Serotonin modulates the electric waveform of the gymnotiform electric fishBrachyhypopomus pinnicaudatus

Abstract

The gymnotiform electric fish Brachyhypopomus pinnicaudatus communicates with a sexually dimorphic electric waveform, the electric organ discharge (EOD). Males display pronounced circadian rhythms in the amplitude and duration of their EODs. Changes in the social environment influence the magnitudes of these circadian rhythms and also produce more transient responses in the EOD waveforms. Here we show that injections of serotonin produce quick, transient, dosedependent enhancements of the male EOD characters similar to those induced by encounters with another male. The response to serotonin administered peripherally begins 5-10·min post injection and lasts approximately 3·h. The magnitude of the response to serotonin is tightly associated with the magnitude of the day-to-night swing of the circadian rhythm prior to injection. Taken together these findings suggest that the male's social environment influences his response to serotonin by altering the function of some part of the downstream chain between the serotonin receptors and the ion channels involved in control of the EOD waveform. Although chronic activation of serotonin circuitry is widely known to elicit subordinate behavior, we find that 5-HT initially increases a dominance signal in these fish. These findings are consistent with the emerging view that serotonin facilitates different adaptive responses to acute and chronic social challenge and stress.

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

“…High 5-HT turnover in parts of the brain has been found in aggressive and dominant individuals (Korzan et al, 2000;Matter et al, 1998) and a "primed" serotonergic system may be necessary to enable an individual to produce an appropriate behavioral response in a complex social context (Sperry et al, 2005). These findings would help explain the apparent paradox we observed in our fish wherein 5-HT injections further masculinized the males' EODs (Stoddard et al, 2003). If the classical account of the serotonin system as an inhibitor of aggression is accurate and enhancements of the EOD in the presence of conspecifics are aggressive, then the reduction in EOD parameters following activation of the 5HT 1A R makes perfect sense, but the increase in these parameters following activation of the 5HT 2 R is unexpected.…”

“…Social encounters and environmental stimuli modulate the EOD waveform by altering the membrane biophysics and discharge waveforms of individual electrocytes (Ferrari et al, 1995;McAnelly and Zakon, 2000;Mills and Zakon, 1991), resulting in either a larger or smaller waveform. Social encounters modulate the EOD within minutes and large waveforms and/or rapid enhancements are associated with dominance status (Franchina et al, 2001;Hagedorn and Zelick, 1989;Stoddard et al, 2003).We have shown that intramuscular injections of 5-HT cause male B. pinnicaudatus to increase their EOD amplitude and duration akin to the waveform changes observed during male-male social interactions (Stoddard et al, 2003). These effects of 5-HT do not result from its direct action on the electrocytes, whereas melanocortin peptides do modulate the discharge waveforms of single electrocytes directly (Markham and Stoddard, 2005).…”

“…Ketanserin was dissolved at pH 6.7, titrated to pH 7.2 with NaOH, and diluted to a final concentration of 2.5 mM. Other pharmacological compounds were dissolved in physiological saline as described previously (Stoddard et al, 2003). …”

“…data). Thus we chose intramuscular injection, which had proven to be successful with serotonin (Stoddard et al, 2003). We prepared the injection solutions to produce the desired dose when injected intramuscularly at 1 μl g −1 body weight.…”

“…All injections were given midday (10:00-15:00) and EOD recording resumed immediately after fish were returned to the tank. Handling time from capture, through injection, to replacement in the tank was less than one minute, and produced little change in EOD waveform (Stoddard et al, 2003). The silent antagonist (i.e., ligand with no intrinsic effect) ketanserin is more useful for distinguishing which of the 5HT 2 receptor subtypes may be exerting an effect.…”