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A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans

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Abstract

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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Figure 1: C. elegans track isotherms around a thermotactic set point (TS) corresponding to their cultivation temperature.
Figure 2: The TS represents an average of a worm's temperature history, and TS resetting does not depend on the presence of bacterial food.
Figure 3: dgk-3 mutants show altered rates of TS resetting.
Figure 4: Mutations in dgk-3 alter the operating range of the AFD neurons upon sustained exposure to new temperatures.

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Acknowledgements

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.).

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  1. Adam Brown

    Present address: Broad Institute, 320 Charles Street, Cambridge, Massachusetts, 02141, USA

Authors and Affiliations

  1. Department of Physics, Harvard University, 17 Oxford Street, Cambridge, 02138, Massachusetts, USA

    David Biron, Christopher Gabel, Damon A Clark & Aravinthan D T Samuel

  2. Department of Biology and National Center for Behavioral Genomics, 415 South Street

    David Biron, Mayumi Shibuya, Sara M Wasserman, Adam Brown & Piali Sengupta

  3. Brandeis University, Waltham, 02454, Massachusetts, USA

    David Biron, Mayumi Shibuya, Sara M Wasserman, Adam Brown & Piali Sengupta

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  1. David Biron
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Contributions

D.B. conducted the behavioral and imaging experiments. M.S., S.M.W., A.B. and P.S. conducted the molecular biology and genetic experiments. C.G. and D.A.C. developed the behavioral and imaging assays. A.B. and C.G. initially noted the dgk-3 mutant phenotype. D.B., A.D.T.S. and P.S. contributed to data analysis and manuscript preparation.

Corresponding authors

Correspondence to Piali Sengupta or Aravinthan D T Samuel.

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Supplementary information

Supplementary Fig. 1

Structure of DGK-3. (PDF 125 kb)

Supplementary Video 1

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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