The effect of transsynaptic stimulation on the dendritic branching pattern of the amphibian Mauthner cell

Abstract

Mauthner cells (M-cells) occur as a pair of large, identifiable neurons at ear level in the medulla of premetamorphic amphibians. Each receives synapses from the ipsilateral vestibular nerve (nVIII); these morphologically distinctive terminals, or club endings, are confined to the proximoventral surface and branches of the M-cell lateral dendrite. I have superinnervated this portion of the M-cell to examine the extent to which forming afferent contacts regulate the growth and branching of the lateral dendrite. Superinnervation was brought about in axolotl (Ambystoma mexicanum) embryos by unilaterally implanting an extra vestibular primordium rostral to the in situ one. The contralateral side served as control. When the larvae reached 21 mm, the ectopic nerve was labeled with HRP. Microscopic analysis revealed that labeled axons entered the medulla at the level of nV, coursed caudad toward the ipsilateral M-cell, and formed club endings on the appropriate region of the lateral dendrite. The number of club endings on experimental cells was greater than on controls. Examination of reconstructed M-cells revealed that the extra innervation on experimental cells produced a localized enhancement of dendritic branching. The data show that ingrowing axons stimulate dendritic growth and thus regulate the development of a normal dendritic pattern on target neurons. I also studied the response of the M-cell to deafferentation in the presence or absence of regenerated afferent contacts. Following the unilateral severence of nVIII in a group of axolotl larvae, the nerve was allowed to regenerate in half. In the remaining larvae, nVIII ganglion cells were removed to prevent regeneration. Reconstructions revealed that the extent of branching on M-cells receiving regenerated synapses was like controls, whereas branching on deprived cells was reduced. Some of the dendritic branches on M-cells receiving regenerated fibers were displaced: they extended into nerve tracts adjacent to the nVRI tract. EM analysis showed that the displaced branches received club endings. Regenerated axons, therefore, were not always confined to the nVIII tract. Deafferentation results in a reduction of dendritic branches; restoration of the branches occurs only when nVRI terminals reestablish contact on the M-cell. The data indicate that regenerating fibers stimulate dendritic growth, even in ectopic regions of neuropil.