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Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans

Abstract

Humans and other animals can sense temperature changes as small as 0.1 °C. How animals achieve such exquisite sensitivity is poorly understood. By recording from the C. elegans thermosensory neurons AFD in vivo, we found that cooling closes and warming opens ion channels. We found that AFD thermosensitivity, which exceeds that of most biological processes by many orders of magnitude, is achieved by nonlinear signal amplification. Mutations in genes encoding subunits of a cyclic guanosine monophosphate (cGMP)-gated ion channel (tax-4 and tax-2) and transmembrane guanylate cyclases (gcy-8, gcy-18 and gcy-23) eliminated both cooling- and warming-activated thermoreceptor currents, indicating that a cGMP-mediated pathway links variations in temperature to changes in ionic currents. The resemblance of C. elegans thermosensation to vertebrate photosensation and the sequence similarity between TAX-4 and TAX-2 and subunits of the rod phototransduction channel raise the possibility that nematode thermosensation and vertebrate vision are linked by conserved evolution.

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Figure 1: In vivo recording from wild-type C. elegans thermosensory neurons.
Figure 2: ThRC response latency.
Figure 3: Temperature dependence of voltage-gated currents in thermosensory (AFD) and chemosensory (AWA) neurons.
Figure 4: Thermoreceptor currents in AFD and AWA neurons at −60 mV.
Figure 5: ThRC adaptation.
Figure 6: AFD signals are similar in well-fed and starved animals.
Figure 7: Ionic properties of AFD thermoreceptor currents (ThRCs).
Figure 8: Thermoreceptor currents (ThRCs) are observed in wild-type, but not in tax-4, tax-2 or triple mutant gcy-8gcy-18gcy-23 AFD neurons, nor in AWC neurons.

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Acknowledgements

We thank C.F. Barrett, T.R. Clandinin, J. Huegenard, A.Y. Katsov, S. Lockery, R. Milo and the Goodman laboratory for comments; G. Wang and Z. Liao for help with genotyping; and P. Sengupta, C. Bargmann, I. Mori and the Caenorhabditis Genetics Center, which is funded by the US National Institutes of Health National Center for Research Resources, for strains. This work was supported by the Baxter, Sloan, McKnight and Klingenstein Foundations (M.B.G.), the National Science Foundation (M.B.G.), the US National Institutes of Health (M.B.G.), a fellowship from the Human Frontiers Science Program (B.L.M.), and a Stanford Graduate Fellowship and Dan David Prize Scholarship (D.R.).

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D.R. conducted electrophysiology experiments, analyzed data and wrote the manuscript. B.L.M. prepared mutant strains, conducted behavioral experiments and contributed to writing the manuscript. M.B.G. conducted electrophysiology experiments, supervised the project and wrote the manuscript.

Corresponding author

Correspondence to Miriam B Goodman.

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Ramot, D., MacInnis, B. & Goodman, M. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat Neurosci 11, 908–915 (2008). https://doi.org/10.1038/nn.2157

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