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 (EODs) and a variety of meaningful adaptive EOD modulations. The command for each EOD arises from a medullary pacemaker nucleus composed of electrotonically coupled intrinsic pacemaker and bulbospinal projecting relay cells. During agonistic encounters, Gymnotus omarorum signals submission by interrupting its EOD (offs) and 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 resemble natural offs. Although in other species chirping is probably 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 I A-type potassium current and, in some cases, by application of vasotocin, a status-dependent modulator peptide of G. omarorum agonistic behavior. Modulation of the electrophysiological properties of pacemaker nucleus neurons in Gymnotiformes emerges as a novel putative mechanism endowing electromotor networks with higher functional versatility.

Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

“…Local AVT application to the PN evoked immediate small amplitude chirp‐like discharges (Figure b; Comas et al, ). When applied near R‐cells, AVT evoked bursts of high rate discharges, but when applied near the PM‐cells, it caused chirp‐like discharges with a longer delay (Comas et al, ). Given that AVT fibers actually reach the proximity of the electromotor CPG (Perrone et al, ; Pouso, Radmilovich, & Silva, ), these observations suggest that AVT acts as a direct modulator of R‐cell excitability during contests.…”

“…In contrast, chirping activity in subordinate G. omarorum can be evoked by the enhancement of R‐cell excitability by the blockade of an I A ‐type potassium current but not by glutamate administration (Figure fourth row; Comas et al, ). This bursting activity is likely to be initially driven by the passive depolarization of R‐cells in response to PM‐cell‐sustained depolarization (Comas et al, ).…”

“…The EOD maintains its regular rate. The peak of the regular full EODs is truncated at 10% (modified from Comas et al, )…”

Glutamatergic Control Of A Pattern-Generating Central Nucleus In A Gymnotiform Fish

“…EOD modulations observed during specific adaptive and social behaviors constitute accessible, prominent, and distinctive electromotor behaviors. These depend on the activation of specific descending inputs to the PN, that arise from distinct prepacemaker nuclei (PPn; Caputi et al 2005; Comas and Borde 2010; Comas et al 2019). More recently, hormonal and peptidergic influences upon the electromotor system have also been characterized (reviewed in Silva 2019).…”

“…A wealth of previous studies (Caputi et al 2005; Kawasaki and Heiligenberg 1989, 1990; Lorenzo et al 2006; Quintana et al 2011, 2014; Spiro 1997) show that distinct types of short term rate EOD modulations depend not only on the specific PPn being activated, but also on both the cellular target of PPn axons within the PN and the neurotransmitter receptors involved (Caputi et al 2005; Curti et al 1999; Dye et al 1989; Kawasaki and Heiligenberg 1989, 1990; Keller et al 1991; Quintana et al 2011, 2014). More recently, the modulation of electrophysiological properties of PN neurons has emerged as a novel putative mechanism, endowing electromotor networks with higher functional versatility (Comas et al 2019). Activation of GABAergic inputs to PM-cells induce them to silence their discharge provoking EOD interruptions (Comas et al 2019; Kawasaki and Heiligenberg 1989, 1990).…”