JOURNA
Vol.
N EUROPHYSIOLOGY No. 5, November
L OF
44,
1980.
Printed
in U.S.A.
Muscle Architecture and Force-Velocity Characteristics of Cat Soleus and Medial Gastrocnemius: Implications for Motor Control SIDNEY ROLAND
A. SPECTOR, R. ROY, AND
PHILLIP F. GARDINER, V. R. EDGERTON
RONALD
F. ZERNICKE,
Departments of Kinesiology, Bruin Research Institute, University of California, Los Angeles, California 90024; und Dkpartment d’Education Physique, Universitg de Montrkul, Montreul, Qukbec, Canada
SUMMARY
AND
CONCLUSIONS
2. Isometric and isotonic contractile parameters of the soleus (SOL) and medial gastrocnemius (MG) muscles of seven adult cats were studied. In addition, architectural characteristics of six contralateral pairs of these ankle extensors were determined. 2. The in situ peak isometric tetanic tension developed by the MG at the Achilles tendon is nearly 5 times (9,846 vs. 2,125 g) that of the SOL muscle. However, when differences between the MG and SOL in fiber length (2.01 vs. 3.66 cm), muscle mass (9.80 vs. 3.31 g), and angle of pinnation (21.4 vs. 6.4”) are considered, the specific tensions of these muscles are similar (approximately 2.3 kg cm-‘). 3. When the effects of muscle architecture are eliminated, the nearly threefold greater maximum isotonic shortening velocity (V,,,) of sarcomeres of the MG (38.3 pm/s) relative to the SOL (13.4 pm/s) is presumably due to intrinsic differences in the biochemical properties of these muscles. However, the V,,, developed by the MG at the Achilles tendon (258.6 mm/s) during a shortening contraction is only 1.5 times that of the SOL (176.3 mm/s) due to the influence of these muscles’ specific architectures. 4. Variations in geometrical characteristics of the SOL and MG are consonant with the relative amounts of participation of these muscles during posture, locomotion, and jumping. Posture requires the development of low forces for prolonged 0022-3077/80/0000-OOOO$O
1.25 Copyright
0 1980 The
periods for which the SOL seems best suited both architecturally and physiologically. The MG, relatively inactive during quiet standing, becomes responsible for a greater percentage of tension and shortening speed during plantar flexion (E3) as gait speeds increase, which is consistent with this muscle’s greater tension- and velocitygenerating capacity. 5. At high speeds of locomotion (3.0 m/s) and jumping, the shortening velocities developed at the end of E3 (approximately 20-40 ms before paw! off) exceed V,,, of the SOL. Consequently, the SOL, although electrically active, cannot contribute to the tensions required to generate the shortening velocities dictated by these movements. 6. These data demonstrate the influence of the differing geometries of the SOL and MG on the roles of these muscles in generating forces at varying velocities, as demanded by the dynamics of the movement. INTRODUCTION
Considerable detail of the isometric contractile properties of the whole muscle and single motor units of the medial gastrocnemius (MG) and soleus (SOL) muscles of the cat has been reported (5, 9- 11, 3 1, 36). These data, along with electromyographic and force information, have been combined into hypotheses that might explain how different types of motor units are used by the cat during posture, locomotion, and jumping (25, 34, 37). However, in view of the significance of muscle architec-
American
Physiological
Society
951
952
SPECTOR
ture when considering force and shortening velocity generated by the muscle (21), precise information on the geometries of the SOL and MG as well as their dynamic contractile parameters need to be clarified to understand more precisely the demands of the musculature and the characteristics of its neural control during normal movements. It would seem appropriate for the recruitment patterns of the innervating motor neurons to be matched with the muscle’s physiological properties of tension development, actual speed of shortening or lengthening, and time to peak tension. While a muscle’s myosin ATPase activity (6) and its sarcoplasmic reticular properties (7) are closely associated with the contractile rate of tension developed isometrically, the actual shortening or lengthening velocity generated by the muscle and transmitted through its tendon depends on the number of sarcomeres in series in the muscle’s fibers and the length and angle of pinnation of the fibers as well. Thus, it would appear advantageous for the motoneuronal recruitment patterns of the MG and SOL muscles during different modes of movement to be compatible with the architecture of these muscles. Consequently, in considering the neuronal recruitment patterns of the MG and SOL muscles, the architectural characteristics and the dynamic contractile properties of these muscles have been studied. The present results contrast the architecture and contractile properties of the MG and SOL muscles and reveal the influence that the muscle geometry must have on the details of the neuromotor recruitment patterns of these muscles. Preliminary results dealing with these questions are reported elsewhere (35). METHODS
The in situ physiological properties of the SOL and MG muscles were determined for seven adult cats weighing between 2.0 and 4.0 kg. Anesthesia was induced with sodium pentobarbital (35 mg/kg ip). To expose the hindlimb musculature, a single midsagittal incision was made posteriorly from the knee joint to the calcaneum. The skin was retracted and the MG
ET AL.
