Plasticity in the startle-escape response of the African cichlid fish, Astatotilapia burtoni
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Ecological context, sensory inputs, and the internal physiological state are integrated for an animal to make appropriate behavioral decisions. However, these factors have rarely been studied in the same system. In the African cichlid fish Astatotilapia burtoni, males alternate between four phenotypes. Two are determined by social status and two are identified by the principle body coloration (yellow or blue). When socially dominant (DOM), fish display bright body coloration and a wealth of aggressive and reproductive behaviors. Subordinate (SUB) males decrease predation risk by adopting cryptic coloration and schooling behavior. Yellow males are more conspicuous than blue males, and DOMs and more conspicuous than SUBs, which means that yellow DOMs are most likely to be seen by predators. We therefore hypothesized that DOMs, yellow DOMs in particular, would show enhanced startle-escape responsiveness to compensate for their increased predation risk. Indeed, behavioral responses to sound clicks of various intensities showed a significantly higher mean startle rate in DOMs than SUBs. When testing the same males after social change, yellow DOMs respond at a higher rate than yellow SUBs but blue males do not show plasticity. Electrophysiological recordings from the Mauthner cells (Mcells), the neurons triggering startle, were performed in anesthetized animals and showed larger synaptic responses to sound clicks in DOMs, consistent with the behavioral results. In addition, the inhibitory drive mediated by interneurons presynaptic to the M-cell was significantly reduced in DOMs. Using behavioral tests, intracellular recordings, and single-cell molecular analysis, immunohistochemistry and in-situ hybridization, I show here that serotonin modulates this socially regulated plasticity via the 5-HT receptor subtype 2 (HTR2A). Specifically, SUBs display increased sensitivity to pharmacological blockade of HTR2A compared with DOMs in both startle-escape behavior and electrophysiological properties of the M-cell. These receptors, however, are not expressed in the Mauthner neurons, but in the inhibitory interneurons that regulate the Mcell’s membrane properties. I show a role for 5-HT in modulating startle plasticity and increase our understanding of the neural basis of behavioral plasticity. More broadly, this study provides an integrative explanation of an ecological and social trade-off at the level of an identifiable decision-making neural circuit.