Presynaptic gain control drives sweet and bitter taste integration in Drosophila

Curr Biol. 2014 Sep 8;24(17):1978-84. doi: 10.1016/j.cub.2014.07.020. Epub 2014 Aug 14.

Abstract

The sense of taste is critical in determining the nutritional suitability of foods. Sweet and bitter are primary taste modalities in mammals, and their behavioral relevance is similar in flies. Sweet taste drives the appetitive response to energy sources, whereas bitter taste drives avoidance of potential toxins and also suppresses the sweet response [1, 2]. Despite their importance to survival, little is known about the neural circuit mechanisms underlying integration of sweet and bitter taste. Here, we describe a presynaptic gain control mechanism in Drosophila that differentially affects sweet and bitter taste channels and mediates integration of these opposing stimuli. Gain control is known to play an important role in fly olfaction, where GABAB receptor (GABABR) mediates intra- and interglomerular presynaptic inhibition of sensory neuron output [3-5]. In the taste system, we find that gustatory receptor neurons (GRNs) responding to sweet compounds express GABABR, whereas those that respond to bitter do not. GABABR mediates presynaptic inhibition of calcium responses in sweet GRNs, and both sweet and bitter stimuli evoke GABAergic neuron activity in the vicinity of GRN axon terminals. Pharmacological blockade and genetic reduction of GABABR both lead to increased sugar responses and decreased suppression of the sweet response by bitter compounds. We propose a model in which GABA acts via GABABR to expand the dynamic range of sweet GRNs through presynaptic gain control and suppress the output of sweet GRNs in the presence of opposing bitter stimuli.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila melanogaster / physiology*
  • Female
  • Sensory Receptor Cells / physiology
  • Sucrose / chemistry
  • Taste Perception*

Substances

  • Sucrose