and SOL muscles were freed from adjacent musculature and connective tissue, with care taken to maintain a normal blood circulation. Surrounding muscles were denervated and the stumps of the distal nerve trunks of the MG and SOL were cleaned of fascia and isolated for stimulation. The SOL and MG tendons were separated from their calcaneal attachments and tied with nylon ligature (2-O suture). The animal was mounted in a frame so that the lower extremity was stabilized by clamps fixed with the knee positioned at 90”. A mineral oil pool, formed from the skin, was maintained at 37 t 1°C using radiant heat from a thermistorcontrolled heater and lamp.
Con tructile proper-ties A modification of the pneumatic isotonic lever system (20), which permitted the recording of both isometric and isotonic contractile events, was used for all contractile measurements. The muscle’s tendon was attached in situ to a light-weight magnesium lever arm on which were mounted force and displacement transducers. During isometric testing, the lever arm was mechanically fixed at the muscle length that yielded a maximal twitch tension response (L,,). All subsequent contractions were initiated from this muscle length. During isotonic testing, the mechanical restraint was removed. Under these conditions, the resistance against which the muscle contracted, in addition to the inertia of the lever system, was supplied by regulated air pressure in a bellows mounted in series with the lever arm. The bellows contained a vent that was continuous with a larger drum (5OL), which effectively eliminated any change in pressure within the bellows during muscle shortening. At resistances below which maximal isometric tension was developed, muscular shortening occurred and the lever arm was displaced, from which muscular shortening velocities were determined (see below). All contractile events were simultaneously recorded on a polygraph and displayed on an oscilloscope. Muscular contractions were elicited with a stimulator through bipolar silver electrodes placed around the distal stump of the severed nerve. Stimulation was performed at approximately twice the minimal voltage required to obtain a maximal twitch response at L,,. A 0. lms square-wave pulse was used to generate an isometric twitch response from which maximal twitch tension (PJ, time to peak tension (CT), and half-relaxation time (l/z RT) were determined. Peak isometric tetanic tension (P,,) was obtained for the SOL and MG at stimulation frequencies of 100 and 200 Hz, respectively. At these tetanic stimulation freauencies. 15-
DYNAMIC
PROPERTIES
OF SLOW
A
Force
lJL
AND
FAST
953
MUSCLE
B
1425Og
JJk
I=@
Dlsplacement
Two sets of force and displacement records from the isotonic tests are illustrated for the MG muscle FIG. 1. of the cat. In each of the records, the displacement curve, indicating muscular shortening from L, (base line of the displacement curve), is digitized to determine the maximum shortening velocity (peak slope of the curve). The force (P) developed is paired temporally with the shortening velocity ( V) as a discrete point on the forcevelocity curve (see Figs. 2, 3, 4). A represents a contraction that generated 8,320 g of tension at a shortening velocity of 60 mm/s, which occurred 1.8 mm below L,, (0.98 L,,). In contrast, the same muscle, at a tendon excusion of 5.2 mm (0.94 L,,) developed a velocity of shortening of 220 mm/s while generating only 2,200 g of tension. For this muscle, P,, equaled 10,300 g while V,,, equaled 350 mm/s.
25 afterloaded contractions at varying loads less than P, were elicited, from which the isotonic properties of each muscle were determined. The absolute tension (P) developed at the muscle length where the maximal rate (V) of tendon excursion (i.e., muscular displacement) occurred was determined for each MG and SOL contraction by digitizing (HP 9864 digitizer; HP 9830 calculator) the force and displacement records (Fig. 1). Each contraction was recorded at a paper speed of 100 mm/s, and discrete samples were digitized each millimeter. This permitted the collection of simultaneous force and displacement data points every 10 ms for the duration of the contraction, beginning at the initial deflection in force. After collection of the P-V pairs, the muscle’s maximal velocity of shortening (V,,3 was derived through a transformation of the variables in Hill’s (26) equation whereby x = P and y = (P, - P)IV. Plotting y as a function of x for all P-V values falling below approximately the 75th percentile of the force domain yielded a positive linear relation (18, 19). The Lax, then, equaled P, divided by the y intercept extrapolated by regression analysis. Finally, characteristic force-velocity curves were established for the muscles.
