Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation

Martijn P.J. Dekkers, Felix Salfelder, Tom Sanders, Oluwatoroti Umuerri, Netta Cohen*, Gert Jansen*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

7 Citations (Scopus)
26 Downloads (Pure)

Abstract

A conventional understanding of perception assigns sensory organs the role of capturing the environment. Better sensors result in more accurate encoding of stimuli, allowing for cognitive processing downstream. Here we show that plasticity in sensory neurons mediates a behavioral switch in C. elegans between attraction to NaCl in naïve animals and avoidance of NaCl in preconditioned animals, called gustatory plasticity. Ca2+ imaging in ASE and ASH NaCl sensing neurons reveals multiple cell-autonomous and distributed circuit adaptation mechanisms. A computational model quantitatively accounts for observed behaviors and reveals roles for sensory neurons in the control and modulation of motor behaviors, decision making and navigational strategy. Sensory adaptation dynamically alters the encoding of the environment. Rather than encoding the stimulus directly, therefore, we propose that these C. elegans sensors dynamically encode a context-dependent value of the stimulus. Our results demonstrate how adaptive sensory computation can directly control an animal’s behavioral state.

Original languageEnglish
Article number1053
JournalCommunications Biology
Volume4
Issue number1
DOIs
Publication statusPublished - 9 Sept 2021

Bibliographical note

Funding Information:
We thank R. Tsien, A. Miyawaki and B. Schafer for constructs, B. Schafer and H. Suzuki for help in setting up imaging and for sharing unpublished results, WormBase for providing annotated data on prior work, and the Caenorhabditis Genetics Center for strains. We also thank C. Brittin, R. Gudde, I. Hope, R. Hukema, S. Lockery, S. Rade-makers and T. Thiele for suggestions. This work was funded by the Center for Biomedical Genetics, the Royal Netherlands Academy of Sciences, ALW/NWO and the EPSRC via grants EP/J004057/1 and EP/N010523/1.

Publisher Copyright:
© 2021, The Author(s).

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