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

Abstract

An analysis of the physiology, morphology, and position of endplates on identified fibers in the Xenopus laevis pectoralis muscle has revealed the following. 1. The percentage of fibers with one endplate is lower in large muscles, and within the same muscle, singly innervated fibers are smaller than dually innervated fibers.2. Single junctions tend to be stronger than junctions on dually innervated fibers. 3. Single junctions typically are located near the middle of their fibers, while the endplates on dually innervated fibers are located toward either end and usually are separated by at least 20% of the total fiber length. A significant proportion of dually innervated fibers appears to be innervated by the same axon at both junctions.4. Junctions on the same dually innervated fiber tend to be more similar in length than do junctions on different fibers of the same input resistance. This observation is the same whether both junctions on a given fiber are formed by the same or different axons. There is no corresponding tendency for greater similarity in physiological strength of paired junctions, which frequently show large differences in endplate potential amplitude.5. The total terminal length on dually innervated fibers of equivalent input resistance is inversely correlated with the mean release per unit length and total release of both junctions. There is no apparent correlation between the distance separating endplates and their strength or length.The data support a model of synaptic regulation in which nerve terminals are attracted, grow, and are maintained in proportion to the amount of a substance supplied by muscle fibers. Our findings suggest that such a substance is produced or distributed uniformly throughout each fiber in amounts proportional to the fiber size and inversely proportional to the total transmitter output of all junctions innervating the fiber. A form of competitive interaction between the terminals which helps to determine synaptic spacing may involve local depletion or inactivation of this substance.

Precision of Reinnervation and Synaptic Remodeling Observed in Neuromuscular Junctions of Living Frogs

“…These findings are consistent with the view that there is ongoing competition between terminals at doubly innervated junctions, even in the absence of synapse elimination. Our results also are consistent with earlier findings that junctions on dually innervated fibers in frogs are substantially weaker and smaller than junctions on singly innervated fibers, both in intact muscles (Haimann et al, 1981a;Nudell and Grinnell, 1983) and reinnervated muscles (Grinnell et al, 1979;Haimann et al, 1981b).…”

Synaptic strength as a function of motor unit size in the normal frog sartorius.

“…Besides the properties noted in the present work, the only obvious intrinsic differences between adult frog motoneurones seems to be in size and in conduction velocity, the latter increasing significantly with motor unit size (Luff& Proske, 1976;Ridge & Thomson, 1980a). It is not clear, however, whether axonal diameter is an intrinsic neuronal feature determining the number of terminal branches and motor unit size, or rather a response to some peripheral advantage over other axons and consequently more trophic feed-back from muscles of a substance analogous to nerve growth factor (Brown, Jansen & Van Essen, 1976;Hollyday & Hamburger, 1976;Betz, Caldwell & Ribchester, 1980;Oppenheim, 1981 (Grinnell, Letinsky & Rheuben, 1979 Nudell & Grinnell, 1983). Many other instances of competitive interaction between terminals on multiply innervated amphibian fibres have been reported (Dennis & Yip, 1978;Wigston, 1980;Bennett, McGrath & Davey, 1979; see reviews by Mark, 1980; In contrast to the sartorius, the fibres of the cutaneous pectoris muscle each have only one end-plate site.…”

Apportionment of the terminals from single preganglionic axons to target neurones in the rabbit ciliary ganglion.

“…Similarly, the diminished density of synaptic contacts on the cell bodies of neurones innervated by several different axons may reflect competition. These phenomena seem likely to be the neuronal analogue of observations in muscle which show that individual synaptic responses in multiply innervated fibres are smaller than responses in singly innervated fibres, and that multiple end plates observe a minimum separation from one another (Haimann, Mallart & Zilber-Gachelin, 1976;AngautPetit & Mallart, 1979;Haimann, Mallart, Tomas i Ferre & Zilber-Gachelin, 1981 a, b;Yao & Weakly, 1981;Nudell & Grinell, 1983).…”