Morphological organization and contractile properties of the wrist flexor muscles in the cat.код для вставкиСкачать
THE ANATOMICAL RECORD 199:321-339 (1981) Mo rpho Iog ical 0rgan ization and Contractile Properties of the Wrist Flexor Muscles in the Cat W.J. GONYEA, S.A. MARUSHIA, AND J.A. DIXON Department of Cell Biology, The University of Texas Health Science Center at Dallas, Dallas, Texas 75235 ABSTRACT A comparison of the anatomy, fiber type profiles, and contractile properties of the wrist flexor muscles was undertaken in the cat. Isometric contractile characteristics were measured for each muscle. Three muscle fiber types, FG, FOG, and SO, were differentiated by staining cross sections of each muscle for ATPase, NADH diaphorase, SDH, and a-GPD activities. The wrist flexor muscles ranged from less than 1%to 4wo SO fiber content; with two of the five heads of the flexor digitorium profundus (FDP) having 1%or less SO fibers (FDP,-l.07%, FDPa4.81%) and the humeral head of the flexor carpi ulnaris muscle (FCU,) having the greatest content of SO fibers. The mean contraction time (CT) plus one-half relaxation time for an isometric twitch was correlated with the percentage of SO fibers and ranged from 40.5 to 111.8 ms. Except for the FCU (37 ms), the CT was less than 25 ms for the wrist flexor muscles. The uniarticular wrist flexor muscles, the flexor carpi radialis (FCR),and the FCU had the highest percentage of SO fibers and were more fatigue-resistant that the multiarticular muscles. Considerable differences exist in muscle structure, fiber type proportions, and contractile properties between the FCR and FCU, which may be related to functional differences between the two sides of the wrist that may exist during the placement of the foot during locomotion. The structural organization, fiber type distribution, and the contractile properties of skeletal muscle should reflect the complexity of tasks that the neuromuscular apparatus of the animal is called upon to perform. To study these structural-functional interactions, a considerable volume of data on the structural organization and physiological properties of whole muscles and single motor units of the hindlimb muscles have been collected (reviewed in Burke and Edgerton, '75; Close, '72). While these studies have yielded a great deal of information, resulting in a very rapid expansion of our understanding of the function of the neuromuscular apparatus, a similar, thorough analysis of the distal forelimb musculature has not been performed. In the cat, increased motor control for the forelimb musculature may be necessary because this animal uses its forelimbs as prehensile organs to catch and manipulate food (Gonyea and Ashworth, '75). In a recent study of the elbow flexor and extensor muscles of the cat, it was observed that deeply situated uniarticular extensor muscles 0003-276x/81/1993-0321$05.50 01981 ALAN R. LISS,INC. consisted predominantly of slow twitch muscle fiber types. It has also been demonstrated that these muscles are used for postural support. The larger extensor synergists and the elbow flexor muscles, which are not used for postural support, are composed primarily of fast twitch muscle fibers (Collatos et at., '77, Smith et al., '77). Collatos and colleagues also demonstrated that the frequency range over which fast twitch muscles increase tension is much greater than that for slow twitch muscles (Collatos et al., '77). Hence it could be assumed that for muscles involved in a number of motor tasks, excluding postural adjustments, fast twitch motor units may be preferentially selected. Although a recent detailed electromyographic (EMG) analysis of the forelimb muscles of the cat has been published (English, '781, no information was included in this study concerning the activity of the wrist flexor muscles in maintaining standing posReceived June 6, 1980; accepted July 24, 1980. 322 W.J. GONYEA, S.A. IMARUSHIA, AND J.A. DMON ture. This information would be useful in elucidating the functional significance of differences in fiber type distribution of these muscles as it was for the elbow musculature (Collatos et al., '77, Smith et al., '77). However, our preliminary studies have not demonstrated any EMG activity of the wrist flexor muscles during quiet standing (unpublished observations) and this has been confirmed by the observations of Dr. English (personal communication). The purpose of this study was to establish the fiber type composition and contractile properties of the wrist flexor muscles in the cat. In this regard, some of these muscles are also the long flexor muscles of the digits (Gonyea and Ashworth, '75). Even though the forelimb has the responsibility of supporting 3@% of the body weight (Manter, '38) and has a major role during propulsion (Smith et al., '77, English, '78), its use as a prehensile organ suggests the possibility