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

Abstract

Serotonin (5-HT) is an indirect modulator of the electric organ discharge (EOD) in the weakly electric gymnotiform fish, Brachyhypopomus pinnicaudatus. Injections of 5-HT enhance EOD waveform "masculinity", increasing both waveform amplitude and the duration of the second phase. This study investigated the pharmacological identity of 5-HT receptors that regulate the electric waveform and their effects on EOD amplitude and duration. We present evidence that two sets of serotonin receptors modulate the EOD in opposite directions. We found that the 5HT 1A R agonist 8-OH-DPAT diminishes EOD duration and amplitude while the 5HT 1A R antagonist WAY100635 increases these parameters. In contrast, the 5HT 2 R agonist α-Me-5-HT increases EOD amplitude but not duration, yet 5-HT-induced increases in EOD duration can be inhibited by blocking 5HT 2A/2C -like receptors with ketanserin. These results show that 5-HT exerts bi-directional control of EOD modulations in B. pinnicaudatus via action at receptors similar to mammalian 5HT 1A and 5HT 2 receptors. The discordant amplitude and duration response suggests separate mechanisms for modulating these waveform parameters. KeywordsSerotonin; Electric organ discharge; Communication signal; 5HT 1A receptor; 5HT 2 receptor; Social interaction; Dominance hierarchy Serotonin (5-HT) is a neuromodulator so ubiquitous that hardly any physiological function or behavior is free from its direct or indirect effects. As a result, a full account of neuroendocrine control of behavior requires a thorough assessment of 5-HT's function across a wide range of circumstances, even as the pervasive presence of 5-HT in the nervous system complicates unambiguous assessment of its functions. Particularly, serotonin is involved in the regulation of diametrically opposed behaviors, aggression and subordinance (Summers and Winberg, 2006). Serotonin activity rises in both dominant and subordinate males but rapidly returns to baseline in dominants while it stays chronically high in subordinates (Overli et al., 1999;Summers and Winberg, 2006). Prior social defeat or success during aggressive interactions affects future aggressive behaviors and the activity of the serotonergic system (Winberg et al., 1992;Winberg et al., 1997b). Furthermore, social experience affects the regulatory effect of serotonin on dominant behaviors via serotonin receptors 1A and 2A (Yeh et al., 1996). Pharmaceutical 5HT 1A agonists inhibit aggression or induce submissive behaviors in a wide range of non-mammalian vertebrates including green anoles (Deckel and Fuqua, 1998), Arctic charr (Hoglund et al., 2002;Winberg and Nilsson, 1993) Bell et al., 2007). In addition, 5HT 1A receptors operate as both postsynaptic receptors and as pre-synaptic autoreceptors to either suppress or stimulate stress responses in teleosts as they do in mammals (Hoglund et al., 2002). Despite the functionally and anatomically conserved nature of the serotonin system in vertebrates (Parent et al., 1984) and the abundance of data indicating a role for 5HT ...

Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression

“…Our data suggest an important excitatory function for AVT in both species (even stronger in G. omarorum, as discussed above), but provide no evidence that 5-HT modulates EOD rate. Previous studies in both species evaluating the effects of the activation of the 5-HT system on locomotor and electric behaviors did not report 5-HT actions on EOD rate in Brachyhypopomus (Allee et al, 2008), whereas pharmacologically increased levels of 5-HT evoked a decrease in EOD rate in Gymnotus (Capurro et al, 1997).…”

“…Pharmacological stimulation of the 5HT 1A receptors in B. gauderio did not affect contest outcome (seven out of eight injected residents won the contest), aggression levels or motivation towards combat (Fig.3). Previous reports in B. gauderio showed that 8-OH-DPAT diminishes amplitude and duration of the EOD waveform (Allee et al, 2008), which is an important proxy of male body size and endocrine status (Gavassa et al, 2011). The lack of effect of the 5-HT 1A agonist in B. gauderio is relevant because this is the first species in which the administration of 5-HT 1A receptor agonists (A)Behavioral protocol: dyads of G. omarorum (0-50% weight asymmetry, N=33) were placed in equal-sized compartments separated by a glass gate that was removed 10min after sunset.…”

“…In several species in which the serotonergic system has been analyzed during agonistic interactions, serotonergic activity increases consistently in subordinates (Yodyingyuad et al, 1985;Blanchard et al, 1991;Summers and Greenberg, 1995;Overli et al, 1999;Summers et al, 2005b) and decreases or remains unchanged in dominants (van Erp and Miczek, 2000;Ferrari et al, 2003;Summers et al, 2003). The activation of 5-HT 1A receptors has been involved in the inhibitory effect of 5-HT on aggression in all vertebrate classes (Deckel and Fuqua, 1998;Sperry et al, 2003;Miczek and Fish, 2006;Clotfelter et al, 2007;Allee et al, 2008;Ten Eyck, 2008). In addition, the 5-HT deficiency hypothesis was formulated based on the correlation between low levels of the 5-HT metabolite 5-hydroxyindoleacetic acid and aggressive or violent behavior in humans and other primates (Krakowski, 2003).…”

Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish

“…Earlier behavioural studies have shown that systemic application of 5-HT decreases aggressive behaviours in weakly electric fish and affects the waveform of the EOD in certain species (Maler and Ellis, 1987;Allee et al, 2008;Smith and Combs, 2008;Stoddard et al, 2006), but we do not yet know under which conditions intrinsic 5-…”

Social and Environmental Regulation of Signal Plasticity and Signal Reliability in the Electric Fish Brachyhypopomus gauderio

“…The hormonal drivers of EOD plasticity have been identified as androgen driving long-term changes , and peptide hormones driving mid-term changes, with serotonin acting centrally Allee et al, 2008) and melanocortins acting directly on the electrocyte ). However, a prior lab study failed to correlate endogenous circulating androgen levels and EOD parameters ).…”