Selective elimination of cross-compartmental innervation in rat lateral gastrocnemius muscle

Abstract

The calf muscles of the rat hindlimb are composed of smaller entities, called neuromuscular compartments, which are the territories of muscle innervated by a single, naturally occurring primary (first-order) muscle nerve branch. While it is quite clear that a precise connectivity exists very early in development between motoneuron pools and individual muscles, the mechanisms responsible for producing the adult pattern of compartmental innervation are unknown. This study uses intracellular recording techniques to demonstrate that neuromuscular compartments are essentially established at birth and that postnatal synapse elimination has little role in establishing neuromuscular compartments. Our results demonstrate the existence of a small number of cross-compartmental connections in neonates which are not present in adults. Examining the removal of these cross-compartmental connections in both normal muscles and in muscles that have had synapse elimination delayed by tenotomy reveals that the synapses responsible for this innervation are eliminated in a selective manner.

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

“…The remaining three unoperated limbs in our sample had no cross-compartmental inputs. These results correspond to the general pattern of cross-compartmental input elimination characterized by Donahue and English (1989). During normal development, fibers with cross-compartmental inputs are a minor component of the LGm during the 1st postnatal week (Fig.…”

“…Control LGm muscles show a higher percentage of cross-compartmental inputs distally during the 1st postnatal week (Donahue and English, 1989); a similar distribution is found in experimental muscles after the LGm nerve branch is cut. If the cut LGm axons were to reinnervate the LGm, it seems highly unlikely that their pattern of synapse formation would resemble the distribution of normal cross-compartmental axons.…”

“…2). In this period, an average of 8.3% of LGm fibers are innervated by axons from other primary nerve branches (Donahue and English, 1989). The number of cross-compartmental inputs decreases until W LGm Denervated P1 4 2 3 4 5 6 7 8 9 10 11 12…”

“…Crosscompartmental inputs are more common and found at older ages in muscles after LGm axotomy. Data for control and unoperated muscles are from Donahue and English (1989). they are almost completely lost by the 8th postnatal day (PSI. After combining the data for non-axotomized rats from the previous study with the present one, only two LGm fibers out of 462 (0.4%) received cross-compartmental inputs after P7.…”

“…The rat lateral gastrocnemius muscle (LG) is composed of four discrete subregions called neuromuscular compartments (Donahue and English, 1989). In the adult rat, each compartment is an independent, nonoverlapping motor unit territory exclusively innervated by a primary branch of the LG nerve ( Fig.…”