Serotonergic neurons of the raphe nuclei of vertebrates project to most regions of the brain and are known to significantly affect sensory processing. The sub-second dynamics of sensory modulation of serotonin levels and its relation to behavior, however, remain unknown. We used fast-scan cyclic voltammetry to measure serotonin release in the electrosensory system of weakly electric fish, Apteronotus leptorhynchus. These fish use an electric organ to generate a quasi-sinusoidal electric field for communicating with conspecifics. In response to conspecific signals, they frequently produce signal modulations called chirps. We measured changes in serotonin concentration in the hindbrain electrosensory lobe (ELL) with a resolution of 0.1 s concurrently with chirping behavior evoked by mimics of conspecific electric signals. We show that serotonin release can occur phase-locked to stimulus onset as well as spontaneously in the ELL region responsible for processing these signals. Intense auditory stimuli, on the other hand, do not modulate serotonin levels in this region suggesting modality specificity. We found no significant correlation between serotonin release and chirp production on a trial-by-trial basis. However, on average, in the trials where the fish chirped, there was a reduction in serotonin release in response to stimuli mimicking similar-sized same-sex conspecifics. We hypothesize that the serotonergic system is part of an intricate sensory-motor loop: serotonin release in a sensory area is triggered by sensory input, giving rise to motor output, which can in turn affect serotonin release at the time-scale of the ongoing sensory experience and in a context-dependent manner.
Significance Statement: Serotonin is a key modulator of neural activity throughout the brains of all vertebrates. Understanding the function of serotonin in sensory processing is critical as its disruption in sensory perception is an important element of many neurological disorders. We studied the temporal dynamics of serotonin release in response to communication signals in weakly electric fish. We found that serotonin release is temporally tightly linked to communication stimuli and likely depends on an individual’s past experience. Interestingly, a fish's own communication behavior can also affect the time-course of serotonin release. Our results are the first to shed light on the sub-second dynamics of serotonin in a sensory area and its relation to ongoing behavior.
Authors report no conflict of interest.
This project was supported by NSERC postdoctoral fellowship to HF, CIHR 6027 and CIHR 49510 grants to LM, NSERC 293306 and Fonds de Recherche du Québec - Nature et Technologies 145726 to RK, and R01 DA022340 grant to JFC.
↵*Joint senior authors.