Position- and fibre type-dependent selectivity by regenerating motor axons in reformation of the topographical projection to the glutaeus muscle in the adult toad (Bufo marinus)

Abstract

The toad glutaeus magnus muscle receives a topographical innervation dependent on the rostrocaudal origins of glutaeus motor axons on the spinal cord. The same projection is re-established in adult animals after cutting the glutaeus muscle nerve and allowing regenerating axons to reinnervate the muscle (Brown and Everett (1990) J. Comp. Neurol. 292:363-372). To determine whether the topographically selective reinnervation of the glutaeus muscle comes about because of genuine positional qualities associated with the pre- and post-synaptic tissues, we undertook two different experimental procedures: first, the nerve supply to the muscle was cut and redirected to ensure that regenerating axons entered the muscle via entirely novel pathways; and second, the triceps femoris nerve was cut so that the glutaeus muscle was reinnervated from a large pool of motor axons which were mostly foreign but segmentally appropriate. The motor projection to the muscle was determined by the glycogen depletion procedure; single glutaeus motor axons were repetitively stimulated in vitro to deplete muscle fibres of their stores of glycogen. The spatial location of fibres belonging to single motor units could then be determined by staining sections of the muscle histochemically for glycogen. A similar to normal projection was re-established after both experiments in that rostrally located motor axons innervated mostly the ventral portion of the muscle and caudal axons mostly the dorsal portion of the muscle. "Intermediate" axons synapsed predominantly with fibres in the middle of the muscle. Furthermore, the arrangement of fibre types in the muscle could not fully account for the reformation of the topographical projection by a type matching mechanism, although a secondary role for fibre types in the subsequent refinement of the projection was clearly suggested by our findings. Our results provide evidence for a distinction between at least two determinants that influence the reinnervation of muscle: positional cues and fibre types, with the former taking precedence over the latter.