An internal thermal sensor controlling temperature preference in Drosophila

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Abstract
In large animals the sensors used to monitor environmental temperature are found at the periphery of the body, and the prevailing wisdom has been that their location in small animals would be the same. For instance it was assumed that insects would sense ambient temperature via their antennae. But a surprise finding in Drosophila has identified the large heat-responsive neurons that detect ambient temperature, and they are located internally, in the brain. The four anterior cell neurons respond to warmth by activating dTrpA1 ion channels, presumably alerting the fly to seek more hospitable climes. These channels are potential targets for the disruption of thermal preference behaviours in insect pests and disease vectors. It is shown here that flies sense ambient warmth not via their antennae, but rather by a small set of neurons in the brain. These 'AC' neurons in Drosophila are sensitive to warmth due to the expression of the warmth-activated ion channel dTrpA1. Animals from flies to humans are able to distinguish subtle gradations in temperature and show strong temperature preferences1,2,3,4. Animals move to environments of optimal temperature and some manipulate the temperature of their surroundings, as humans do using clothing and shelter. Despite the ubiquitous influence of environmental temperature on animal behaviour, the neural circuits and strategies through which animals select a preferred temperature remain largely unknown. Here we identify a small set of warmth-activated anterior cell (AC) neurons located in the Drosophila brain, the function of which is critical for preferred temperature selection. AC neuron activation occurs just above the fly’s preferred temperature and depends on dTrpA1, an ion channel that functions as a molecular sensor of warmth. Flies that selectively express dTrpA1 in the AC neurons select normal temperatures, whereas flies in which dTrpA1 function is reduced or eliminated choose warmer temperatures. This internal warmth-sensing pathway promotes avoidance of slightly elevated temperatures and acts together with a distinct pathway for cold avoidance to set the fly’s preferred temperature. Thus, flies select a preferred temperature by using a thermal sensing pathway tuned to trigger avoidance of temperatures that deviate even slightly from the preferred temperature. This provides a potentially general strategy for robustly selecting a narrow temperature range optimal for survival.