Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons.

Mariana M Marquez,Maurice J Chacron

doi:10.3389/fnint.2020.00038

Abstract

Organisms must constantly adapt to changes in their environment to survive. It is thought that neuromodulators such as serotonin enable sensory neurons to better process input encountered during different behavioral contexts. Here, we investigated how serotonergic innervation affects neural and behavioral responses to behaviorally relevant envelope stimuli in the weakly electric fish species Apteronotus albifrons. Under baseline conditions, we found that exogenous serotonin application within the electrosensory lateral line lobe increased sensory neuron excitability, thereby promoting burst firing. We found that serotonin enhanced the responses to envelope stimuli of pyramidal cells within the lateral segment of the electrosensory lateral line lobe (ELL) by increasing sensitivity, with the increase more pronounced for stimuli with higher temporal frequencies (i.e., >0.2 Hz). Such increases in neural sensitivity were due to increased burst firing. At the organismal level, bilateral serotonin application within the ELL lateral segment enhanced behavioral responses to sensory input through increases in sensitivity. Similar to what was observed for neural responses, increases in behavioral sensitivity were more pronounced for higher (i.e., >0.2 Hz) temporal frequencies. Surprisingly, a comparison between our results and previous ones obtained in the closely related species A. leptorhynchus revealed that, while serotonin application gave rise to similar effects on neural excitability and responses to sensory input, serotonin application also gave rise to marked differences in behavior. Specifically, behavioral responses in A. leptorhynchus were increased primarily for lower (i.e., ≤0.2 Hz) rather than for higher temporal frequencies. Thus, our results strongly suggest that there are marked differences in how sensory neural responses are processed downstream to give rise to behavior across both species. This is even though previous results have shown that the behavioral responses of both species to envelope stimuli were identical when serotonin is not applied.

Highlights

Organisms must detect and perceive natural stimuli efficiently and adaptively to survive in ever-changing environments (Wark et al, 2007; Sharpee et al, 2014)
The situation appears to be qualitatively different when considering A. albifrons. This is because, contrary to A. leptorhynchus, male A. albifrons tend to have lower electric organ discharge (EOD) frequencies than females (Zakon and Dunlap, 1999) and because androgen treatment decreases EOD frequency (Dunlap et al, 1998). These results suggest that, in male A. albifrons, a lower EOD frequency is a signal of increased dominance
In the case of the serotonergic system, the remarkable conservation across vertebrate species suggests a common function (Parent, 1981). While this may be true in general, our results show that even when comparing two very closely related species such as A. leptorhynchus and A. albifrons, application of serotonin in the same brain area can give rise to opposite effects on behavioral responses

Summary

Introduction

Organisms must detect and perceive natural stimuli efficiently and adaptively to survive in ever-changing environments (Wark et al, 2007; Sharpee et al, 2014). We investigated how serotonin application affects neural and behavioral responses to sensory input in the weakly electric fish species Apteronotus albifrons using the same paradigms used previously by our group (Marquez and Chacron, 2020b) in the closely related species Apteronotus leptorhynchus. It has been shown that the tuning of ELL pyramidal cells to envelope stimuli is similar in both species Both A. leptorhynchus and A. albifrons display identical behavioral responses to envelope stimuli in that the animal’s EOD frequency follows the detailed timecourse of the envelope in an almost one-to-one fashion (Metzen and Chacron, 2014, 2015; Huang et al, 2016; Martinez et al, 2016; Thomas et al, 2018)

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