Effect of precocious and delayed afferent arrival on synapse localization on the amphibian mauthner cell

Abstract

Afferents often form synapses on restricted regions of their target cells. The connections between vestibular axons and the Mauthner cell are an example of this sort of specificity. The Mauthner cells are a pair of identifiable central neurons in certain fish and amphibians. In the axolotl (Ambystoma mexicanum), the large vestibular axons form club endings on only one portion of one dendrite of the Mauthner cell. During development, this specific distribution might result from nothing more than when and where the growing axons and dendrite meet (spatiotemporal model). Alternatively, the distribution might reflect constraints on where the developing axons may grow (axon segregation model) or form synapses (active recognition model). As a test of the spatiotemporal model, ears and vestibular ganglia from older embryos (Harrison stage 33/34-) were unilaterally grafted in place of prospective ear/ganglion placodes of younger embryos (stage 23). Light and electron microscopic examination revealed that the axons precociously entered the brain and formed synapses on the Mauthner cell. Similarly, grafts from younger to older embryos resulted in a delay. In both situations, mapping the club endings on the mature Mauthner cells of 21-mm larvae revealed a distribution similar to that of the contralateral control cells. Thus precocious and delayed afferent arrival did not alter the eventual localization of the synapses. These results conflict with the spatiotemporal model and imply that the vestibular axons are either restricted to a certain region of the neuropil or capable of recognizing a specific region of the Mauthner cell surface.