A memory of prior thermal experience governs Caenorhabditis elegans thermotactic behavior. On a spatial thermal gradient, C. elegans tracks isotherms near a remembered temperature we call the thermotactic set-point (TS). The TS corresponds to the previous cultivation temperature and can be reset by sustained exposure to a new temperature. The mechanisms underlying this behavioral plasticity are unknown, partly because sensory and experience-dependent components of thermotactic behavior have been difficult to separate. Using newly developed quantitative behavioral analyses, we demonstrate that the TS represents a weighted average of a worm's temperature history. We identify the DGK-3 diacylglycerol kinase as a thermal memory molecule that regulates the rate of TS resetting by modulating the temperature range of synaptic output, but not temperature sensitivity, of the AFD thermosensory neurons. These results provide the first mechanistic insight into the basis of experience-dependent plasticity in this complex behavior.
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We are very grateful to C. Gauthier for technical assistance, the Caenorhabditis Genetics Center for strains, the C. elegans Gene Knockout Consortium for the dgk-3(gk110) allele, I. Mori (Nagoya University) for the nhr-38::YC2.12–expressing transgenic strain, H. Suzuki (University of California, San Diego) for the YC2.12 clone, A. Fire (Stanford University) for the C. elegans expression vectors, and C. Bargmann, L. Griffith, O. Hobert, M. Rosbash and the Sengupta and Samuel labs for discussion and comments on the manuscript. This work was supported by a Human Frontier Science Program cross-disciplinary fellowship (D.B.), the US National Institutes of Health (NS44232, P.S.), and the US National Science Foundation, the McKnight Foundation and the Sloan Foundation (A.D.T.S.).
The authors declare no competing financial interests.
Structure of DGK-3. (PDF 125 kb)
Isothermal tracking exhibited by wild-type animals cultivated at 20 °C and placed on a spatial thermal gradient, ranging from 18 °C on the left to 22 °C on the right. Animals track isotherms around 20 °C. Movie speed ×30. (MOV 264 kb)
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Biron, D., Shibuya, M., Gabel, C. et al. A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans. Nat Neurosci 9, 1499–1505 (2006). https://doi.org/10.1038/nn1796
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