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

Asuka Takeishi,Wenxing Yang,Jihye Yeon,Nathan Harris,Piali Sengupta

doi:10.7554/elife.61167

Asuka Takeishi, Wenxing Yang + Show 3 more

Open Access

https://doi.org/10.7554/elife.61167

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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.

Highlights

Responses of animals to sensory stimuli are extensively modulated by their internal state (Grunwald Kadow, 2019; Kim et al, 2017; Li and Dulac, 2018; Stowers and Liberles, 2016)
We find that temperature responses in neither AFD nor AIY are altered upon prolonged food deprivation, the probability and duration of temperature responses in AWC are increased under these conditions
We show that expression of ins-1 in the gut is necessary for internal state-dependent thermotaxis behavioral plasticity, and establish that gut-derived INS-1 signaling targets DAF-16/FOXO in AWC to regulate temperature responses and circuit activity in response to feeding state

Summary

Introduction

Responses of animals to sensory stimuli are extensively modulated by their internal state (Grunwald Kadow, 2019; Kim et al, 2017; Li and Dulac, 2018; Stowers and Liberles, 2016). Starvation modulates responses to food-related chemical cues, and generally and broadly regulates animal behaviors (Dietrich et al, 2015; Rengarajan et al, 2019; Sayin et al, 2019; Trent et al, 1983; Yang et al, 2015). These behavioral changes may allow animals to prioritize food seeking over other behavioral drives. How starvation signals are integrated to alter neuron and circuit properties are not fully understood

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