Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo.

The fast electrosensory pathway (FEP) of gymnotiform fish is mediated by tuberous electroreceptor organs innervated by ganglion cells that synapse with spherical cells of the electrosensory lateral line lobe (ELL). Spherical cells project to the magnocellular mesencephalic nucleus. The electrosensory environment was represented somatotopically within ELL. The mandibular (MN) and the supraorbital (SON) nerves projected to rostral ELL (occupying 19-28% and 4-10%, respectively), and the posterior branch of the anterior lateral line nerve (pALLN) projected to caudal ELL (occupying 56-64%). Labeling with horseradish peroxidase or biotinylated dextran-amine demonstrated three kinds of synaptic endings coupling primary afferents to spherical cells: multiple synaptic knobs, medium-sized calyxes, and very large calyxes. Multiple synaptic knobs arose from MN and SON primary afferents and were found in a narrow rostral area covering the centrolateral (CLS) and lateral (LS) segments of ELL. Medium and large calyxes, proceeding from the same nerves, predominated in the remaining parts of the three segments of ELL containing spherical cells. Calyx-type endings were also found in the LS-occupying regions in which the pALLNs projected. Calyx-type endings formed gap junctions but also contained vesicles and showed submembrane specializations typical of chemical synapses. The postsynaptic spherical cells were linked by dendrosomatic gap junctions and were also contacted by unlabeled en passant synaptic boutons, whose fine structure suggested chemical transmission. Electrophysiological studies indicated that spherical cell responsiveness diminished after electrosensory stimulation. This apparently inhibitory phenomenon may be subserved by the unlabeled synaptic boutons, which possibly originate from interneurons that have yet to be identified.