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Distribution and Innervation of Short, Interdigitated Muscle Fibers in Parallel-Fibered Muscles of the Cat Hindlimb

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Distribution and Innervation of Short, Interdigitated Muscle Fibers in Parallel-Fibered Muscles of the Cat Hindlimb JOURNAL OF MORPHOLOGY 191:l-15 (1987) Distribution and Innervation of Short, lnterdigitated Muscle Fibers in Parallel-Fibered Muscles of the Cat Hindlimb G.E. LOEB, C.A. PRAlT, C.M. CHANAUD AND F.J.R. RICHMOND Laboratory of Neural Control, National Institute of Neurological and Communicative Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, 20205; and Department of Physiology, Queen's University, Kingston, Ontario, Canada K7L 3N6 ABSTRACT The cat hindlimb contains several long, biarticular strap mus- cles composed of parallel muscle fascicles that attach to short tendons. Three of these muscles - sartorius, tenuissimus, and semitendinosus - were studied by dissecting individual gold-stained fibers and determining the surface dis- tribution of acetylcholinesterase-stained end-plate zones. In each muscle, fascicles were composed of muscle fibers that ran only part of the fascicle length and tapered to end as fine strands that interdigitated with other taper- ing fibers within the muscle mass. Most muscle fibers measured 2-3 cm in length. Fascicles of muscle fibers were crossed by short transverse bands of endplates (1 mm wide by 1-5 mm long) that were spaced at fairly regular intervals from the origin to the insertion of the muscle. The endplate pattern suggested that the fiber fascicles were organized into multiple longitudinal strips. In the sartorius, the temporospatial distribution of electromyographic (EMG) activity evoked by stimulating fine, longitudinal branches of the parent nerve confirmed that each strip was selectively innervated by a small subset of the motor axons. These axons appeared to distribute their endings through- out the entire length of the fascicles, providing for synchronous activation of their in-series fibers. Although mammalian muscles can exhibit Much less attention has been paid to the a remarkable variety of forms (Warwick and differences in muscle fiber organization that Williams, '731, most can be classified as pin- may occur within the muscle fascicles them- nate or parallel according to their fiber ori- selves. For example, it is often assumed, and entations (e.g. McMahon, '84; Pierrynowksi occasionally reported (e.g., Sacks and Roy, and Morrison, '85). Pinnate muscles are usu- '82) that the long fascicles of parallel-fibered ally composed of fibers that are much shorter muscles are comprised of similarly long in- than the muscle as a whole and run obliquely dividual muscle fibers, running the entire between two (or more) closely approximated length of each fascicle and attached at both planes of attachment. In contrast, parallel- ends to the muscle origin and insertion. Such fibered muscles commonly consist of fiber an organization, if it exists, would pose seri- fascicles running most of the length of the ous problems for the mechanical stability of muscle and arranged in sheet-like or strap- long muscles. Because conduction velocities like arrays that are parallel to the line-of- in mammalian extrafusal muscle fibers are pull of the muscle. The functional signifi- typically 2-10 dsec (Eccles and O'Connor, cance of fascicle arrangements in pinnate '39; Schwartz-Giblinet al., '84), muscle fibers versus parallel muscles has been examined spanning the 15 cm length of some cat mus- theoretically and experimentally in some de- cles would have propagation times in excess tail (Gans and Bock, '65;Gans, '82), and it is of their twitch rise times. As a result, central now well recognized that the architectural portions of long muscle fibers would begin to arrangement has a significant effect on the length-tension relationship, shortening ve- Address reprint requests to Dr. G.E. Loeb, National Institutes locities, and force-developing capabilities of of Health, Bldg. 36, Rm. 5A429, 9000 Roekville Pike, Bethesda, the muscle. MD 20205. 0 1987 ALAN R. LISS, INC 2 LOEB ET AL I(Fig. 1). These results have been supple- mented by histochemical studies of motor endplate distributions and, in the case of sar- torius, by studies of electrically evoked elec- tromyographic (EMG) and muscle-nerve activity resulting from focal microstimula- tion of nerve branches supplying narrow lon- gitudinal strips of the muscle. The various anatomical, mechanical, and physiological specializations are discussed in relation to the special mechanical properties and control problems of long, parallel-fibered muscles. MATERIALS AND METHODS Muscle microdissection A total of four sartorius, four semitendino- sus and eight tenuissimus muscles were dis- sected from eight adult cats weighing 2.8- 4.2 kg, that were killed with an overdose of sodium pentobarbital. The