Cellular mechanisms of developmental and sex differences in the rapid hormonal modulation of a social communication signal

Abstract

Some gymnotiform electric fish species rapidly modify their electric signal waveforms by altering the action potential (AP) waveforms of their electrocytes, the excitable cells that produce the electric organ discharge (EOD). The fish Brachyhypopomus gauderio alters EOD amplitude and pulse duration as a social signal in accordance with the prevailing social conditions, under the dual regulation of melanocortins and androgens. We show here that B. gauderio uses two distinct cellular mechanisms to change signal amplitude, and its use of these two mechanisms varies with age and sex of the signaler. EOD amplitude and waveform are regulated by the coordinated timing and shaping of two APs generated from two opposing excitable membranes in each electrocyte. The two membranes fire in sequence within 100 μs of each other with the second AP being broader than the first. We have shown previously that mature males increase EOD amplitude and duration when melanocortin peptide hormones act directly on electrocytes to selectively broaden the second AP and increase the delay between the two APs by approximately 25 μs. Here we show that females selectively broaden only the second AP as males do, but increase amplitude of both APs with no change in delay between them, a previously unreported second mechanism of EOD amplitude change in B. gauderio. Juvenile fish broaden both APs and increase the delay between the APs. Cellular mechanisms of EOD plasticity are therefore shaped during development, presumably by sex steroids, becoming sexually dimorphic at maturity.