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The Molecular Basis for Attractive Salt-Taste Coding in Drosophila

Science  14 Jun 2013:
Vol. 340, Issue 6138, pp. 1334-1338
DOI: 10.1126/science.1234133

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Too Much or Too Little

An important task of the nervous system is to distribute information appropriately throughout the brain. The olfactory and gustatory systems of Drosophila provide good models for understanding these processes and the underlying mechanisms (see the Perspective by Su and Carlson). Lin et al. (p. 1338) mapped out the circuit that detects carbon dioxide (CO2), an important environmental and communication signal for fruit flies. Two distinct classes of projection neurons mediate avoidance of high and low concentrations of CO2, while a third class, comprising inhibitory neurons, shuts down the low-concentration pathway at high concentrations. In contrast to other basic taste qualities, salt is innately attractive at low concentrations, but aversive at high concentrations. The mechanisms underlying salt detection are poorly understood in any species mainly because of a lack of specific molecular tools. Zhang et al. (p. 1334) discovered that Drosophila uses two types of gustatory receptor neurons to distinguish between high and low concentrations of salt. One type is activated maximally by low salt and induces attractive feeding behavior. The other class of receptors is activated primarily by high salt and leads to avoidance behavior.

Abstract

Below a certain level, table salt (NaCl) is beneficial for animals, whereas excessive salt is harmful. However, it remains unclear how low- and high-salt taste perceptions are differentially encoded. We identified a salt-taste coding mechanism in Drosophila melanogaster. Flies use distinct types of gustatory receptor neurons (GRNs) to respond to different concentrations of salt. We demonstrated that a member of the newly discovered ionotropic glutamate receptor (IR) family, IR76b, functioned in the detection of low salt and was a Na+ channel. The loss of IR76b selectively impaired the attractive pathway, leaving salt-aversive GRNs unaffected. Consequently, low salt became aversive. Our work demonstrated that the opposing behavioral responses to low and high salt were determined largely by an elegant bimodal switch system operating in GRNs.

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