animals had sim- ilar skeletal dimensions but differed in obes- ity. In seven cats, muscles were removed immediately after death, but in a single cat, hindlimb muscles were allowed to go into rigor for 3 hr so that fiber and sarcomere lengths would be stabilized prior to dissec- Fig. 1. Anatomical arrangement of the cat hindlimb tion. Muscles were measured and pinned to muscles studied. TEN, tenuissimus; SAa, sartorious pars parain blocks. They were immersed in 25% anterior; SAm, sartorius pars medialis; STp, semitendi- formic acid for 30-240 min, blotted, and im- nosus proximal head; STd, semitendinosus distal head. pregnated in gold chloride. For individual muscles, the concentration of gold chloride ranged from 0.5-2.0% and exposure times contract while their distal portions were still ranged from 1-18 hr. The varied impregna- relaxed; this would stretch out the passive tion schedules were employed to provide a sarcomeres at the fiber ends. There appear selection of muscles with different degrees of to be two ways in which long parallel-fibered staining and fiber strengths; prolonged ex- muscles have been structured to circumvent posure to gold chloride increases the depth this problem. A few muscles (including sem- and quality of staining but causes fibers to itendinosus, rectus abdominis, and the neck become brittle. Muscles were blotted and re- muscles, biventer cervicis and splenius) are duced overnight in 25% formic acid, then subsectioned by tendinous inscriptions into a washed thoroughly in tap water and stored number of short, serially-arranged compart- in glycerin for up to 24 months. Prolonged ments, so that the fascicle lengths are only a immersion in glycerin softens the connective fraction of the muscle length as a whole (Bar- tissues within muscle and facilitates single deen, '03; Cullen and Brodal, '37; Tobias and fiber dissections. Arnold, '63; Bodine et al., '82; Armstrong et Each stained muscle was subdivided into al., '82; Richmond et al., '85). Other parallel- muscle bundles measuring about 1-3 mm in fibered muscles have no inscriptions, but in- the transverse plane and running from mus- stead appear to be composed of short muscle cle origin to insertion. From a sampling of fibers that are distributed in serial or over- these bundles were dissected 10-50 muscle lapping arrays (Bardeen, '03; Huber, '16; Ad- fibers to assess the quality of staining in each rian, '25; Cooper, '29; Coers, '59). specimen. The preliminary dissections estab- In our study, microdissection techniques lished that all three hindlimb muscles were were used to analyze the lengths and ar- predominantly composed of muscle fibers less rangements of individual, gold-stained mus- than 4.0 cm in length and these had typical cle fibers from three cat hindlimb muscles - interfascicular terminations (cf. Richmond et sartorius, tenuissimus, and semitendinosus al., '85). However, it was not possible from MUSCLE-FIBER ORGANIZATION IN NONPRIMATE MUSCLES 3 these random dissections of fiber bundles to and uneven photographic contrast; hence, discern whether regional differences existed endplate distribution is shown as an anatom- in muscle-fiber length or patterns of termi- ical drawing made from a combination of nation. Thus, systematic fiber dissections these photographs and the actual stained were carried out in two sartorius, one semi- specimen (Fig. 8). tendinosus, and two tenuissimus muscles whose muscle fibers showed sufficient tensile strength that fascicles could be microdis- sected into their component fibers with little Evoked potential mapping fiber breakage. Every effort was made to analyze the features of each fiber encoun- The sartorius muscle was selected for elec- tered in sequence during the teasing process trophysiological studies because its intra- to minimize the possibility that fibers were muscular nerve branches are clearly visible selected in a nonrandom manner. Because and readily accessible on the inner surface of of the nongaussian distributions of fiber this broad, thin muscle. In three pentobarbi- lengths, we calculated both means and me- tal-anesthetized animals, the left sartorius dians of various populations, although these muscle was surgically exposed and reflected were never significantly different. to expose its nerve supply and the adjacent A similar number of fibers in all muscles saphenous nerve. Both electrical stimulation was further studied at the light microscopic and recordings were made with hand-held level by mounting the fibers in glycerin on electrodes consisting of closely spaced (2-3 glass slides. In each muscle, sarcomere mm) bipolar balls or nerve hooks formed on lengths for some fibers were determined by the end of 0.010 inch platinum wire. To acti- directly measuring the distance spanned by vate fine intramuscular nerve branches, the ten sarcomeres using a ~100oil immersion ball electrodes were positioned directly
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