Abstract
The biogenic amine serotonin (5-HT) is an important neuroactive molecule in the central nervous system of the majority of animal phyla. 5-HT binds to specific G protein-coupled and ligand-gated ion receptors to regulate particular aspects of animal behavior. In Drosophila, as in many other insects this includes the regulation of locomotion and feeding. Due to its genetic amenability and neuronal simplicity the Drosophila larva has turned into a useful model for studying the anatomical and molecular basis of chemosensory behaviors. This is particularly true for the olfactory system, which is mostly described down to the synaptic level over the first three orders of neuronal information processing. Here we focus on the 5-HT receptor system of the Drosophila larva. In a bipartite approach consisting of anatomical and behavioral experiments we describe the distribution and the implications of individual 5-HT receptors on naïve and acquired chemosensory behaviors. Our data suggest that 5-HT1A, 5-HT1B, and 5-HT7 are dispensable for larval naïve olfactory and gustatory choice behaviors as well as for appetitive and aversive associative olfactory learning and memory. In contrast, we show that 5-HT/5-HT2A signaling throughout development, but not as an acute neuronal function, affects associative olfactory learning and memory using high salt concentration as a negative unconditioned stimulus. These findings describe for the first time an involvement of 5-HT signaling in learning and memory in Drosophila larvae. In the longer run these results may uncover developmental, 5-HT dependent principles related to reinforcement processing possibly shared with adult Drosophila and other insects.
Highlights
The biogenic amine serotonin (5-HT) exerts an essential role in a wide range of insect behaviors by its action as neurotransmitter, neuromodulator, and/or neurohormone
To clearly disentangle 5HT2A-Gal4 dependent expression from marker expression we crossed 5-HT2A-Gal4 with UAS-myr::tomato and labelled Gal4 positive cells via an anti-DsRed antibody [65]. This is necessary as the enhancer trap piggyBac construct carries a “3xP3-EYFP” marker that is recognized by the anti-GFP antibody [50, 66, 67]
The “3xP3-EYFP” marker is expressed under the control of the endogenous Pax6 gene and on its own drives expression in the larval visual system and brain [68, 69]
Summary
The biogenic amine serotonin (5-HT) exerts an essential role in a wide range of insect behaviors by its action as neurotransmitter, neuromodulator, and/or neurohormone (reviewed by [1]). For the adult fruit fly Drosophila melanogaster it was shown that 5-HT signaling is involved in chemosensation [2, 3], aggression [4, 5], mating [6], feeding [7, 8], and locomotion [7, 9]. 5-HT acts as natural ligand for a group of G protein-coupled receptors and ligand-gated ion channels found in the central and peripheral nervous systems [10,11,12]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
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