(cm)
4. For two units (CZ, Al), plots of latency between the stimulus artifact and EMG as the recording electrode was moved along the muscle. Sharp potentials, rounded potentials, 0. Solid line fitted to points; dashed line, mirror image of solid line. Horizontal solid line indicates the latency due to conduction in the
FIG.
the 0; the nerve.
an optimal length 4 mm longer than that of the whole muscle but its fibers covered a large area and a large proportion of them were sited near the tendon. Activation of motor units in the cat has been observed by previous workers as localized contractions (4, 7, 9). The present observations add further support to these findings and show that each motor unit in the FHL muscle of the cat has a distinct territory and is not uniformly scattered throughout the muscle mass as in the rat (5, 10, 12). It is interesting to compare this with the specific sensitivity of Golgi tendon organs to just a few of the motor units within a muscle (8). It is concluded that in cat FHL muscle motor units have a limited territory. The larger units tend to have larger territories probably with a higher density of fibers within their territory. No other correlation could be found between mechanical properties of the units and the territory occupied by the units. References 1. APPELBERG, lumbrical 2. RUCHTHAL, territory
B., and F. EMONET-DI?NAND. 1967. Motor units of the first superficial muscle of the cat. J. Neurophysiol. 30 : 154-160. F., C. GULD, and P. ROSENFALCK. 1957. Multielectrode study of the of a motor unit. .4cta Pltssiol. Scud. 39 : 83-104.
MOTOR
UNIT
483
BULLER, A. J., D. M. LEWIS, and R. M. A. P. RIDGE. 1965 Some electrical characteristics of fast twitch and slow twitch skeletal muscle fibres in the cat. J. Physiol. London 160 : 29-30 P. 4. DENSLOW, J. S., and 0. R. GUTENSOHN. 1950. Distribution of muscle fibres in a single motor unit. Fed. Proc. 9 : 31. 5. EDSTROM, L. and E. KUGELBERG. 1963. Histochemical composition, distribution of fibres and fatigability of single motor units. Anterior tibia1 muscle of the rat. 3.
J. Nezcrol. Neurosurg. Psychiat. FEIXDEL, W., J. R. HINSHAW,
31 : 424433.
and G. WEDDELL. 1952. The pattern of motor innervation in mammalian striated muscle. J. Anat. 86 : 35-48. 7. GORDON, G., and A. H. S. HOLBOURN. 1949. The mechanical activity of single motor units in reflex contractions of skeletal muscle. J. Physiol. London 110:
6.
26-35.
8. HOUK, J., and E. HENNEMAN. 1967. Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J. Neurophysiol. 30: 466-481. 9. HUST, C. C., and S. W. KUFFLER. 1951. Stretch receptor discharges during muscle contraction. J. Physiol. Lorldon 113 : 298-315. 10. KRNJEVI~‘, K., and R. MILEDI. 1958. Motor units in the rat diaphragm. J. Physiol. London
140:
427-439.
11. LEWIS, D. M., and J. C. LUCK. 1963. Effect of initial length on the tension developed by motor units in flexor hallucis longus muscle of the cat. J. Physiol. Londo~~ 197: 42-43 P. 12. NORRIS, F. H., JR., and R. L. IRWIN. 1961. Motor unit area in a rat muscle. Anter. J. Physiol.
200 : 944946.
13. OLSON, C. B., and C. P. SWETT, JR. 1966. -4 functional and histochemical characterization of motor units in a heterogenous muscle (flexor digitorum longus) of the cat. J. Cowp. Nczcrol. 126 : 475-498.
