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.

Internal State: Dynamic, Interconnected Communication Loops Distributed Across Body, Brain, and Time

“…First, the body plays a critical role in shaping internal state. The studies highlighted in this review add to the growing literature in both vertebrates and invertebrates showing that signals from the body can modify neural circuits at the very first stage of sensory processing ( Root Cory et al 2011 ; Sengupta 2013 ; Takeishi et al 2020a , 2020b ). The resulting changes at peripheral sensory neurons can lead to changes in the valence and salience of sensory inputs, altering processing in downstream circuits, and in turn modifying behavior.…”

“…Starvation can also enhance gustatory and olfactory sensitivity, allowing for increased attraction to certain tastes such as sugar or enhanced detection of low odor concentrations ( Marella et al 2012 ; Inagaki et al 2014 ). Additionally, starvation regulates thermosensory behaviors, altering an organism’s foraging strategy, baseline temperature preference, or thermoregulatory behaviors such as shivering ( Tan and Knight 2018 ; Takeishi et al 2020a , 2020b ). In the context of hunger, we have elected to focus on a few studies using invertebrate model systems that have begun to elucidate how key endocrine and neural players and mechanisms coordinate changes in behavior over varying timescales ( Root Cory et al 2011 ; Ko et al 2015 ; Takeishi et al 2020a , 2020b ; Fig.…”

“…In the worm Caenorhabditis elegans , food deprivation leads to insulin release from the gut, which in turn activates a bilateral pair of peripheral sensory neurons (called AWC) that respond to temperature ( Fig. 3A' ; Takeishi et al 2020b ). Temperature-mediated responses in satiated worms typically rely on the core-thermotaxis circuit (mediated by AFD and AIY neurons), which promotes a sequence of forward crawling, turn, and reversal behaviors that allow the worm to navigate to the most-favorable temperature region in their environment ( Mori and Ohshima 1995 ; Takeishi et al 2020a ).…”

“…However, when worms are food deprived, this normal thermotaxis response is disrupted due to the recruitment of a parallel pathway mediated by the AWC neurons. AWC and the downstream circuitry instead promote increased turn and reversal behaviors, as worms search for food instead of thermotaxing to their preferred temperature ( Takeishi, et al 2020b ). Thus, a worm’s satiety state can lead to insulin-mediated activation of sensory neurons, which in turn drastically modulates the behavioral response of the animal.…”

Regulation of Satiety Quiescence by Neuropeptide Signaling in Caenorhabditis elegans

“…Among the 40 ins genes, ins-1 is most similar to the human insulin in its sequence and antagonizes DAF-2 insulin receptor (Pierce et al, 2001). INS-1 plays roles in salt conditioning, olfactory feedback, and thermotaxis plasticity by starvation (Tomioka et al, 2006;Chalasani et al, 2010;Takeishi et al, 2020). These studies indicate that INS peptides play critical roles in conveying the animal's metabolic states.…”