Architectural
characteristics
The contralateral hindlimbs of six cats used for contractile properties were infused with 10% formal saline with the knee and ankle positioned at 90”. After 24 h, the MG and SOL muscles were excised and placed in formal saline for an additional 24- to 48-h period. The muscles were macerated in 30% wt/vol HNO, for 2-7 days, and finallv stored in 50% glycerol ( 13).
Muscle length (excluding tendon) and the angles formed by the muscle fibers with respect to the line of pull of the muscle’s tendon were measured. Fiber bundles were teased from proximal, middle, and distal aspects of the muscle. From each of these regions, the lengths of between 10 and 20 fibers were determined with calipers. Data from a pilot investigation indicated a marked similarity in ipsi- and contralateral architectural profiles for both the MG and SOL of the cat. Thus, the architectural information obtained from the contralateral muscles permitted the assessment of morphological profiles for the ipsilateral SOL and MG muscles tested for contractile properties. Average fiber lengths for the ipsilateral muscles were derived by multiplying the lengths of these muscles, measured in situ at L,,, times the fiber length to muscle length ratio determined for their contralateral counterparts. “Physiological“ cross-sectional area (cm’) for each ipsilateral muscle was calculated by dividing muscle volume by fiber length (15) and correcting for the angle of pinnation of each muscle (24). Statistical analyses to determine significant differences between the MG and SOL muscles, for all measured architectural and contractile parameters, were performed using the Dunn-Bonferroni t statistic. RESULTS
Architecture The marked variations in architecture between the contralateral cat SOL and MG
SPECTOR
954 TABLE
1. Basic architecture Muscle
SOL MG
of soleus and medial gastrocnemius
Length, cm
Fiber
7.24 2 0.88 7.63 + 0.77
Values are means properties (n = 6).
3.51 + 0.61 1.89 + 0.34
Morphology Muscle
SOL MG
Wt,*
3.31 + 0.67 9.80 2 2.67
of muscles
Length, cm
7.60 8.13
+ 0.52 2 0.34
muscles Fiber Angle Pinnation,* deg
of
6.4 2 0.5 21.4 2 7.4
contralateral to those tested for contractile the MG and SOL for the given parameters.
t 596 g *cm-” COP) are not significantly different (P > 0.05). The effect of the muscle mass being arranged such that crosssectional area, and thus tension production, is maximized is illustrated by the observations that the MG weighs 3 times more than the SOL but produces 4.6 times the tetanic tension of the SOL. Speed-related contractile properties Selected isometric and isotonic indices, which describe the relative speeds of the SOL and MG muscles, are included in Table 4. A 2.3 times longer isometric CT for the SOL (79 * 14 ms) than the MG (34 t 4 ms) is seen. However, when the whole muscle’s shortening velocity is determined isotonically, the speed of shortening of the whole MG is only 1.5 times greater (176.3 t 50.5 vs. 258.6 t 86.0 mm/s) than that of the SOL. When expressing velocity relative to the average length of all fibers, there is a 2.7 times difference in shortening speed (4.8 t 1.2 vs. 12.8 t 4.1 fiber lengths per second) between the SOL and MG muscles, respectively. After further corrections of the variations in angles of pinnation of the two muscles, the intrinsic velocity of shortening (shortening speed of an average sarcomere) of the MG is almost 3 times faster than for the SOL muscle. Angle l
tested for contractile
Muscle g
Length/ Length,* %
48.2 A 5.7 24.7 t 3.9
t SD. Results are derived from muscles * Significant difference (P < 0.05) between
Tension-related contractile properties The absolute and specific twitch and tetanic tensions developed by the SOL and MG are compared in Table 3 using morphological data determined for the ipsilateral muscles (listed in Table 2). The greater mass of the MG can develop significantly more absolute twitch and tetanic tensions than the SOL (P < 0.05). However, when normalized with respect to the muscle’s physiological cross-sectional area, the specific tensions developed by the SOL (2,317 t 378 g cm-” cos+) and MG (2,301 2.
Fiber Muscle
Length,* cm
muscles are shown in Table 1. The lengths of these muscles are essentially equal (P > 0.05), but the fibers of the SOL extend about 48% of the muscle’s length (3.51 t 0.61 cm), in agreement with values reported for the SOL of the rat (13) and cat (I), while the fiber lengths of the MC (1 89 + 0.34 cm) are only 25% of the length of’thatmuscle. For both the SOL and MG, fiber lengths are consistent throughout individual muscles (except for the most proximal region of the MG, where fiber lengths are shorter). The angles of pinnation are uniform within muscles, but the angle is significantly greater (P < 0.05) for the MG (21.4 t 7.4”) than for the SOL (6.4 iI 0.5”).