of a more complex motor control for the wrist flexor muscles than that observed for hindlimb muscles. Hence these studies were undertaken to assess structural-functional correlations in the wrist flexor muscles that may be useful in assessing different adaptive strategies in motor control. A preliminary report on the contractile properties of two wrist flexor muscles and a detailed anatomical analysis of the flexor carpi radialis (FCR) muscle have appeared elsewhere (Gonyea and BondePetersen, '77; Gonyea and Ericson, '77). METHODS MYOkY There are five muscles that cross the flexor surface of the wrist: the flexor carpi radialis (FCR), flexor carpi ulnaris (FCU), palmaris longus (PLM), flexor digitorum superficialis (FDS), and the flexor digitorum profundus (FDP).The FDS is a small, rudimentarymuscle in the cat (Crouch, '69);this muscle was therefore not included in this investigation. All other wrist flexor muscles were studied in 24 adult cats of both sexes. The muscles were stripped from their osseous attachments, cleaned of all extraneous tissue including all tendon not directly receiving muscle fibers, and weighed. A brief description of the attachments of each muscle and a general description of the gross muscle fiber architectural arrangement is also given. Histochemistry Muscles from six cats were prepared for histochemical examination. Sections repre- senting the total cross-sectional area from the greatest girth of each muscle belly were taken and mounted in tragacanth gum on a cork disc and rapidly frozen by immersion in Freon cooled with liquid nitrogen. Transverse serial sections were cut a t 8 pm on a cryostat (-20°C) and mounted on coverslips by thawing, and stained for adenosine triphosphatase (ATPase) activity (preincubations at pH 10.4 and 4.4, Guth and Samaha, '701, reduced nicotinamid adenine dinucleotide diaphorase (NADH diaphorase, Novikoff et al., '611, succinate dehydrogenase (SDH, Pearse, '72), menadionelinked a-glycerophosphate dehydrogenase (a-GPD, Wattenberg and Long, '60),and a modified Gomori trichrome technique (Engel and Cunningham, '63). Myofibers cut in serial section and using the above histochemical procedures could be separated into three groups and classified according to Peter et al. ('72) as fast-twitch glycolytic (FG), fast-twitch oxidative glycolytic (FOG), and slow-twitch oxidative (SO) (Fig. 1). Microscopic fields from superficial, middle, and deep regions of each muscle cross section were photographed, and the three fiber types were identified and counted. Distribution of fiber types among the three fields was examined using a Kruskal-Wallis nonparametric analysis of variance (Noether, '76; Zar, '74). This was done to determine if there was a uniform distribution of fiber types throughout the cross-sectional area of each muscle. A Kruskal-Wallis analysis of variance and a nonparametric multiple comparison test was also used to determine differences in fiber type distribution between the wrist flexor muscles. When P < 0.05 was achieved the differences were considered significant. Contractile properties These studies were made on a total of 24 cats. The animals were given a n intraperitoneal injection of Nembutal anesthesia (35 mgkg). Additional anesthesia was administered when necessary throughout the experiment, using an indwelling catheter placed in the femoral vein. All of the insertion tendons of the wrist flexor muscles were cut and the muscles were then freed from surrounding connective tissue. Care was used not to disturb the blood supply to the muscles that were to be studied. A piece of the pisiform bone was kept in connection with the insertion tendon from the FCU. A steel hook was attached to each muscle tendon that was being prepared for recording using nylon suture. In this way, the muscle was ready for ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES 323 Fig. 1. Serial sectionsof the FCR showing the three fiber types: SO, FOG, and FG. x 350. a) ATPasealkaline preincubation; b) ATPase-acid preincubation; c) NADHdiaphorase; d) a-glycerophosphatedehydrogenase. 324 W.J. GONYEA. S.A. MARUSHIA. AND J.A. DMON attachment to a force transducer (Grass E"rl0). The cat was placed on a Narishige cat frame and a skin pool was erected on the limb to be examined. The pool was filled with mineral oil, which was maintained a t 37 2 1°C by a heating lamp. The cat's body temperature was maintained at the same range by a heating pad. The temperature of the oil and the rectal temperature were monitored by thermocouples. The limb was securely fastened to the frame by clamps placed on the humerus and around the wrist. Both the medial and ulnar nerves were dissected free and cut. The FCR, PLM, and the radial three heads of the FDP are innervated by the median nerve. The FCU and the ulnar two heads of the FDP are innervated by the ulnar nerve. Only one muscle per nerve