Distinctive mechanisms underlie the emission of social electric signals of submission in Gymnotus omarorum

Abstract

South American weakly electric fish (order Gymnotiformes) rely on a highly conserved and relatively fixed electromotor circuit to produce species-specific electric organ discharges (EOD) and a variety of meaningful adaptive EOD modulations. The command for each EOD arises from a medullary pacemaker nucleus composed by electrotonically coupled intrinsic pacemaker and bulbospinal projecting relay cells. During agonistic encounters Gymnotus omarorum signals submission by interrupting its EOD (offs) and by emitting transient high rate barrages of low amplitude discharges (chirps). Previous studies in gymnotiformes have shown that electric signal diversity is based on the segregation of descending synaptic inputs to pacemaker or relay cells and differential activation of the neurotransmitter receptors -for glutamate or γ-aminobutyric acid (GABA)- of these cells. Therefore, we tested whether GABAergic and glutamatergic inputs to pacemaker nucleus neurons are involved in the emission of submissive electric signals in G. omarorum. We found that GABA applied to pacemaker cells evokes EOD interruptions that closely resembled natural offs. Although in other species chirping is likely due to glutamatergic suprathreshold depolarization of relay cells, here, application of glutamate to these cells was unable to replicate the emission of this submissive signal. Nevertheless, chirp-like discharges were emitted after the enhancement of excitability of relay cells by blocking an IA-type potassium current and, in some cases, by application of vasotocin, a status-dependent modulator peptide of G. omarorum agonistic behavior. Modulation of electrophysiological properties of pacemaker nucleus neurons in gymnotiformes emerges as a novel putative mechanism, endowing electromotor networks with higher functional versatility.