TABLE
ET AL.
Fiber
properties Length,* cm
3.66 + 0.25 2.01 2 0.10
Physiological Muscle Cross Section,* cm’ 0.85 t 0.14 4.96 + 1.29
tested for contractile properties is 2.9 t 0.6 kg Values are means + SD. Mean body weight of animals (rz = 7). Physiological cross-sectional area = (muscle weight)/(fiber length * muscle density)/(angle of pinnation). Values for angle of pinnation are taken from Table 1. Muscle density value (1.0564 g/crnls) taken from Murphy * Significant difference (P < 0.05) between the MG and SOL for the given parameters. and Beardsley (25).
DYNAMIC
3. Maximum medial gastrocnemius
TABLE
538 + 2,055 f 2,125 9,846
137 597
f 336 t 1,607
OF SLOW
twitch and tetanic muscles g’cos-‘*
g” Twitch SOL MG Tetanic SOL MG
PROPERTIES
541 + 139 2,216 + 643 2,132 10,515
+ 330 2 167
AND
FAST
MUSCLE
955
tension of soleus and
g-g
MUSC-’
154 k 229 +
g
g-cm-’ 35 65
677 f 213 1,027 t 261
. c-n-2.
Pt
605 f 146 489 f 145 2,304 2,166
(-OS-1
608 + 146 525 + 165
+ 376 f 556
2,317 2,301
/P,,
0.25 + 0.05 0.21 2 0.04
+ 378 + 596
Tension values are means * SD. PJP,, refers to the isometric twitch-tetanic ratio. Cos denotes angle of pinnation, cm-:! refers to physiological cross-sectional area, and g. musc- l denotes muscle weight, the values of which are taken from Tables 1 and 2. * Significant difference (P < 0.05) between the MG and SOL for the given parameters.
correction of V,;,, for the fibers of the SOL the cat (1, 9, 11, 29, 31), as well as the affects this value by only I%, whereas a rat (13, 14), dog (2), and human (3, 24). 7% difference may be noted when correcting Studies by Burke et al. (9) and Bagust (5) for the 21” angle of pull for the MG at the have combined architectural data with the optimal length (L,). It should be noted, isometric contractile properties of the cat however, that this angle may possibly SOL muscle, while Burke et al. (10, 1l), change significantly from L, within a single Reinking et al. (32), and Stephens et al. (36) shortening or lengthening contraction (2 1). have combined these data for the MG of Preliminary evidence (38) shows that this is the cat to determine differences in the not a significant factor when considering physiology of these fast and slow muscles shortening velocities and forces, at least and their motor units under isometric with the SOL muscle. conditions. No investigation to date, howThe relationship between the force and ever, has incorporated the cat MG muscle’s velocity generated by the SOL and MG geometry with its dynamic contractile propunder various loading conditions is illuserties to parcel out quantitatively the intrated in Figs. 2 through 4. Figure 2 shows fluence of this muscle’s architecture on its the contrasting velocities for particular ability to generate shortening velocity and forces generated by the MG and SOL when tension. Also, the results of Murphy and velocity is expressed per average fiber Beardsley (29) concerning architectural inlength of the muscle. Greater dissimilarities fluences on the maximum shortening vein shortening velocities between the two muscles may be seen in Fig. 3, where the TABLE 4. Velocity and related influences of these muscles’ differing archiof soleus and medial tectures are minimized by expressing ve- parameters muscles locity per sarcomere and correcting for gastrocnemius the angles of pinnation. In contrast to Twitch Contraction Time,* Twitch Half-Relaxation Figs. 2 and 3, the influence of muscle ms Time,* ms architecture on the force-velocity relationships of the SOL and MG, expressed in absolute units of grams and millimeters per SOL 79-c 14 92 + 25 MG 342 4 28z 5 second, is depicted in Fig. 4 and illustrates the more closely aligned maximum shortMuscle, Fiber,* Sarcomere.* Sarcomere.* ening velocities developed at the Achilles mm.s-’ I, pm-s-’ pm es-’ .cos-’ tendon by these muscles. Isott~erric
.S-’
Mtr.ritt~i4tt~
176.3 2 50.5 258.6 + 86.0
isoiotlic
slrortet~itl~
4.8 e I.2 12.8 + 4.1
\*elocir>
13.3 + 3.5 36.0 + II.5
DISCUSSION
SOL MG
Much information has accumulated on the architectural profiles of various muscles of
Values are means + SD. * Significant difference tween the MG and SOL for the given Darameters.