was stimulated to fatigue. The nerve of the muscle to be stimulated was placed on silver bipolar electrodes. Stimulation was by monophasic pulses of 0.2 ms duration a t 2-3v in excess of the voltage required to obtain peak twitch tension. Each muscle studied was then set and maintained at optimal length for maximum twitch tension. The time to peak tension (CT), one-half relaxation time (%RT), and maximum tension (Pt)of a single isometric twitch were measured for each muscle. Tension-frequency curves were generated by stimulating each muscle nerve at 10 pulses/sec for about 2 sec. This procedure was continued every 60 sec with the stimulus frequency increased in increments of 10 pulses/sec until the muscle being stimulated exhibited a fused tetany. The preparation was then stimulated at 300 pulses/sec to determine maximum tetanic tension (Po)and the rate of tension development (VJ. The maximum tension developed at each stimulus frequency was also measured. Fatigue characteristics for each muscle were investigated by stimulating the muscle a t 40 pulses/sec for 330 ms at 1 sec intervals as described by Burke et al. ('71).The fatigue index (FI) was calculated by expressing tetanic tension measured at 2 min as a percentage of the maximum tension produced within the first 5 sec (Collatos et al., '77). All muscles were stimulated for a t least 30 min and the rate of fatigue (FR) was calculated as a percentage of the maximum tension taken a t 1 min intervals. the total wrist flexor mass. The FCR tookorigin from the medial epicondyle of the humerus by tendinous fibers (partly external aponeurosis). The muscle tapered gradually toward its insertion, and a n extensive aponeurotic sheet covered most of its deep surface. The terminal tendon (primarily internal aponeurosis) entered the paw through an osteofibrous canal where it was enclosed in a synovial sheath. At the metacarpus i t split into two strong tendons which inserted onto the palmar proximal surface of the second and third metacarpals. The FCR was innervated by the median nerve. The mean percentage of the three fiber types for three different regions (fields) taken from the cross-sectional area of each muscle were compared in Table 1. For the FCR muscle there was a significant difference in the distribution of FG and SO fiber types (Table 1; Fig. 1) with the SO fiber types concentrated in the deeper regions of the cross-sectional area of the muscle. This fiber type distribution for the FCR is similar to that previously described (Gonyea and Ericson, '77). The FCR had 35%FG fibers, 29% FOG fibers, and 36% SO fibers (Table 2). The contractile properties of the wrist flexor muscles are given in Table 3. The FCR had a short CT of 23 ms, but a much longer %RT of 31 ms. The Pt for this muscle was 0.27 kg while the P, for the FCR was 2.23 kg. The V, for the FCR was a slow 49 g ms-' while the PtP, was a n unusually low 0.14 (Table 3). The palmaris longus muscle (PLM) This muscle had a unipinnate internal fiber arrangement. The muscle weighed 1.90 rt 0.09 g, which was 12.1% of the flexor mass. The PLM took origin from a restricted area on the medial epicondyle (Fig. 2). In addition, it had the most superficial location of the forearm flexor muscles. The muscle arose by tendinous fibers (external aponeurosis) from the deep surface of the muscle belly. The muscle was fleshy for almost the entire length of the forearm and formed a tendon very near the carpus. Insertion was by a broad tendon formed from a n extensive aponeurotic sheet covering the distal half of the superficial surface of the PLM. The insertion tendon expanded into four or five incompletely separable tendons that contribute to the formation of the palmar aponeurosis. The PLM was innervated by the RESULTS median nerve. The flexor carpi radialis muscle (FCR) The PLM had an even distribution of all The FCR had a bipennate fiber pattern (Figs. three fiber types throughout its cross-sectional 2 and 3) and weighed 1.04 0.09g (mean 2 area (Table 1).This muscle consisted of 5% FG standard error of the mean) which was 6.59%of fibers, 29% FOG fibers, and 19% SO fibers * 325 ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES TABLE 1. Fiber type profile of wrist flexor muscles. Six animals were used for each muscle sample. % FG 5 t SEM) (X t SEM) Muscle Field FCR 1 (superficial) 2 (middle) 3 (deep) 47.1 t 4.3'.' 26.4 ? 5.0 23.4 2 3.9 30.8 t 4.5 35.0 t 3.2 22.4 2 3.1 22.1 t 3.0'.' 37.9 ? 3.5 54.2 t 3.0 PLM 1 2 3 60.0 ? 4.4 52.4 t 5.6 45.3 t 3.9 25.9 2 3.3 26.4 f 4.1 33.8 t 3.5 14.1 t 1.8 21.2 ? 2.5 20.9 t 2.8 FCUh 1 2 3 28.8 2 4.3 26.1 2 4.2 28.7 t 6.6 23.6 t 2.2 24.7 ? 3.4 20.2 t 1.2 47.6 2 4.9 49.2 t 7.1 51.1 t 6.1 1 2 3 43.6 t 5.7 34.2 t 5.3 39.0 t 5.8 24.7 t 3.1 27.4 f 3.0 24.7 t 4.0 31.7 ? 6.3 38.4 t 5.0 36.2 t 7.2 FDP, 1 2 3 71.8 2 1.6 69.4 i 0.64 72.6 2 1.5 26.6 t 2.2 29.2 ? 1.4 27.3 t 1.6 1.65 ? 