Anatomy and behavioral function of serotonin receptors in Drosophila melanogaster larvae

PLoS One. 2017 Aug 4;12(8):e0181865. doi: 10.1371/journal.pone.0181865. eCollection 2017.

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.

MeSH terms

  • Animals
  • Behavior, Animal / physiology*
  • Brain / metabolism
  • Drosophila melanogaster / anatomy & histology*
  • Drosophila melanogaster / physiology*
  • Female
  • Larva / anatomy & histology*
  • Larva / physiology*
  • Learning / physiology
  • Male
  • Memory / physiology
  • Receptors, Serotonin / metabolism*

Substances

  • Receptors, Serotonin

Grants and funding

This work was supported by the Deutsche Forschungsgemeinschaft (TH1584/ 1-1 and TH1584/3-1 to A.S.T), the Swiss National Science Foundation (31003A132812/1 to A.S.T.), the Baden Württemberg Stiftung (to A.S.T.), the Bioimaging Center and Zukunftkolleg of the University of Konstanz (to A.S.T.). A.H. is supported by the International Max Planck Research School for Organismal Biology. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.