Multisite gating in tonic sensory circuits integrates multimodal context to control persistent behavioral states

Abstract

Maintaining or shifting between behavioral states according to context is essential for animals to implement fitness-promoting strategies. How integration of internal state, past experience and sensory inputs orchestrate persistent multidimensional behavior changes remains poorly understood. Here, we show that C. elegans integrates food availability and environment temperature over different timescales to engage in persistent dwelling, scanning, global or glocal search strategies matching thermoregulatory and feeding needs. Transition between states, in each case, requires lifting multiple regulatory gates including AFD or FLP tonic sensory neurons activity, neuropeptide expression and downstream circuit responsiveness. State-specific FLP-6 or FLP-5 neuropeptide signaling acts on a distributed set of inhibitory receptors to promote scanning or glocal search, respectively, bypassing dopamine and glutamate-dependent behavioral state control. Multisite gating-dependent behavioral switch by GPCRs in tonic sensory circuits might represent a conserved regulatory logic for persistent behavioral state transitions enabling a flexible prioritization on the valance of multiple inputs.

System-wide mapping of neuropeptide-GPCR interactions inC. elegans

“…Some RFamide neuropeptide systems, however, show a high level of crosstalk by interacting with promiscuous GPCRs. Among these, the promiscuous receptors DMSR-1 and EGL-6 have been implicated in regulating behavioral states, such as those related to sleep, foraging and reproductive behaviors 50,[118][119][120] . Although more functional studies of peptide-GPCR couples are needed, distinct types of interactions may be specialized for different biological functions.…”

Molecular encoding of stimulus features in a single sensory neuron type enables neuronal and behavioral plasticity

“…dac-1 levels also report the absolute warm temperature upon prolonged exposure. Resting calcium levels in AFD have recently been reported to be correlated with growth temperature (Thapliyal et al, 2022; Ippolito et al, 2021). Basal calcium levels in AFD at different temperatures may drive differential expression of downstream targets via distinct regulatory molecules including CMK-1.…”