30,
NEUROLOGY
Motor
Unit
475-483 (1971)
Areas
in a Cat
Limb
Muscle
SARAH KNOTT, D. M. LEWIS, AND J. C. LUCK l Department
of Physiology, Received
Unizlersity
of Bristol,
England
November 2, 1970; November 30, 1970
revision received
In an investigation of the areas of motor units in the flexor hallucis longus muscle of the cat, the electromyogram was recorded from the surface of the muscle with a bipolar concentric electrode. With the muscle set at the optimal length for each unit, observations were carried out on seven motor units which produced maximum isometric tensions of 0.28-22 g. The motor units were not uniformly scattered over the surface of the muscle but each had a distinct, localized territory. It is assumed that there was a similar localization in the deeper muscle layers. There was a clear correlation between the surface area from which an electromyogram could be recorded and between EMG amplitude and the maximum tension developed by different units. The distributions were not correlated with any mechanical parameter of the units. Introduction
During a study of the mechanical properties of the medial head of the flexor digitorum longus muscle of the cat (below called flexor hallucis longus or FHL),” the anatomical distribution of the muscle fibers belonging to single motor units was investigated. Previous workers have agreed that the individual muscle fibers of a unit are scattered and are intermingled with fibers of other units; Feindel, Hinshaw and Weddell in rabbit and monkey (6) and Edstrom and Kugelberg in rat (5) demonstrated this phenomenon by histological techniques, and similar results were obtained by KrnjeviC and Miledi (10) and Norris and Irwin (12) using a technique in which rat muscle was systematically penetrated with a microelectrode. There is, however, disagreement about the extent to which fibers of a single motor unit are distributed throughout a muscle. All observations in rat muscles show that the elements of a unit are found to be scattered 1 This work has been assisted by a grant from The Medical Research Council. 2The long “flexor” of the toes has two heads in the cat and the separate tendons fuse in the foot before dividing to serve all digits. The medial head has been called “flexor hallucis longus” by some workers (3). This nomenclature has been retained in this paper although other workers have used the anatomically more correct name “flexor digitorum longus” (13). 475
476
KNOTT,
LEWIS,
AND
LUCK
throughout the whole muscle. However, in man (Z), and in cat (4, 7), less direct evidence indicates that the units may be much more localized. In many of the cat experiments (7), units were isolated by eliciting minimal muscle contractions and this procedure might well have involved only a particular type of unit. Such a limitation might be very important for it has been shown that cat muscles contain a wide variety of units, whether they be classified by twitch contraction time or tetanic tension (13). The present paper presents evidence that confirms that motor units have a limited territory in the cat FHL muscle. Although only a small group of units was investigated, great care was taken to ensure that the units selected covered the full range of contraction times, tensions, and optimal lengths that had been found in a previous investigation ( 11). Methods Observations were made on seven motor units in three cats (2.2, 2.3, and 1.6 kg) anesthetised with pentobarbitone sodium (40 mg/kg), supplemented when necessary. The FHL muscle was exposed by a midline calf skin incision. To give maximal access to the muscle the medial head of gastrocnemius was excised and the remainder of triceps surae drawn laterally; finally, the fascia over the muscle was divided and removed extensively. All nerves in the back of the leg were divided except that to FHL ; the spinal roots L6 to Sl were exposed by laminectomy and cut centrally. Skin flaps were supported to allow exposed tissues to be covered with pools of liquid paraffin, the temperatures of these and of the whole animal being maintained at 37-38 C. The lower leg was fixed in a rigid position by clamping at either end of the tibia and fibula. The tendon of the FHL was cut distally and tied directly to a strain gauge (Ether U.F.l) which was mounted on a