13.4 + 3.5 38.8 2 12.4 (P < 0.05) be-
956
SPECTOR
15.0 .
3.0
-4
0,
1 0
20
1 40 FORCE
(%P(O))
FIG. 2. Force (percent maximum isometric tension) and velocity (fiber L,‘s/s) relationships of individual fibers of the SOL and MG muscles are plotted. By expressing velocity of shortening in terms of the average fiber length of the muscle, differences in fiber lengths between the MG and SOL, which influence shortening speed, are minimized. The CI values (mean + SD) derived from Hill’s equation (26) are 497.5 + 222.2 for the SOL and 4312.0 * 1704.0 for the MG muscle. The h constants are 39.9 + 17.1 and 112.8 t 39.7 for the SOL and MG, respectively.
locity of the cat SOL are at variance with other findings (8, 16, 28). The derived V,,, of the SOL (5.7 fiber lengths per second) in their study (29) may have been influenced by possible underestimation of the mean fiber lengths in their soleus muscles. Therefore, a detailed investigation of the architectural and dynamic contractile properties of the MG and SOL is presented. In addition, the results of this study are integrated into hypotheses that must be taken into account in understanding the motoneuronal recruitment patterns observed during different modes of movement. Signi$cance of muscle urchitecture on tension development Fiber angulation allows for a greater number of muscle fibers to attach along the length of the tendon, assuming a limited volume for a muscle (21). The difference in
ET AL.
angle of pinnation between the SOL and MC, coupled with variations in muscle mass (2.9~) and fiber length (1.8x), explains the more than fivefold difference in physiological cross-sectional area between the MG and SOL muscles (Table 2). In fact, the similarity between the mean cross-sectional areas of MG and SOL fibers (5,340 pm; see Ref. 22) in conjunction with these muscles’ architectural differences, implies that within the MG are situated more than 5 times the number of muscle fibers as found in the SOL muscle. This variation in fiber number between these two muscles is supported by the estimates of the number of fibers of the SOL (22,000-30,000) and MG (170,000) reported by Clark ( 12) and Burke et al. (1 l), respectively. The disparity in fiber number between the two muscles enables the MG to develop greater absolute twitch and tetanic tension than the SOL (Table 3). However, the isometric or dynamic tension generated at
---SOL -MMG
8 g
10.0
4, - 1,
FORCE
&&P(O))
FIG. 3. Force-velocity relationships of individual sarcomeres of the SOL and MG muscles are plotted. Velocities are expressed in micrometers per second per sarcomere and are corrected for the muscles’ angles of pinnation at L,. In this manner, architectural contrasts between these muscles are minimized so that the intrinsic speed of the contractile elements of these muscles may be estimated. Force values are expressed as percentages of isometric peak tetanic tension.
DYNAMIC
PROPERTIES
OF SLOW
AND
FAST
MUSCLE
957
250
0
2000
4ooo
---
SOL
-
MG
6000 FORCE (G)
8000
10000
FIG. 4. Force-velocity relationships of the whole SOL and MG muscles are plotted. Velocities are expressed in absolute units of millimeters per second and forces are expressed in grams. These curves illustrate the relation between force and velocity developed at the Achilles tendon by the MG and SOL muscles.
the muscle’s tendon is disproportionately reduced as the angle of pinnation increases. Therefore, there is an even greater disimilarity between the MG and SOL when the absolute intrinsic tension (g cos-*) of muscle fibers is considered (Table 3). The variation in tension, when expressed per muscle weight (g-g-*), is due to the nearly twofold difference in fiber lengths between the two muscles. When the angle of pinnation is considered, differences in these muscles’ tensions normalized to muscle weight are proportional to the contrasting fiber lengths of the muscles. Therefore, contrasts in tension expressed per muscle weight are not indicative of variations in intrinsic strength of these muscles. The specific tensions generated by the SOL and MG are quite similar (2.3 kg cm-“). Expressing tension in this manner minimizes the influences of angle of pinnation, fiber length, and muscle mass and, as supported in other investigations (see Ref. 15), demonstrates that the specific tension developed by whole muscle is the same for the fast and slow muscles of this study. l
SigniJicance of muscle architecture on velocity of shortening The nearly threefold contrast in intrinsic shortening velocities between the MG and SOL (Table 4) indicates the extent of the
difference in these muscles’ biochemical properties. The biochemical investigation of Barany (6) demonstrated that the shortening velocities of a large number of vertebrate and invertebrate muscles were “generally proportional” to their myosin ATPase activities. However, in that study (6), shortening velocities were expressed in units of muscle lengths per second and, therefore, were also influenced by variations that might exist in angles of pinnation and in fiber lengths relative to muscle from species to species. Removal of these architectural influences would provide a more precise assessment of the myosin ATPase-V,,, relationship of these muscles. The 2.9 times greater intrinsic V,,, of the MG than the SOL found in this study, coupled with the 2.6 times higher myosin ATPase activity of the MG than the SOL found by Barany (see Tables 1 and 2, Ref. 6) supports the general correlation, although it need not be a cause and effect relationship between a muscle’s intrinsic speed and its myosin ATPase activity. Interrelationship of architecture and contractile properties on movement dynamics The slow SOL muscle of the cat has long been considered a “postural” muscle (17). Smith et al. (34) have reported significant
958
SPECTOR
ET AL.
