Intramuscular Length Changes and Complex Length-Tension Relationships During Stimulation of Individual Nerve Branches

The feline anterior sartorius is a long strap-like muscle composed of short muscle fibers. Nerve branches that enter this muscle contain the axons of motor units whose constituent muscle fibers are distributed asymmetrically within the muscle. In the present study, twitch and tetanic isometric contractions were evoked by stimulating individual nerve branches while muscle force was recorded and intramuscular length changes were monitored optically by the movement of reflective markers on the muscle. Contractions elicited by stimulating the parent nerve produced little change in the positions of the surface markers. Contractions elicited by stimulating the proximally or distally directed nerve branches caused the muscle to shorten at the end closest to the nerve branch and lengthen at the opposite end. Some muscles were supplied by a centrally directed nerve branch whose stimulation produced variable effects: in some cases a portion of the muscle shortened whereas the rest lengthened, but in other cases, the positions of the surface markers showed little change. The intramuscular length changes produced by stimulating single nerve branches were greater during isometric contractions at short whole-muscle lengths than at long whole-muscle lengths. The twitch and tetanic length-tension relationships obtained by stimulating the individual nerve branches were not congruent with the length-tension relationship produced when the parent nerve was stimulated. At short whole-muscle lengths, stimulation of a single nerve branch generated only a small fraction of the force that could be generated by the muscle when the parent nerve was stimulated. As whole-muscle length increased, an increased fraction of total muscle force could be generated by stimulating a single nerve branch. The results suggest that a complex relationship between passive and active elements contributes to the total muscle force and depends on the distribution of active and passive muscle units throughout the muscle. o 1992 Wiley-Liss, Inc. A common presumption in the field of muscle physiology is that the force generated by a whole muscle is a scaled-up version of the force generated by a single motor unit; in turn, the force generated by a single motor unit is a scaled-up version of the force generated by a single muscle fiber. This assumption seems plausible for simple muscles such as cat soleus in which all muscle fibers extend the full length of their fascicles, from the connective tissue of the origin to that of the insertion (Burke et al., ’74). However, this assumption may not be true for muscles that have more complex architectural organizations. One of the specializations that has potentially important implications for the mechanics of muscle is the construction of long muscle fascicles from short muscle fibers. Two modes of construction are used, alone or together, to create long contractile assemblies. In some muscles, fibers are linked in-series by tendinous inscriptions; in others, fibers taper and end intrafascicularly. The former strategy divides the muscle longitudinally into a series of shorter “mini-muscles’’ as exemplified by cat semitendinosus, splenius, and biventer cervicis (Bodine et al., ’82; Richmond et al., ’85; Armstrong et al., ’88). The mechanics of the individual compartments o 1992 WILEY-LISS, INC. 172 S.H. SCOTT ET AL might individually follow the relatively simple rules described above. However, control of the overall force of the ensemble of inseries compartments would be complicated, particularly if all compartments were not recruited identically. In the latter strategy, which is perhaps more common in long muscles, serial linkages between fibers are not clearly demarcated by gross anatomical landmarks such as tendinous inscriptions. Instead, muscles such as cat tenuissimus, biceps femoris, and medial and anterior sartorius have long muscle fascicles composed of short tapering fibers that end intrafascicularly (Adrian, '25; Loeb et al., '87; Lev-Tov et al., '88; Chanaud et al., '91). These fibers do not attach to tendinous tissue that might direct the force generated by the fiber onto the muscle origin and insertion. Rather, the muscle fibers appear to couple their forces into the connective tissue enveloping their tapered (and possibly nontapered) portions (Trotter, '90; Trotter and Purslow, personal communication). Adjacent fibers generally belong to different muscle units (Smits et al., '911, so that tension must be transmitted for some distance laterally across inactive fibers when only a few motor units have been recruited. Force transmission in the muscle is further complicated by the complex arrangement of muscle-unit territories. Anterior sartorius is supplied by two or three nerve branches that contain largely separate populations of axons and enter the muscle a t different rostrocaudal levels. Groups of motor units supplied by a single nerve branch are distributed asymmetrically within anterior sartorius both in the proximodistal and mediolateral axes of the muscle (Thomson et al., '91). Further, the muscle fibers in a single motor unit are distributed over much of the length of the muscle in a circumscribed strip-like territory, but with markedly different numbers of fibers from one end of the muscle to the other (Smits et al., '91). Thus, the cross-sectional area of muscle fibers supplied by an individual motoneuron and even by a whole nerve branch varies markedly at different proximodistal levels along the muscle. The complex architecture of anterior sartorius provides an anatomically well-characterized and experimentally accessible model in which to examine at least some of the mechanical properties that can emerge in such muscles during different patterns of motorunit recruitment. In this muscle, the smallest controllable unit of muscle-the motor unit-cannot generate a uniform force from one end of the muscle to the other. However, it is not yet clear how force generation and transmission will be affected by the lateral and longitudinal interposition of passive, relatively compliant muscle units among active muscle fibers. The problem is interesting not merely from a theoretical point of view; the properties of long muscles with short fibers must be understood as a first step in designing appropriate methods to re-animate paralyzed limbs. Implantable electronic devices are being developed to produce functional recovery of paralyzed muscles by stimulating muscle nerves a n d / o r in t ramuscular branches of motoneurons (Grandjean and Mortimer, '86). I t is important to understand the forces that may be produced and transmitted if such stimulation results in the uneven recruitment of muscle fibers along the length of a long muscle. In this study, we have analyzed the mechanical characteristics of contractions evoked by stimulating nerve branches known to supply asymmetrically distributed muscle territories. The time-course and amplitude of the resulting forces were associated with optically measured changes in intramuscular lengths during whole muscle isometric contractions. These features were compared to the mechanics of contractions produced by synchronous stimulation of all nerve branches supplying anterior sartorius. MATERIALS AND METHODS