Dye coupling without gap junctions suggests excitatory connections of gamma-aminobutyric acidergic neurons.

Abstract

After injections of the low-molecular-weight tracer neurobiotin into the preeminential nucleus of the brain of the mormyrid fish Gnathonemus petersii, we observed that retrogradely labeled, large fusiform projection neurons (LFd cells) of the deep granular layer of the electrosensory lobe (ELL) were surrounded by 30-50 labeled satellite granular cells. More superficially located projection cells, including large fusiform cells in the superficial granular layer (LFs) and large ganglionic (LG) cells in the ganglionic layer, were never surrounded by labeled satellites. LFd-satellite cells have a small soma (diameter 5-8 microm), a few small dendrites, and an apical axon that terminates in the plexiform and ganglionic layers of the ELL. They contact LFd projection neurons with dendrodendritic, dendrosomatic, and somatodendritic puncta adhaerentia-like appositions, designated here as "neurapses." In the electron microscope, these contacts resemble synapses without presynaptic vesicles. Because no gap junctions were found between LFd and satellite granule cells, we suggest that the neurapses allow the passage of neurobiotin, though not biocytin or biotinylated dextran amine. These contacts may provide the intermediate substrate for the postulated, but so far unknown, excitatory connection between primary afferent input and LFd projection neurons, via gamma-aminobutyric acid (GABA)-ergic granular cells. We suggest that certain puncta adhaerentia-like contacts might not be only adhesive structures and that LFd-satellite granular cells might both excite LFd projection cells via neuraptic contacts of their dendrites and cell bodies and inhibit more superficial LF and LG cells via their GABAergic axonal synapses. Our results suggest that puncta adhaerentia-like contacts could be responsible in some cases for the electrical coupling found electrophysiologically in local inhibitory circuits.