1.7 1.50 t 1.2 0.10 f 0.06 FDP, 1 2 3 43.2 i 4.1 44.5 t 2.7 47.3 t 2.9 36.9 t 2.9 39.5 2 3.8 36.1 f 1.5 19.9 t 2.3 16.1 f 2.0 16.6 i 2.7 FDP, 1 2 3 58.1 2 3.2 52.9 2 4.7 56.7 t 3.4 31.3 t 3.0 37.1 ? 3.8 33.2 t 1.8 10.6 ? 0.90 10.0 t 1.0 10.1 ? 1.9 FDP, 1 2 3 50.7 t 4.3,J 40.2 2 4.3 52.9 f 5.1 40.3 t 4.6 45.0 2 4.7 39.9 ? 5.1 9.04 t 1.7'.4 14.7 i 2.6 7.30 i 1.1 FDP, 1 2 3 66.2 t 2.1 64.1 2 1.7 68.0 t 1.8 33.1 i 2.1 35.0 t 1.8 29.2 ? 2.2 0.63 t 0.40 0.73 t 0.48 2.73 ? 1.8 FCU, % FOG % SO (E t SEM) lP<O.OOl 2Significantly different from all other fields P<0.05 +Significantly different between fields 1 8 2 TABLE 2. Differences in fiber type distribution compared between the wrist flexor muscles' Muscle FCU, FCR-. FCU, FDP, FDP, PLM FDP, FDP, FDP, % FG (a ? SEMI 27.9 i 2.8 35.2 +- 3.5 38.6 2 3 . 2 1 '"1 47.9 45'0 t i- 2.8 52.6 ? 2.9 55.9 f 2.11 66.1 t 1.1 71.3 t 0.79 Muscle FCU, FCU[I FDP, PLM FCR FDP, FDP, FDP, FDP, % FOG (E i SEMI 22.8 i 1.4 25.6 t 1.9 1 28.7 2 2.2 29.3 f 2.8 32.5 k 1.3 33.9 t 1.7 37.5 t 1.6) 41.7 ? 2.7 1 Muscle FDP, FDP PLM FCU. FCU, FCR % SO (X t SEM) 0.81 2 0.391 1.07 t 0.67J 10.4 ? 1.3 17.5 ? 1.3 18.7 ? 1 . 5 1 35.4 2 3.5 35.5 ? 3.7 49.3 t 3.3 3 *Means contained within brackets did not differ significantly. All comparisons outside brackets were significantly different, P i 0.05. Six animals were used for each muscle sample. (Table 3, Fig. 5).The PLM had a very short CT The flexor carpi ulnaris (FCU) of 24 ms. The %RTwas nearly the same as CT a t 26 ms. The Pt for the PLM was 0.43 kg,while P,, This muscle consisted of two heads proxwas 2.95 kg. The Vt was a rapid 61 g m-' and imally which unite to insert by a single tendon (Fig. 3). The internal fiber arrangement Pdg was 833 g. 326 W.J. GONYEA, S.A. MARUSHIA, AND J.A. DMON TABLE 3. Contractile properties of wrist flexor muscles* Muscle CT, ms FCR 23.2 FDP, 23.8(::0.98] PLM 23.9 FDP, ? Muscle FDP, 0.85 FDP, f 0.90 PLM (24) 24.2 t 1.5 J FCR (8) FCU Muscle FCU FCU 37.0 f 2.2 (16) P,, kg Muscle 2.15 t 0 . 3 4 7 FCR FCR FDP, (24) 2.95 t 0.45J (24) 4.43 & 0.46 FDP, 5.57 t 0.47 J FCU PLM (8) 16.7 c 1.2 (8) 18.0 2 1.3 (8) 26.3 2 2.3 (24) 30.5 c 2.6 (24) 73.5 f 6.5 (16) m Muscle ] ] o 1 PLM 0.19 f 0.01 I + MRT, ms Muscle PLM (24) FCR FCU (24) 111.8 t 6.8 (16) FDP, Muscle Vt, g * ms-l Muscle PLM 44.4 f 5.47 Pdg FCU 7] 12 J 101 FDP, ] 0.95 ? 0.13 (8) 662 2 84 (15) (24) 61.4 t 8 . 2 9 FDP, 124) 86.7 2 10 FCR (8) FDP, Pt,kg 0.27 & 0.03 (24) 0.43 2 0.05 (24) 0.47 % 0.07 (16) 0.81 k0.08 FDP, (8) 0.19 2 O . O ~ FDP, (24) 0.22 f 0.01 (16) CT FDP,, 0.14 2 0.01 1 FCU (24) 0.17 f 0 . 0 2 4 FCR (8) FDP. ~ (XI %RT,ms 18) (16) 1,146 f . l O 9 J (8) *Means contained within brackets did not differ significantly. All comparisons outside brackets were significantly different, P muscles tested) (8) C 0.05. (Number of primarily a unipennate fiber arrangement. The first head (FDP,) arose by fleshy fibers from the flexor surface of the ulna. Its fibers converged to form the medial portion of the common insertion tendon (Fig. 8). The first head had a uniform fiber distribution (Table 1) which consisted of 71% FG fibers, 28% FOG fibers, and 1% SO fibers (Table 2; Fig. 9). The second head (FDP,) arose by tendinous fibers from the distal end of the medial epicondyle of the humerus just deep to FDP, (Fig. 8). Its fibers joined with FDP,. This head had a uniform fiber distribution (Table 1) which consisted of 45% FG fibers, 38% FOG fibers, and 17% SO fibers (Table 2; Fig. 4). Heads one and two were innervated by the ulnar nerve. The portion of the FDP innervated by the ulnar nerve (FDP,) had a CT of 24 ms and a short %RT of 18 ms. The Pt for this muscle was 0.81 kg while the P,,was 4.43 kg. The Vt was a very fast 87 g ms-', while P,/g was 870 g. The third head (FDP,) arose by a strong tendon (external aponeurosis) from the middle portion of the medial epicondyle (Figs. 2 and 3). It also shared an aponeurotic sheet with the FCR a t the proximal end of that muscle. The The flexor digitorum profundis (FDP) FDP, had a uniform fiber type distribution This muscle arose by five separate heads. The (Table 1) which consisted of 56%FG fibers, 34% FDP weighed 9.48 % 0.78 g , which was 60.3% FOG fibers, and 10% SO fibers (Table 2; Fig. of the wrist flexor muscle mass. The muscle had 11). was unipennate and the muscle weighed 3.30 0.21 g, which was 21.0% of the total wrist flexor mass. One head arose from the medial epicondyle of the humerus (FCU,,) by a strong short tendon which was formed by a broad aponeurotic sheet on the superficial surface of the muscle. The second head had a fleshy origin from the medial surface of the proximal third of the ulna (FCU,), and the origin extended onto the surface of the olecranon process. The FCU inserted onto the proximal surface of the pisifonn bone by tendinous and fleshy fibers. The FCU was innervated by the ulnar nerve. Both FCUh and FCU, had uniform muscle fiber type distributions (Table 1).The FCUh had 28% FG fibers, 23% FOG fibers, and 4% SO fibers (Table 2; Fig. 6). The FCU, had 3wo FG fibers, 26%FOG fibers, and 35% SO fibers (Fig. 7). The CT for the FCU was a long 37 ms while the %RT was an even longer 74 ms. The Pt was 0.47 kg and the P, was only 2.15 kg. The Vt was a slow 44.4 g ms-I while P,,/gwas a low 662 g (Table 3). - ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES 327 \ J Fig. 2. Diagrammatic representation of the cat’s superficial forearm flexor muscles. Fig. 3. Diagrammatic representation of the cat’s intermediate forearm flexor muscles. 