micrometer, thus allowing movement relative to the muscle origin. Isometric twitches and fused tetani (300-msec duration) of the whole muscle and some of its component motor units were measured over a range of muscle lengths to determine the optimal length ( 11). Single units were obtained by splitting the cut ventral roots (usually L7) with fine forceps, examining the subdivisions until the antidromic action potential evoked from the muscle nerve was seen to be single by all-or-none behavior when the stimulus was held constant at threshold intensity. To confirm this as single, care was taken to test for all-or-none behavior of the unit at threshold by observing muscle twitch, electromyogram (EMG) with belly-tendon leads and the antidromic response in the ventral root filament. The muscle was fixed at its optimal length for measurements of motor unit EMG, which was made with a bipolar concentric needle electrode (outside diameter 0.4 mm) which had been ground flat at the tip to give uniform contact with the muscle surface. The limb was orientated to expose as great an area of muscle as possible ; the medial two-thirds of the surface
MOTOR
UNIT
477
was exposed in a horizontal plane while the lateral third sloped downward. The electrode was held in a micromanipulator one axis of which was arranged parallel to the muscle surface, another at right angles to the long axis of the muscle, and the third normal to the surface. Initially, the muscle surface was mapped with a l-mm grid, at each point the electrode being lowered onto the surface until the EMG was maximal. Finally, the regions of activity were explored in greater detail transversely across the muscle. Results
Details of the mechanical properties of the units are shown in Table 1. Contraction times for the units ranged 17-40 msec and isometric twitch tensions 0.28-22 g. The whole muscles had contraction times of 20 msec and developed maximal twitches of 325, 390, and 225 g (A, B, C, respectively). The optimal muscle lengths for the unit isometric twitches were from 4.5 mm longer to 1 mm shorter than the optimal lengths for whole muscle contractions. Figure 1 shows the distribution of EMG in response to single stimuli obtained from the seven units. The black areas are those in which sharp, large-amplitude potentials were recorded. In the other shaded areas the potentials were of small amplitude and were rounded. Typical potentials are inserted in the diagram for unit Bl. Figure 1 also shows the arrangement of tendon (black) and muscle fibers (dotted) with a median raphe and terminal aponeurosis. The lengths of the muscle fibers in FHL vary between 2 and 4 cm. The maximum peak to peak amplitude of the EMG of the units and their estimated areas (as fractions of the total muscle surface area) are presented in Table 1 : These two variables are plotted against unit tension in Fig. 2A and B, respectively. In the double logarithmic plots used, linear regression lines could be fitted with a significance greater than 0.01, with slopes of 0.94 (voltage on tetanic tension, r = 0.91) and 0.44 (area on tension, r = 0.90). A similar correlation was found between log area and log voltage (regression coefficient = 1.92, r = 0.92). The relationship of the three variables could be expressed by the multiple regression equation (R = 0.93) : Log tension = 0.78 log area + 0.55 log voltage + 0.092. Similar correlations were found when twitch rather than tetanic tensions were used but the significance was somewhat less. Figure 3 shows in detail the EMG potentials recorded in a transverse exploration of three typical units. The potentials, including those in the troughs, were sharp and are included in the black-shaded areas of Fig. 1. Potentials in the stippled areas were too small to be distinguished from zero on the ordinate scale used in Fig. 3. In two casesthe EMG could be recorded for a sufficient distance along
478
KNOTT,
LEWIS,
AND
LUCK
,’ B 1 13
$1 ,‘\I’ ‘! (‘,(//S I \\ ‘, 1 ‘,, I,‘, \ ‘I ’ \‘$ \
1 cm
[
~
B
1 c3
1. Each figure shows the area frown which the EMG of one motor unit was recorded. Black area, sharp potentials ; stippled area, rounded potentials ; white area. no potentials: typical potentials with Bl. Diagram to right of Bl is the arrangement FIG.
of tendon
(black)
and muscle
fibers
(lines).
