The formation of synapses in amphibian striated muscle during development.

Abstract

SUMMARY1. A study has been made of the formation of synapses in developing reinnervated and cross-reinnervated amphibian twitch muscles which receive either a focal (iliofibularis) or a distributed (sartorius) innervation from 'en plaque' nerve terminals using histological, ultrastructural and electrophysiological techniques.2. During the development of the tadpole through metamorphosis to the adult frog, the sartorius myofibres increased in length at about twice the rate of the iliofibularis myofibres, due to a fast rate of growth at their insertions on to the pelvic tendon.3 5. Reinnervation or cross-reinnervation of the sartorius and the iliofibularis muscles in adults or at a late stage of development simply reconstituted the normal focal and distributed innervation patterns of the muscles, as found in the control muscles of the contralateral and unoperated legs.6. These observations on synapse formation in amphibia are consistent M. R. BENNETT AND A. G. PETTIGREW with the hypothesis that during development the axon making the initial synaptic contact on the muscle cells induces a property over a length of muscle membrane adjacent to this site which makes it refractory to synapse formation; thus during reinnervation or cross-reinnervation of adult muscles this refractory property constrains synapse formation to these sites.

Regulation of synaptic position, size, and strength in anuran skeletal muscle

“…There was a marked decrease in the percentage of singly innervated fibers with increasing muscle size, from approximately 25% in muscles having mean fiber lengths of 0.7 to 0.75 cm (from animals weighing about 10 gm) to under 5% in muscles having mean fiber lengths greater than 0.9 cm (from animals weighing 40 gm or more). Presumably this decrease in proportion of single innervated fibers is a growth-related phenomenon, similar to that reported by Bennett and Pettigrew (1975) in the frog sartorius.…”

“…This distribution is shown in Figure 5. Apparently there is some influence acting to ensure a minimum separation between these paired junctions, a conclusion reached by Bennett and Pettigrew (1975) in their study of synaptic spacing in the developing frog sartorius. It is noteworthy, also, that no junctions were found within 20% of either end of the fiber.…”

“…If there is a decline in the amount of growthpromoting factor available, for example, because a strong second terminal has appeared, reducing the overall level of synthesis of the substance and/or inactivating or depleting it, a long terminal might shrink. A mechanism of this sort could explain the dynamic equilibrium that appears to exist at normal frog junctions, characterized by both elongation and retraction of terminal branches as a function of seasonal or other factors (Bennett and Pettigrew, 1975;Wernig et al, 1980;Herrera and Grinnell, 1981).…”

“…Conversely, there is competition between active junctions on muscle fibers, resulting in synapse elimination during early postnatal development, and elimination of supernumerary synapses on adult fibers (see reviews by Lame and Jansen, 1980;Grinnell and Herrera, 1981). This competition can take place up to a few millimeters distance (implying interaction via the muscle fibers) but apparently not further away (Frank et al, 1975;Bennett and Pettigrew, 1975;Brown et al, 1976;Kuffler et al, 1977Kuffler et al, , 1980Grinnell et al, 1977Grinnell et al, , 1979Haimann et al, 1976Haimann et al, , 1981. On the basis of these findings, Jansen and his colleagues (Jansen et al, 1978;Kuffler-et al, 1980;Lomo and Jansen, 1980) have suggested that muscle fibers produce a substance that induces sprouting and synapse formation, the amount of which varies inversely with the level of muscle fiber activity.…”

“…It is well known that larger diameter muscle fibers -tend to have larger junctions (Co&s, 1955;Anzenbacher and Zenker, 1963;Kuno et al, 1971;Bennett and Pettigrew, 1975;Harris and Ribchester, 1979). However, synapses of equal size may differ sharply in quanta1 content or EPP size, and frequently short terminals are stronger than longer ones.…”