328 W J . GONYEA, S.A. MARUSHIA, AND J.A. DIXON Fig. 4. Representation fiber type distribution in the second head of FDP. x 140. a) ATPase-alkaline preincubation; b) NADH-diaphorase. Fig. 5. Representative fiber type distribution in the PLM. x 140. a) ATPase-alkaline preincubation; b) NADHdiaphorase. ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES 329 Fig. 6. Representativefiber type distributionin the humeral head of the FCU. x 140. a) ATPase-alkaline preincubation; b) NADH-diaphorase. Fig. 7. Representativefiber type distribution in the ulnar head of the FCU. x 140. a) ATPase-alkaline preincubation; b) NADH-diaphorase. 330 WJ.GQNYEA, S.A. MARUSHIA, AND J.A. DIXON \ Fig. 8. Diagrammatic representation of the cat’s deep forearm flexor muscles. The fourth head (FDP,) also arose from the medial epicondylejust medial and deep to that of FDP, and deep to the origin of the PLM (Figs. 8 and 12). The FDP, had a nonuniform fiber type distribution with a slight but significant concentration of the FG fibers peripherally and SO fiber concentration in the core of the muscle (Table 1).The FDP, fiber type proportions were 48% FG fibers, 42% FOG fibers, and 1Wo SO fibers (Table 2; Fig. 13). The fifth head (FDP,) arose by fleshy fibers from the flexor surface of the radius and the adjacent parts of the interosseous membrane (Figs. 8 and 12). This head lies deep to the insertion tendon of the FCR and most of its fibers join the tendinous portion of the FDP,. The FDP, had a uniform fiber type distribution (Table 1) which consisted of 66%FG fibers, 33% FOG fibers, and 1%SO fibers (Table 2; Fig. 10). These three heads were innervated by the median nerve (FDP,). The FDP, had a CT of 24 ms and a very short %RTof 17 ms. The P, for the FDP, was 0.95 kg and the P, was 5.6 kg. The V, was a very fast 101 g ms-I while the P,/g was a very high 1,146 g. All five heads form a large common insertion tendon. The tendon divided into five strong tendons which pass to the five digits, and inserted into the base of the terminal phalanx. Fiber type distribution. It can be observed that most of the wrist flexor muscles, except the FCR and FDP,, had a uniform muscle fiber type distribution throughout their cross-sectional area. For the FDP, the very small percentage of SO fibers were concentrated in the central region of the muscle. For the FCR, the SO fibers were concentrated in the deep portion of the muscle (Table 2). A comparison was made of the percentage of the three fiber types between all the wrist flexor muscles (Table 2). The percentage of FG fiber types ranged from 27.9%to 71.3%, and the FCUhhad a significantly smaller concentration of the FG fiber types and the FDP, had a significantly larger concentration of FG fiber types when compared with the other wrist flexor muscles (Table 2). Except for FCR and FCU,, FDP, and FDP4,and PLM and FDP,, all other possible combinations demonstrated a significantly different percentage of FG fibers (Table 2). There was a dramatic reduction in the mean range for the percentage of FOG fiber types when compared with the range for the FG fibers for the wrist flexor musculature (Table 2). The percentage of FOG fibers ranged from 22.8 to 41.7. As was the case for the FG fibers, the FCU, had the lowest percentage of FOG fiber ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES 33 1 Fig. 9. Serial sections of the first head of the FDP fiber type distribution consisting of only fast twitch fibers. x 140. a) ATPas+alkaline preincubation;b) ATPase-acid preincubationc).) NADH-diaphorase;d) a-GPD. 332 W.J. GONYEA, S.A. MARUSHIA, AND J.A. DIXON Fig. 10. Representative sections of the fifth head of the FDP showing that it consists of nearly 100% fast-twitch fibers. x 140. a) ATF'ase-alkaline preincubation;b) NADH-diaphorase. Fig. 11. Representativefiber type distribution of the third head of the FDP. x 140. a) ATPaealkaline preincubation; b) NADH-diaphorase. ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES 333 Fig. 12. Diagrammatic representation of the deeply situated forearm flexor muscles. types and this concentration was significantly lower than all the other wrist flexor muscles (Table 2). The FDP, (37.5%) and the FDP, (41.7%)had the highest percentage of FOG fibers and these values did not differ significantly between these two muscles but were significantly higher than the other wrist flexor muscles. The percentage of SO fiber types for the wrist flexor muscles ranged from 0.8 to 49.3. The lowest concentration of SO fiber types was less than 1%(0.81%)for FDPS,which did not differ significantly with that for FDP, (1.07%). The FCUh had the greatest relative number of SO fibers with 49.3%0(Fig. 6), which was a significantly greater proportion of SO fibers than the other wrist flexor muscles (Table 2). The single joint wrist flexor muscles, FCUh, FCU,, and FCR, were very similar in fiber type composition, with a mean fast-twitch percentage of 51,64, and 65 (FG and FOG fibers), and the oxidative percentage (SO and FOG fibers) was 72, 61, and 65, respectively. However, the FCR had compartmentalized fiber type distribution, whereas the other two muscles had a uniform fiber type distribution (Tables 1and 2). The six remaining multijoint flexor muscles had a very high percentage of fast-twitch muscle fibers. The PLM and FDP, had 81% and 83%,the FDP, and FDP, both had 9Wo ,and the FDP, and FDP, both had 99% fast-twitchfibers. In addition, only the FDP, (55%) and FDP, (5wo)had a proportion of oxidative fibers that was greater than 50%. The PLM (47%) and FDP, (44%) had just slightly less than 5@%, whereas FDP, had only 33% and FDP, 29% oxidative fiber composition. Contractile properties. The mean CT for the wrist flexor muscles was less than 25 ms, except the FCU, which had a mean CT of 37 ms, and this was a significantly longer CT than all other wrist flexor muscles (Table 3). The mean %RT was also significantly longer for the FCU and significantly shorter for the FDP when compared with the other wrist flexor muscles (Table 3). The mean CT + Y2RT for the FCU was more than twice as long (111.8 ms) as that for the other muscles. The maximum Pt was significantly smaller for the FCR and greater for the FDP muscles when compared with the other wrist flexor muscles, which indicated the smallest and largest muscle weights respectively for these two muscles. However, only FDP developed a significantly greater Po when compared with that for the other muscles. The Poper gram of muscle showed that all the wrist flexors were similar i n tension development except the FCU, which produced significantly less tension 334 W.J. GONYEA, S.A. MARUSHIA, AND J.A. DIXON Fig. 13. ATPase and oxidative activity showing the oxidative (a, b) and glycolytic (c, d) region in the fourth head of the FDP. x 140. a) ATPase-alkaline preincubation; b) NADHdiaphorase; c) ATPase-alkaline preincubation; d) NADH-diaphorase. ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES per gram of muscle than the other muscles (Table 3). The ratio PJP, was significantly higher for the FCU (0.22) and significantly lower for the FCR (0.14) when compared between muscles. As would be expected for their fiber type composition, the FDP (101 pms-I) had the fastest V,, while the FCU had the slowest V, (44.4 g-ms-'). The fatigue index was plotted against the mean percentage of SO fibers and mean percentage of oxidative fibers (SO + FOG) for each muscle (Fig. 14). All of the wrist flexor muscles had fewer than 50% SO fibers, and all of the muscles except the FCU had a fatigue index of less than 0.50. The inclusion of the FOG fibers resulted in a smaller range for the mean percentage oxidative composition for all muscles (39-67%) than with just the SO fibers (7-42%). Both the FCR and FCU were dominated by oxidative fibers; however, the relative increase in SO fibers for the FCU when compared with the FCR resulted in a substantial difference in the fatique index between these two muscles (0.48 vs. 0.63; Fig. 14). The wrist flexor muscles were stimulated for 30 min and the percentage tension lost was measured (fatigue rate). It was observed (Fig. 15) that the FCU was the most fatigue-resistant and the FDP the most fatigable of the wrist flexor muscles. The FCU lost 37% of its tension after 2 min of stimulation and 52% after 7 min of stimulation, after which point no additional tension was lost. The FCR lost 51% of its tension after 2 min of stimulation and continued to lose tension for 10 min of stimulation, a t which time only 25% of the maximum tension remained. At this point a steady state was reached. The PLM lost 58%of its maximum tension after 2 min and continued to lose tension gradually throughout the 30 rnin stimulation period, a t which point 30% of the maximum tension remained (Fig. 15). The two components of the FDP lost 60% of their maximum tension after 2 min of stimulation. The tension continued to decline throughout the stimulation period with only 1Wc of the max tension remaining a t the end of this period. The tension produced a t different stimulation frequencies was expressed as percentage of mean P, for each muscle (Fig. 16). The FCU developed a greater percentage of Po at the lower stimulus frequencies when compared with that of the other muscles. The FCR developed a relatively smaller percentage Po than the other muscles. 