Evidence for compartmental identity in the development of the rat lateral gastrocnemius muscle

Abstract

In adult rats, each neuromuscular compartment of the lateral gastrocnemius muscle (LG) is exclusively innervated by a primary branch of the LG nerve. In neonates, however, a small percentage of LG cells receives inputs from more than one primary nerve branch; these inputs are known as cross-compartmental. Cross-compartmental inputs are normally lost from the medial compartment of LG (LGm) by the 8th postnatal day. To investigate the mechanisms involved in the elimination of cross-compartmental inputs, muscle fibers in the LGm compartment were denervated by cutting the LGm nerve branch in 1-4 day old rat pups and in adult rats. We then assessed the degree of cross-compartmental innervation within the "denervated" compartment using intracellular recordings from neonatal muscle fibers or immunohistochemical staining for nerve cell adhesion molecule (N-CAM) and neurofilament protein in adult muscles. Following LGm axotomy in neonates, cross-compartmental innervation is more extensive than in controls and is present as late as 20 days after birth. Thus, in the absence of "native" LGm axons, neonatal cross-compartmental inputs proliferate by axonal sprouting and the formation of new synapses on vacant LGm fibers. In contrast, axotomized adults do not form new cross-compartmental inputs over the same time period. The differential response of neonates and adults to muscle nerve branch denervation is evidence for the existence of some form of compartment-specific recognition. We propose that compartmental identity either arises or becomes relatively more potent during ontogeny and normally acts selectively to eliminate foreign axons and deter the formation of new cross-compartmental inputs. 0 1993 Wiley-Liss, Inc.

The lateral thoracic nerve and the cutaneous maximus muscle—A novel in vivo model system for nerve degeneration and regeneration studies

“…3a–b). This observation, however, is in agreement with other observations in which sprouts fail to extend into denervated regions from fully innervated muscle (Gatesy and English, 1993). In addition, there was little if any sprouting across the dorsal midline after a unilateral transaction of the LTN (supplementary Fig.…”

Specificity and development of innervation pattern ofXenopus pectoralis muscle

“…This degree of compactness of innervation is much greater than has been reported in either frog ( Trussell and Grinnell, 1985) or mammalian muscle (Gates and Betz, 1993;Smits et al, 1994). Muscles with multiple tendons or broad insertions, such as the frog gluteus (Bennett and Lavidis,198 I ) and the mammalian intercostal (Dennis and Harris, 1980), gluteal (Brown and Booth, 1983;English, 1990), lateral gastrocnemius (Gatesy and English, 1993), and masseter muscles (Weijs et al, 1993 ), often show motor unit localization within smaller muscle compartments defined by the presence of different nerve branches. In the snake transversus abdominis, each segmental muscle often has only one or two fast twitch motor axons, plus a greater number of slow twitch and tonic fiber axons, innervating a total of about 100 muscle fibers.…”

“…This specificity mainly takes two forms: there is early preferential (but not exclusive) innervation of a consistent histochemical muscle fiber type (Thompson et al, 1984;madby and Jansen, 1990;Thompson et al, 1990;Betz et al, 1990;Nelson and Thompson, 1994); and a given pool of motoneurons projects selectively to a single appropriate muscle, or even muscle compartment, and the "erroneous" connections that are found outside this region early in development get eliminated during maturation ( Lance-Jones and Landmesser, 198 la,b;Brown and Booth, 1983;Bennett and Lavidis, 1984;Callaway et al, 1989;Bennett and Ho, 1988;English, 1990;Gatesy and English, 1993). Even after this refinement, however, motor units tend to be widely distributed across a muscle or muscle compartment, with extensive spatial overlap of motor units of the same physiological/ histochemical type.…”

Muscle moment arms and sensitivity analysis of a mouse hindlimb musculoskeletal model

“…; Arnold et al. ), as there is substantial evidence that different portions of a muscle can work heterogeneously to produce total muscle force (Gatesy & English, ). In cases where it was found that modelled muscles would pass through other anatomical landmarks (either bone, retinaculae or other muscles), either ‘via points’ or wrapping surfaces were used to constrain them to realistic paths of action (Fig.…”

“…GM was represented here by three separate muscles [GM (dorsal), GM (middle) and GM (ventral)], to account for its broad origin on the iliac crest, while M. biceps femoris posterior (BFP) was also represented by three muscles [BFP (cranial), BFP (middle) and BFP (caudal)] due to its broad insertion on the lateral aspect of the fibula and adjacent fascia. This is common in musculoskeletal modelling (Delp et al 1990;van der Helm et al 1992;Arnold et al 2010), as there is substantial evidence that different portions of a muscle can work heterogeneously to produce total muscle force (Gatesy & English, 1993). In cases where it was found that modelled muscles would pass through other anatomical landmarks (either bone, retinaculae or other muscles), either 'via points' or wrapping surfaces were used to constrain them to realistic paths of action ( Fig.…”