the muscle surface to enable a measurement of the muscle fiber conduction velocity to be made. The plots of total latency from these measurements are shown in Fig. 4. A third unit could be followed with less certainty, but limits of conduction velocity could be determined and are shown in Table 1. Discussion
In these experiments limited measurements of the EMG have been made by recording activity from the surface of the muscle. As shown in Fig. 3, maxima and minima could be recorded in a reproducible fashion and would indicate that the electrode recorded potentials at only a short range of about
MOTOR
UNIT
479
1-2 mm. Further evidence to support this assumption was the fact that when a normal, pointed needle electrode was pushed into the muscle through an area with large EMG potentials, the size of these potentials was reduced at a depth of 2-3 mm from the surface, that is about half the thickness of the muscle. These observations were not made systematically and were done only terminally in each experiment because of the danger of damage to vessels and nerves. This evidence indicates that activity was limited to bundles of fibers perhaps corresponding to the fasciculae of fibers (diameter 0.5-l mm) which can easily be seen on inspection of the muscle surface. The fact that the potentials could be traced along the course of these fasciculae with consistent changes of latency reinforce this conclusion. The slope of the lines in Fig. 4 were 3.6 and 2.7 m/set and these may be compared with previous conduction velocity measurements of 3.66 (SD -t- 0.35) m/set obtained from heterogeneous fasciculae in this muscle (3). From Table 1 it can be seen that the conduction velocity of unit Al falls outside this range. However, Buller, Lewis and Ridge (3) measured to the beginning of the compound muscle action potential, and their estimates of conduction velocity would refer only to the fastest-conducting fibers in the bundles. Unit Al had a long contraction time and the conduction velocity of its fibers falls within the range found for a slow-contracting muscle (soleus) of 2.95 -t 0.076 m/set (3). A correlation between tension and EMG has been reported previously by Appleberg and Emonet-D&and (1) using belly-tendon electrodes which would record potentials from large areas. The present methods have allowed activity to be recorded from a restricted area of the muscle and it has been found that the maximum EMG within the territory of a unit varies from one unit to another, increasing with the tension of the unit. One explanation of this finding might be that the proportion of fibers within the territory innervated by a nerve was not constant. The largest units would have the highest density of innervation. Thus, the nerves of large motor units would not only branch more widely in a muscle but also more frequently, therefore innervating a greater proportion of muscle fibers. If it could be assumed that the depth of the unit territories in the muscle was not greatly different from the measured width, then the region from which potentials were mapped would be proportional to the cross-sectional area of the unit territory. Errors due to this assumption would be likely to be less than the differences between unit areas. Thus, the results fit the expectation that the tension developed by the unit was function of both the cross-sectional area and the density of fibers within the area. Apart from the correlation with muscle tension, there was no indication that unit distribution determined other mechanical properties. It is true that the slower units (time of peak twitch tension more than 30 msec) had
Al A2 A3 Bl Cl c2 c3
Unit
98 90 90 86 89
69
NITW velocity Wsec)
f4.5 +4.0 -0.5 f4.0 f3.0 -1.0 +1.5
Opt. length cf. whole muscle (mm)
SUMMARY
0.28 1.3 22 1.6 0.44 16 2.0
(Ed
Twitch
OF DATA Tension
1.0 6.1 83 22 1.4 33 9.8
(9)
Tetanus
ON MECHANICAL
TABLE
3.6 4.6 3.8 14 3.1 2.1 4.9
Tetanus/ twitch
PROPERTIES
1
40 28 17 28 32 18 21
Contraction time (msec)
OF MOTOR
90 4.50 3,000 350 2.5 2,000 600
Maximum EMG bcv)
UNITS
area 0.1 0.2 0.35 0.35 0.05 0.5 0.2
Unit
3.6
4 to 6
2.7
Muscle fiber velocity (m/see)
x
z i?
5
ii < 3
“=r
2
MOTOR
.
481
UNIT
.
.
10'
'
1
3
lelanic
10
. .-
'
Trnsm
0.01+---
100
30
.
30 letanic
(9)
.
.
-
100
Tenston (a)
FIG. 2. Plots of tetanic tension against maximum EMG amplitude (A) and fractional surface area of the whole muscle (B) for the single motor units. Logarithmic scales used on all axes.
limited areas, but the slow units were always small ones and, therefore, this correlation would be expected to follow. Tetanus/twitch ratios might be expected to be large if the unit were situated far from the common tendon and acted through a relatively large series compliance. That this is not so is illustrated by unit Bl, which, although it had a high ratio of 14, had some of its fibers inserted directly into the final tendon. Similarly, unit A 1 was situated far from the tendon but had a normal tetanus/twitch ratio. The optimal length for a unit twitch tension might also be expected to vary with unit size and distance from the tendon. However, unit A2 had . A3 ? a c; g
o-3- /\ 7, 0.3-
_
2
_ /
B1
‘i.., ,W.l\*,*j*’ C Ok ., = s 0.3 - .-.? i : ,,/ \l\.Pr\ ,”
O/i
\
c2
SE
0’
. .