335 DISCUSSION The wrist joint of the cat was not simply a hinge joint allowing flexion and extension; i t also provided some rotation and ulnar and radial deviation. In fact, it has been demonstrated that rotation a t the wrist joint is necessary to facilitate foot placement during locomotion (Gonyea, '78). It has also been demonstrated that both forearm flexor and extensor muscles of the cat that cross the wrist have monosynaptic excitatory connections of IA afTerents to heteronomous motor neurons (Willis et al., '66). This pattern of excitatory monosynaptic input to supposedly antagonistic motor nuclei has been correlated with the function of the retractile claw apparatus for the cat. Gonyea and Ashworth ('75) have demonstrated that in order for the cat to protrude its retractile claws, both the flexor and extensor muscles must act in a synergistic fashion to fix the wrist and the metacarpolphalangeal and interphalangeal joints. This action was necessary because of the FDPs protruding the claws against the resistance of a n elastic retractor ligament. This study has demonstrated that the claw retractile muscles, the FDP, were dominated by powerful fast-twitch fibers. The FDP constituted 60.3%of the flexor muscle mass. All heads of this muscle were dominated by fast-twitch fibers. This muscle was innervated by two major nerves; heads 1and 2 were innervated by the ulnar nerve and heads 3 , 4 , and 5, by the median nerve. The extreme ulnar (FDP,) and radial (FDP,) heads had a very similar fiber composition, as both had 1% or less SO fibers and over 60%FG fibers. With its insertion onto the distal phalanx and providing the force for claw protrusion, the FDP appeared to be organized for very powerful and rapid movements with very little endurance. Like the flexor muscles of the elbow, knee, and ankle joints of the cat (Ariano et al., '73; Burke et al., '74;Collatos et al., '771, most of the muscles for the wrist joint can be characterized as primarily fast (< 25% SO) on the basis of their fiber type composition. Of the nine different muscle bellies constituting the four major wrist flexor muscles, those that spanned several joints (multiarticular) all had less than 20%SO fibers. These included the five heads of the FDP and the PLM. In fact, the extreme ulnar head (FDP,) and the extreme radial head (FDP,) of the FDP were found to have essentially 100%fast fibers for they contained 1%or less SO fiber types. The two heads of the FCU 336 W.J. GONYEA, S.A. MARUSHIA, AND J.A. DIXON . 0 FDP, c < - FOPm FCU A FCR A PLM 0 0.60 , FDP, FCU A FCR .. A PLM - 0.20- 0 80 60 20 100 40 X Oxidotive Fibers Fig. 14. Mean fatigue indexes (tetanictension at 2 min as percentage maximum tension) from each muscle are plotted against the mean percentage of SO fibers and oxidative fibers (SO and FOG) for each muscle. 2 4 6 8 10 20 Stimulus Time ( m i d 30 Fig. 15. Mean percent tetanic tensions for each muscle are plotted against the time muscle has been stimulated at a rate of 40 pulsedsec for 330 ms at 1-secintervals. Numbers of observations are given in Table 3. 100 80 0 FDP, FDPm FCU A FCR A PLM 60 *a" 40 20 0 20 40 60 80 Stimulation Frequency 100 '3, Fig. 16. Mean percent maximal tetanic tensions (% Po) for each muscle are plotted for different frequenciesof stimulation. Numbers of observations are given in Table 3. ANATOMY AND PHYSIOLOGY OF FOREARM MUSCLES and the FCR are essentially uniarticular, and even though FCUh and FCR arise from the humeral epicondyle, they have no moment arm a t this joint. All three muscles contain a significantly higher proportion of SO fibers than the multiarticular muscles. However, these muscles cannot be characterized as predominantly slow (8Wo SO) as has been observed for extensor muscles (Ariano et al., '73; Burke et al., '74; Collatos et al., '77). A high density of SO fibers has been correlated with postural muscles and even though the wrist joint is fully extended during quiet standing and rest, antihyperextension seems to be provided by ligamentous support (Gonyea, '78) and not by muscle activity a s measured by EMG activity (unpublished observations). Both the FDP, and the FCR had an uneven fiber type distribution. The SO fibers for the FDP, were concentrated in the core of the muscle. However, this muscle had only 10% SO fibers, and therefore a slight concentration of SO fibers in the core of the muscle may not be important in the function of the muscle. For the FCR, however, the SO fibers were found to be concentrated in the deep region of the muscle and the difference in fiber type distribution was highly significant (Table 11, which supports our earlier findings (Gonyea and Ericson, '77). The muscle spindles