EMG activity in the SOL during movements locomotion and jumping. As a result, the of varying dynamics, including quiet standMG, though relatively inactive during posing, locomotion, and jumping. Force de- ture, becomes responsible for a larger terminations by Walmsley et al. (37) supproportion of the force generated at the ported these findings and indicated that ankle during all speeds of locomotion (37). The relative amounts of participation of relatively consistent and substantial amounts of motor-unit recruitment of the SOL occur the MG and SOL in the development of during each of these activities. force are also influenced by these muscles’ That the SOL muscle generates, on the abilities to generate adequate shortening velocities dictated by the dynamics of the average, more than twice the tension produced by the MG during standing (37) may movement (Fig. 4). For example, during be an advantage metabolically due to the the E3 phase of the cat stepping cycle (30), greater efficiency (work done per micromole from initiation of hindlimb plantar flexion of ATP) of the slow SOL in maintaining until paw lift-off, corresponding to shortenisometric tension compared with faster ing of the triceps surae musculature, the muscles (4). Because angulation of fibers SOL may generate an average shortening of the SOL is less than that of the MG, a velocity of 26 mm/s (23) at a walking speed of type greater percentage of force developed by of 0.67 m/s. Comprised exclusively muscle fibers of the SOL is transmitted S motor units (9), this muscle may potenthrough this muscle’s tendon. The differtially develop no less than 50% of its peak ence in fiber angulations between these isometric tetanic tension (Fig. 4), assuming muscles is also consistent with the producnearly or maximal motor-unit recruitment. as the speed of locomotion tion by the SOL of greater tensions for However, prolonged periods than the MG muscle. increases to 1.6 m/s, the SOL must shorten In fact, during an isometric twitch response, at an average velocity of approximately when neither fiber length nor angle of 101 mm/s during Ezl (23). At this rate, the pinnation affect the time to peak tension SOL may develop no more than 10% of its or relaxation time, the net impulse (i.e., peak tension, assuming maximal motor-unit the integral of tension x time) developed activation. In contrast, the MG, comprised of a heterogeneous population of type S, by the SOL throughout the contraction will exceed that of a muscle with a short CT FR, and FF motor units (lo), may potenand relaxation time, assuming the same tially develop nearly 40% of its maximal peak tension in both muscles. Thus, the isometric tension (Fig. 4), as it shortens at a more parallel fiber arrangement of the SOL, rate of only 83 mm/s (23) at the same “trotwhich permits a more direct transmission ting speed” (1.6 m/s). Because no more than of force at this muscle’s tendon, would seem 30% of the tetanic force of the MG is reto be the more economical design of these quired during locomotion (37), only about 50-55% of the motor units of the MG two muscles for tension development during standing. (including type S and FR) are activated. Locomotion and jumping, as opposed to That the shortening velocity of the MG is include the shortening only 82% of the SOL muscle’s shortening postural activities, rate at a locomotor speed of 1.6 m/s is due and lengthening of the MG and SOL tendons of these muscles (23). The rate to the crossing of both the knee and ankle of displacement of the Achilles tendon as joints by the MG muscle (23). This anaof the MG places well as the combined tension generated by tomical characteristic the MG, SOL, and their synergists in the this muscle at an advantage, compared to the SOL, under conditions where high production of torque about the ankle will velocities of shortening are required at the vary with the speed of locomotion. Walmsthe MG ley et al. (37) reported that because of the Achilles tendon, thus permitting to produce greater tension during phasic limited amount of additional motor-unit recruitment of the SOL from postural to movements than would be true if it was uniarticular. locomotor activities, this muscle’s EMG Walmsley et al. (Fig. 3 in Ref. 37) demonand peak force development may increase onlv slightlv during varving speeds of strated that, although nearly maximally
DYNAMIC
PROPERTIES
OF SLOW
activated, the SOL muscle was incapable of maintaining its tension in parallel with the MC during a fast run (3.0 m/s) and ceased developing tension at least 20 ms before its counterpart. Further evidence was presented (Fig. 4 in Ref. 37) supporting this pattern of behavior of the MG and SOL during plantar flexion prior to a vertical jump. During this activity, the SOL became ineffective in developing force approximately 40 ms before the MG became silent, although the SOL remained electrically active. In this case, the SOL must shorten at a rate of more than 180 mm/s (23). Therefore, whereas the peak tension output of the SOL is not significantly altered when low speeds of locomotion are involved, this muscle’s ability to sustain substantial levels of tension during high rates of plantar flexion, when maximally activated, is greatly affected by its force-velocity properties. On the other hand, during jumping, recruitment of type FF motor units of the MG, responsible for 70-75% of tetanic tension generated by this muscle (37), produces substantial increases in force required to generate the high shortening velocities.