/
, 0.2
hnsverse
\./
o-4
O-6 distance
(cm)
3. EMG amplitude (peak-to-peak values) recorded from three motor units (A3, Bl, CT!) at 0.5-mm steps transversely across the muscle. FIG.
482
KNOTT,
Longitudinal
LEWIS,
AND
Distance
LTJCK
(cm)
4. For two units (CZ, Al), plots of latency between the stimulus artifact and EMG as the recording electrode was moved along the muscle. Sharp potentials, rounded potentials, 0. Solid line fitted to points; dashed line, mirror image of solid line. Horizontal solid line indicates the latency due to conduction in the
FIG.
the 0; the nerve.
an optimal length 4 mm longer than that of the whole muscle but its fibers covered a large area and a large proportion of them were sited near the tendon. Activation of motor units in the cat has been observed by previous workers as localized contractions (4, 7, 9). The present observations add further support to these findings and show that each motor unit in the FHL muscle of the cat has a distinct territory and is not uniformly scattered throughout the muscle mass as in the rat (5, 10, 12). It is interesting to compare this with the specific sensitivity of Golgi tendon organs to just a few of the motor units within a muscle (8). It is concluded that in cat FHL muscle motor units have a limited territory. The larger units tend to have larger territories probably with a higher density of fibers within their territory. No other correlation could be found between mechanical properties of the units and the territory occupied by the units. References 1. APPELBERG, lumbrical 2. RUCHTHAL, territory
B., and F. EMONET-DI?NAND. 1967. Motor units of the first superficial muscle of the cat. J. Neurophysiol. 30 : 154-160. F., C. GULD, and P. ROSENFALCK. 1957. Multielectrode study of the of a motor unit. .4cta Pltssiol. Scud. 39 : 83-104.
MOTOR
UNIT
483
BULLER, A. J., D. M. LEWIS, and R. M. A. P. RIDGE. 1965 Some electrical characteristics of fast twitch and slow twitch skeletal muscle fibres in the cat. J. Physiol. London 160 : 29-30 P. 4. DENSLOW, J. S., and 0. R. GUTENSOHN. 1950. Distribution of muscle fibres in a single motor unit. Fed. Proc. 9 : 31. 5. EDSTROM, L. and E. KUGELBERG. 1963. Histochemical composition, distribution of fibres and fatigability of single motor units. Anterior tibia1 muscle of the rat. 3.
J. Nezcrol. Neurosurg. Psychiat. FEIXDEL, W., J. R. HINSHAW,
31 : 424433.
and G. WEDDELL. 1952. The pattern of motor innervation in mammalian striated muscle. J. Anat. 86 : 35-48. 7. GORDON, G., and A. H. S. HOLBOURN. 1949. The mechanical activity of single motor units in reflex contractions of skeletal muscle. J. Physiol. London 110:
6.
26-35.
8. HOUK, J., and E. HENNEMAN. 1967. Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J. Neurophysiol. 30: 466-481. 9. HUST, C. C., and S. W. KUFFLER. 1951. Stretch receptor discharges during muscle contraction. J. Physiol. Lorldon 113 : 298-315. 10. KRNJEVI~‘, K., and R. MILEDI. 1958. Motor units in the rat diaphragm. J. Physiol. London
140:
427-439.
11. LEWIS, D. M., and J. C. LUCK. 1963. Effect of initial length on the tension developed by motor units in flexor hallucis longus muscle of the cat. J. Physiol. Londo~~ 197: 42-43 P. 12. NORRIS, F. H., JR., and R. L. IRWIN. 1961. Motor unit area in a rat muscle. Anter. J. Physiol.
200 : 944946.
13. OLSON, C. B., and C. P. SWETT, JR. 1966. -4 functional and histochemical characterization of motor units in a heterogenous muscle (flexor digitorum longus) of the cat. J. Cowp. Nczcrol. 126 : 475-498.