Abstract
The sensation of bitter substances can alert an animal that a specific type of food is harmful and should not be consumed. However, not all bitter compounds are equally toxic and some may even be beneficial in certain contexts. Thus, taste systems in general may have a broader range of functions than just in alerting the animal. In this study we investigate bitter sensing and processing in Drosophila larvae using quinine, a substance perceived by humans as bitter. We show that behavioral choice, feeding, survival, and associative olfactory learning are all directly affected by quinine. On the cellular level, we show that 12 gustatory sensory receptor neurons that express both GR66a and GR33a are required for quinine-dependent choice and feeding behavior. Interestingly, these neurons are not necessary for quinine-dependent survival or associative learning. On the molecular receptor gene level, the GR33a receptor, but not GR66a, is required for quinine-dependent choice behavior. A screen for gustatory sensory receptor neurons that trigger quinine-dependent choice behavior revealed that a single GR97a receptor gene expressing neuron located in the peripheral terminal sense organ is partially necessary and sufficient. For the first time, we show that the elementary chemosensory system of the Drosophila larva can serve as a simple model to understand the neuronal basis of taste information processing on the single cell level with respect to different behavioral outputs.
Highlights
The sense of taste is the initial evaluation step that determines food quality and is critical for food acceptance or rejection
We show that 12 gustatory sensory receptor neurons that express both GR66a and GR33a are required for quinine-dependent choice and feeding behavior
We show that the elementary chemosensory system of the Drosophila larva can serve as a simple model to understand the neuronal basis of taste information processing on the single cell level with respect to different behavioral outputs
Summary
The sense of taste is the initial evaluation step that determines food quality and is critical for food acceptance or rejection. Drosophila larvae are a powerful experimental system for deciphering information at the single-neuron level, from peripheral sensory organs to higher brain centers, because of the simplicity of its neuronal circuitry, their non-redundant cellular organization, and their genetic tractability (Colomb et al, 2007; Louis et al, 2008; Keene et al, 2011; Kwon et al, 2011) This is illustrated by multiple studies that characterized the larval olfactory system at a fine scale (Ramaekers et al, 2005; Gerber and Stocker, 2007; Masuda-Nakagawa et al, 2009; Selcho et al, 2009; Pauls et al, 2010; Schleyer et al, 2011; Thum et al, 2011). We expand this approach in the gustatory system to obtain a first functional understanding of the molecular and neuronal basis of bitter sensing
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