AND
FAST
MUSCLE
959
Recently, Smith et al. (33) have demonstrated the selective recruitment of the fast-twitch lateral gastrocnemius of the cat without concommitant SOL activation during rapid hindlimb paw shaking. During this movement, the SOL muscle must shorten at velocities greater than 200 mm/s (see Ref. 33), in which case the SOL could produce a minute amount of force, within lo-20 ms of excitation, even if it was maximally activated. Therefore, during paw shaking this muscle must be considered ineffectual, at best, in contributing to the forces generating the eventual shortening velocities during ankle plantar flexion (1,150”/ s; see Ref. 33) required for the execution of this repetitive movement. ACKNOWLEDGMENTS
We gratefully acknowledge the assistance of Dr. Wendell N. Stainsby during the initial cat experiments using the pneumatic isotonic lever. We also thank Drs. R. J. Gregor and J. L. Smith for their critical reviews of the manuscript.
Received 5 November 27 May 1980.
1979; accepted
in final
form
REFERENCES 1. AL-AMOOD, W. S. AND POPE, R. A comparison of the structural features of muscle fibers from a fast- and slow-twitch muscle of the pelvic limb of the cat. J. Anut. 113: 49-60, 1972. 2. ALEXANDER, R. McN. The mechanics ofjumping by a dog (Cunis familiaris). J. Zool. 173: 549573, 1974. 3. ALEXANDER, R. McN. AND VERNON, A. The dimensions of knee and ankle muscles and the forces they exert. J. Hum. Mowmcnt Stud. 1: 115- 123, 1975. 4. AWAN, M. 2. AND GOLDSPINK, G. Energy utilization by mammalian fast and slow muscle in doing external work. Biochim. Biophys. Actct 216: 229-230, 1970. 5. BAGUST, J. Relationships between motor nerve conduction velocities and motor unit contraction characteristics in a slow twitch muscle of the cat. J. Physiol. London 238: 269-278, 1979. 6. BARANY, M. ATPase activity of myosin correlated with speed of muscle shortening. J. Gen. Physiol. 50: 197-218, 1967. 7. BRODY, I. A. Regulation of isometric contraction in skeletal muscle. Exp. Nuurol. 50: 673-683, 1976. 8. BULLER, A. J., KEAN, C. J. C., AND RANATUNGA, K. W. The force-velocity characteristics of cat fast- and slow-twitch skeletal muscle following cross-innervation. J. Physiol. London 2 13: 66-67, 1971. 9. BURKE, R. E., LEVINE, D. N., SALCMAN, M.,
TSAIRIS, P. Motor units in cat soleus muscle: physiological, histochemical and morphological characteristics. J. Physiol. London 238: 503513, 1974. 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: 723-748, 1973. BURKE, R. E. AND TSAIRIS, P. Anatomy and innervation ratios in motor units of cat gastrocnemius. J. Physiol. London 234: 749-765, 1973. CLARK, D. A. Muscle counts of motor units: a study of innervation ratios. Am. J. Physiol. 96: 296-304, 193 1. CLOSE, R. Dynamic properties of fast and slow skeletal muscles of the rat during development. J. Physiol. London 173: 74-95, 1964. CLOSE, R. The relation between intrinsic speed of shortening and duration of the active state of muscle. J. Physiol. London 186: 542-559, 1965. CLOSE, R. I. Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52: 129- 197, 1972. CLOSE, R. AND HOH, J. F. Y. Force-velocity properties of kitten muscles. J. Physiol. London 192: 815-822, 1967. DENNY-BROWN, D. E. The histological features of striped muscle in relation to its functional activity. Proc. R. Sot. London Ser. B 104: 371-411, 1929. DONALD, T. C., UNNOPPETCHARA, K., PETERSON, AND
10.
