Thermosensory processing in the Drosophila brain.

Wendy W Liu,Ofer Mazor,Rachel I Wilson

doi:10.1038/nature14170

Wendy W Liu, Ofer Mazor + Show 1 more

Open Access

https://doi.org/10.1038/nature14170

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Journal: NatureJobs	Publication Date: Mar 4, 2015
Citations: 92	License type: cc-by

Affiliation: Harvard University, Harvard NeuroDiscovery Center

Abstract

In Drosophila, just as in vertebrates, changes in external temperature are encoded by bidirectional opponent thermoreceptor cells: some cells are excited by warming and inhibited by cooling, whereas others are excited by cooling and inhibited by warming1,2. The central circuits that process these signals are not understood. In Drosophila, a specific brain region receives input from thermoreceptor cells2,3. Here we show that distinct genetically-identified projection neurons (PNs) in this brain region are excited by cooling, warming, or both. The PNs excited by cooling receive mainly feedforward excitation from cool thermoreceptors. In contrast, the PNs excited by warming (“warm-PNs”) receive both excitation from warm thermoreceptors and crossover inhibition from cool thermoreceptors via inhibitory interneurons. Notably, this crossover inhibition elicits warming-evoked excitation, because warming suppresses tonic activity in cool thermoreceptors. This in turn disinhibits warm-PNs and sums with feedforward excitation evoked by warming. Crossover inhibition could cancel non-thermal activity (noise) that is positively-correlated among warm and cool thermoreceptor cells, while reinforcing thermal activity which is anti-correlated. Our results show how central circuits can combine signals from bidirectional opponent neurons to construct sensitive and robust neural codes.

Highlights

The central circuits that process the somatic senses are poorly understood
For the first time, thermosensory projection neurons (PNs) postsynaptic to peripheral thermoreceptor cells that are excited by cooling, warming, or both
Warm-PNs receive a weak excitatory input from cool thermoreceptors which is normally masked by strong crossover inhibition from the cool pathway

Summary

Introduction

The central circuits that process the somatic senses are poorly understood. Among the somatic senses, thermosensation is intriguing from a fundamental neural coding perspective. A warm stimulus rarely evoked a sense of warmth from a cool spot, and vice versa Based on these observations, they proposed that different thermal sensations arise from the stimulation of distinct receptors in the skin that give rise to only one perceptual quality (Green, 2004; Norrsell et al, 1999). They proposed that different thermal sensations arise from the stimulation of distinct receptors in the skin that give rise to only one perceptual quality (Green, 2004; Norrsell et al, 1999) This theory was later popularized by Max von Frey (1852–1932) as the specificity theory of somesthesis, which later became known as the “labeled-line” hypothesis (Ma, 2010; Prescott and Ratte, 2012). In Drosophila, silencing warm-activated thermoreceptor cells attenuates behavioral responses to warming but not cooling; silencing cool-activated thermoreceptor cells attenuates behavioral responses to cooling but not warming (Gallio et al, 2011)

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