Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity

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Abstract

Internal state alters sensory behaviors to optimize survival strategies. The neuronal mechanisms underlying hunger-dependent behavioral plasticity are not fully characterized. Here we show that feeding state alters C. elegans thermotaxis behavior by engaging a modulatory circuit whose activity gates the output of the core thermotaxis network. Feeding state does not alter the activity of the core thermotaxis circuit comprised of AFD thermosensory and AIY interneurons. Instead, prolonged food deprivation potentiates temperature responses in the AWC sensory neurons, which inhibit the postsynaptic AIA interneurons to override and disrupt AFD-driven thermotaxis behavior. Acute inhibition and activation of AWC and AIA, respectively, restores negative thermotaxis in starved animals. We find that state-dependent modulation of AWC-AIA temperature responses requires INS-1 insulin-like peptide signaling from the gut and DAF-16 FOXO function in AWC. Our results describe a mechanism by which functional reconfiguration of a sensory network via gut-brain signaling drives state-dependent behavioral flexibility.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data for all behavioral and imaging data have been provided in Excel spreadsheets with data for individual figure panels in separate tabs. Two spreadsheets are provided for main and supplementary figures

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Author details

Asuka Takeishi

Center for Brain Science, RIKEN, Wako, Japan

Competing interests
No competing interests declared.
Jihye Yeon

Department of Biology, Brandeis University, Waltham, United States

Competing interests
No competing interests declared.
Nathan Harris

Department of Biology, Brandeis University, Waltham, United States

Competing interests
No competing interests declared.
Wenxing Yang

Physiology, West China School of Basic Medical Sciences and Forensic Medicine, Chengdu, China

Competing interests
No competing interests declared.
Piali Sengupta

Department of Biology, Brandeis University, Waltham, United States

For correspondence
sengupta@brandeis.edu

Competing interests
Piali Sengupta, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0001-7468-0035

Funding

National Institute of General Medical Sciences (R35 GM122463)

Piali Sengupta

National Institute of Neurological Disorders and Stroke (T32 NS007292)

Nathan Harris

National Institute of Neurological Disorders and Stroke (F32 NS112453)

Nathan Harris

RIKEN (H28-1058)

Asuka Takeishi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.