11.
12.
13.
14.
15. 16.
17.
18.
SPECTOR
19.
20.
22.
23.
24.
25.
26.
27.
28.
D., AND HEFNER, L. L. Effect of initial muscle length on V,;,, in isotonic contraction of cardiac muscle. Am. J. Physiol. 223: 262-267, 1972. EDMAN, K. A/P., MULIERI. L. A., AND SCUBONMULIERI, B. Non-hyperbolic force-velocity relationship in single muscle fibers. Actu Physiol. &and. 98: 143-156, 1976. FALES, J. T., LILIENTHAL, J. L., TALBOT, S. A., AND ZIERLER, K. L. A pneumatic isotonic lever system for dog skeletal muscle. J. Appl. Physiol. 13: 307-308, 1958. GANS, C. AND BOCK, W. J. The functional significance of muscle architecture: a theoretical analysis. Ergeh. Annt. Entwicklungsgesch. 38: 115- 142, 1965. GARDINER, P. F., BOTTERMAN, B. R., ELDRED, E., SIMPSON, D. R., AND EDGERTON, V. R. Metabolic and contractile changes in fast and slow muscles of the cat after glucocorticoid-induced atrophy. Exp. Neurol. 62: 271-255, 1978. GOSLOW, G. E., REINKING, R. M., AND STUART, D. S. The cat step cycle: hindlimb joint angles and muscle lengths during unrestrained locomotion. J. Morphol. 141: l-42, 1973. HAXTON, H. A. Absolute muscle force in the ankle flexors of man. J. Physiol. London 103: 267-273, 1944. HENNEMAN, E. AND OLSON, C. B. Relations between structure and function in the design of skeletal muscles. J. Neurophysiol. 28: 85-99, 1965. HILL, A. V. The heat of shortening and the dynamic constants of muscle. Proc. R. Sot. London Ser. B 126: 136-195, 1938. JOYCE, G. C., RACK, P. M. H., AND WESTBURY, D. R. The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J. Physiol. London 204: 461474, 1969. KEAN, C. J. C., LEWIS, D. M., AND MCGARRICK, J. D. Dynamic properties of denervated fast and
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30.
31.
32*
33*
34 l
35 .
36 .
37.
38.
slow twitch muscle of the cat. J. Physiol. London 237: 103- 113, 1974. MURPHY, R. A. AND BEARDSLEY, A. C. Mechanical properties of the cat soleus muscle in situ. Am. J. Physiol. 227: 1008-1013, 1974. PHILIPPSON, M. L’autonomic et la centralization dans le systeme nerveux des animaux. Trctv. Lath. Physiol. Inst. Solvay 7: l-208, 1905. RACK, P. M. H. AND WESTBURY, D. R. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J. Physiol. London 204: 443-460, 1969. REINKING, R. M., STEPHENS, J. A., AND STUART, D. G. The motor units of cat medial gastrocnemius: problem of their categorization on the basis of mechanical properties. Exp. Bruin Res. 23: 301-313, 1975. SMITH, J. L., BETTS, B., EDGERTON, V. R., AND ZERNICKE, R. F. Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. J. Neurophysiol. 43: 6 12-620, 1980. SMI-I-H, J. L., EDGERTON, V. R., BETTS, B., AND COLLATOS, T. C. EMG of slow and fast ankle extensors of cat during posture, locomotion, and jumping. J. Neurophysiol. 40: 503-5 13, 1977. SPECTOR, S., GARDINER, P. F., ROY, R. R., AND EDGERTON, V. R. Isotonic and geometric properties of cat medial gastrocnemius and soleus muscle. Med. Sci. Sports 11: 114, 1979. STEPHENS, J. A. AND STUART, D. G. The motor units of cat medial gastrocnemius: twitch potentiation and twitch-tetanus ratio. Pfluqers Arch. 356: 359-372, 1975. WALMSLEY, B., HODGSON, M. A., AND BURKE, R. E. Forces produced by medial gastrocnemius and soleus during locomotion in freely moving cats. J. Ncjurophysiol. 41: 1203- 1216, 1978. ZERNICKE, R. F., SPECTOR, S., EDGER-I-ON, V. R., ROY, R. R., AND GARDINER, P. F. Intracontractile dynamics of the cat soleus. Mvtl. Sci. Sports 1 I: 1 14, 1979.
