Cytology and immunocytochemistry of the nucleus extrolateralis anterior of the mormyrid brain: possible role of GABAergic synapses in temporal analysis

Abstract

Mormyrid fish use their electrosensory/electromotor system for both electrolocation and electrocommunication. One type of electroreceptor, the knollenorgan, has a low threshold and is used strictly for detecting a conspecific's electric organ discharge. Knollenorgan afferents terminate with mixed synapses (gap junctions and asymmetric chemical synapses) on neurons of the nucleus of the lateral line lobe (nLLL), which in turn projects to a midbrain nucleus--the nucleus extrolateralis anterior (ELa). ELa contains numerous granule cells, which are adendritic, and scattered larger neurons, here termed interstitial cells, which possess several branched dendrites. Because of the overall paucity of dendrites, the neuropil of ELa is scarcely developed and myelinated fibers predominate in between the cell bodies. Axons presumed to originate in nLLL make mixed synapses on both the interstitial and the granule cells. The interstitial neurons are immunoreactive for glutamic acid decarboxylase (GAD), the synthetic enzyme for the inhibitory neurotransmitter gamma-aminobutyric acid (GABA), while the granule cells are GAD-negative. Many GAD-positive synapses are found on each granule cell soma; at smaller densities, GAD-positive boutons also synapse on the cell bodies and dendrites of interstitial cells. The GAD-positive boutons have pleomorphic vesicles and make symmetric synapses. Such boutons presumably originate from a plexus of interstitial cell axons. Mormyrid fish use their knollenorgan afferents for precise temporal discriminations, and this information is needed for electrocommunication. The ELa, with its relatively simple neuronal circuitry, is the most likely site for precise temporal analysis in the knollenorgan afferent pathway, and we propose that the GABAergic synapses on the granule cells may be essential for accurate detection of specific time intervals.