have been shown to be concentrated in the oxidative compartment of the FCR (region high in SO and FOG fiber types) (Gonyea and Ericson, '771, and it has been postulated that the compartmentalization of fiber types and spindles in the FCR may demonstrate a strong structure-function relationship (Botterman et al., '79). Accordingly, motor units may be spatially separated within the FCR, being restricted to one of the fiber type compartments. The significant difference in the size of the muscle fiber types when compared between the oxidative and glycolytic compartments (Gonyea, '79) and the presence of intramuscular nerve branches that are unique to each compartment (Galvas and Gonyea, '80) lends support to the concept of spatial separation of motor units. Intramuscular nerve branches have also been shown to supply muscle fibers in a restricted territorial volume in the gastrocnemius muscle of the cat (Letbetter, '74). The control of wrist position during locomotion and the necessity to maintain the wrist in a pronated position during locomotion may, in part, require a more complex structural organization for the radial wrist flexor, the FCR, than that observed on the ulnar side. This organizational difference may 337 imply differences in the motor control between the ulnar and radial sides of the wrist musculature. This hypothesis has been supported by our finding a substantial difference in the rostrocaudal distribution of motor nuclei in the cervical cord for these two muscles (Iwamoto et al., '80). In this regard, the FCR had an extensive longitudinal distribution for its motor nucleus, whereas the FCU had a very confined distribution, which may reflect spatial separation of afferent input to the FCR motor nucleus. Each muscle belly had a reasonably distinct muscle fiber type composition. There was far less difference in the percentage of FOG fiber types than the SO or FG fiber types when compared between muscles (Table 2). In a comparison of the fiber type distribution for the two primary wrist flexor muscles, FCR and FCU, there was no significant difference for all three fiber types between the FCR and FCU,. However, the FCUhwas significantly different from all other muscles in its fiber type composition, for it was dominated by SO fibers (49.3%). Hence there was one portion of FCU that had a similar fiber type composition to t h a t of the FCR. However, the FCU weighed 3.3g while the FCR only weighed 1.04g. It appeared that the FCU had an additional oxidative component (FCUh) which resulted in this muscle's having a uniquely oxidative fiber composition when compared to the other muscles. The functional differences between the FCR and FCU are unknown a t this time. Although during grasping, wrist flexion is also accompanied by ulnar deviation which may require a fatigue-resistant capacity to maintain this position and may account for the relative increase in SO fibers in the FCU when compared with the other muscles; whereas ulnar wrist control required a n oxidative component, this property was not present on the radial side. All of the wrist flexor muscles had a very short CT (between 23 and 24 ms) except the FCU, which had a CT of 37 ms. It has been adequately demonstrated that CT increases with greater percentages of SO fibers (Collatos et al., '77; McPhedranet al., '65;Wuerkeret al., '65)as was the case in this study with the FCU. In fact, the CT + %RT was over twice as long for the FCU as any other wrist flexor muscle. As would be expected, the smaller muscles produced less tension than the heavier muscles. However, the ratio PJP, was significantly higher for the FCU than the other wrist flexor muscles, which was probably related to the relatively high percentage of SO fibers for that muscle (Close, '72). The FCR, however, had a 338 W.J. GONYEA, S.A. MARUSHIA, AND J.A. DIXON very low P+/P, ratio, which was significantly smaller than all other muscles except the FDP, and was quite low for the values of other fast muscles that have been reported which usually are near the value of 0.2 (Close, '72). This difference may be related to the differences in the organization of the FCR with the compartmentalization of fiber types substantially altering the mechanical properties of this muscleduring a single isometric twitch. It has been recently demonstrated that the motor nucleus for the FCR had an extensive rostrocaudal distribution in the cervical spinal cord when compared with that of the FCU or to the distribution of the motor nuclei in the lumbar cord for hindlimb muscles (Burke et al., '77; Iwamoto et al., '80). The complex organization of the FCR and the differences in morphological and contractile properties between the FCR and FCU may reflect the need for complex motor programs for controlling the prehensile movements of the distal limb musculature. 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