Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity
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
Article and author information
Author details
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.
Reviewing Editor
- Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States
Version history
- Received: July 16, 2020
- Accepted: October 18, 2020
- Accepted Manuscript published: October 19, 2020 (version 1)
- Version of Record published: November 5, 2020 (version 2)
Copyright
© 2020, Takeishi et al.
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.
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