Morphological correlates of electrotonic coupling in the magnocellular mesencephalic nucleus of the weakly electric fish Gymnotus carapo.

Abstract

The magnocellular mesencephalic nucleus (MMN) of Gymnotus carapo was studied by electron microscopy. This particular nucleus, characteristic of weakly electric fish, contains two principal classes of neuron. (1) Large neurons (25-35 mum): these are rounded unipolar cells, with the perikaryon partially covered by a sheath of compact myelin. The axon leaves the neuron as a short thick unmyelinated process not resembling the initial segment of multipolar neurons. The axon branches profusely and becomes myelinated very close to its origin. The perikaryal surface not covered by the myelin sheath receives abundant club endings. The synaptic interface between club endings and large neurons is characterized by alternating gap junctions and attachment plaques. In addition, at the periphery of the club endings, "active" zones are generally present, and this synapse is therefore a "mixed" synapse. (2) Small neurons (5-12 mum): these are uni- or bipolar cells, scattered throughout the nucleus, and occasionally, grouped in small clusters. Gap junctions were not observed between neuronal perikarya in such clusters. The synaptic investment of small neurons is formed by long cup endings which almost completely encircle the perikarya. The synaptic interface between cup endings and the perikarya of small neurons is characterized by large areas of gap junctions. A single cup ending establishing gap junctions with two small neurons within the plane of the section was frequently observed and this arrangement provides a morphological basis for electrotonic coupling between small neurons by way of presynaptic fibres. In the neuropil of the MMN, there are abundant synaptic islands constituted by a large axon terminal in synaptic contact with small unidentified profiles; both synaptic elements are surrounded by numerous thin glial lamellae. At the synaptic interface, in the islands, both gap junctions and "active" zones are present. The synaptic islands must also be considered as "mixed" synapses. The morphological results presented here correlate with electrophysiological data (Szabo et al., 1975). The very short delay (0.8-1.3 ms) of the MMS response to the fish's own electric organ discharge can only be explained by the existence of electrotonic transmission along the neuronal chain of the electrosensory pathway. The presence of gap junctions between club endings and large neurons provides a morphological basis for electrotonic transmission at the mesencephalic level of the electrosensory pathway.