SYNAPTIC SITE SPECIFICITY: THE PATHS AND TERMINAL DISTRIBUTIONS OF SURGICALLY DISPLACED AFFERENTS IN THE AMPHIBIAN MAUTHNER CELL SYSTEM (DEVELOPMENTAL BIOLOGY, AXOLOTL, NEURONAL SPECIFICITY)

Abstract

In the axolotl (Ambystoma mexicanum) a single pair of large identified neurons called Mauthner cells (M-cells) are located in the medulla at the level of the ear. The entire ipsilateral vestibular input (nVIII) to the M-cell is localized on the ventral surface and branches of its proximal lateral dendrite, while the ipsilateral lateral line input (nVII) terminates on the distal portions: nVIII and nVII terminals are identifiable as club endings in both the light and electron microscopes (LM and EM, respectively). Prior to nVIII and nVII ingrowth, prospective ears and nVIII and nVII ganglia were unilaterally transplanted up to 450(mu)m rostral or caudal to their normal site. The contralateral side served as a control. LM analysis of 21(mu)m larvae revealed anatomically normal brains and M-cells. Hair cells in the transplanted ears were innervated by fibers originating in translocated ganglia; the central nerve roots from these ganglia entered the brain at anomalous positions along the anteroposterior axis. EM analysis demonstrated club endings on the M-cells from the operated sides; the distribution of club terminals was the same as that of control cells.;Horseradish peroxidase (HRP)-labeling of a control nVIII in a 21mm feeding larva revealed a discrete rostrocaudally oriented tract in the ventrolateral white matter. Labeling of a control nVII demonstrated three anteroposterior running tracts in the dorsolateral neuropil. Rostrally and caudally translocated nVIII and nVII were labeled with HRP when the animals reached 21mm larval stages. Labeled fibers entered the brain at ectopic sites, but coursed in tracts indistinguishable from those of controls. HRP-filled synapses on the M-cell could be visualized in the LM and EM: they were confined to their usual nVIII and nVIIl termination zones. Thus, displaced nVIII and nVII axons enter the brain at ectopic locations, course rostrocaudally in characteristic tracts and synapse on appropriate target regions of the ipsilateral M-cell. These data are consistent with a recognition or axonal segregation model, but are inconsistent with a hypothesis that proposes a spatio-temporal mechanism as being sufficient to explain the ontogeny of highly ordered neuronal connections. Axon growth paths are restricted and may organize connectivity patterns by limiting the access of afferents to particular targets.