Sensory neurons couple arousal and foraging decisions in C. elegans

Foraging animals optimize feeding decisions by adjusting both common and
rare behavioral patterns. Here, we characterize the relationship between
an animal’s arousal state and a rare decision to leave a patch of
bacterial food. Using long-term tracking and behavioral state
classification, we find that food leaving decisions in C.
elegans are coupled to arousal states across multiple timescales.
Leaving emerges probabilistically over minutes from the high arousal
roaming state, but is suppressed during the low arousal dwelling state.
Immediately before leaving, animals have a brief acceleration in speed
that appears as a characteristic signature of this behavioral motif.
Neuromodulatory mutants and optogenetic manipulations that increase
roaming have a coupled increase in leaving rates, and similarly acute
manipulations that inhibit feeding induce both roaming and leaving. By
contrast, inactivating a set of chemosensory neurons that depend on the
cGMP-gated transduction channel TAX-4 uncouples roaming and leaving
dynamics. In addition, tax-4-expressing sensory neurons promote
lawn-leaving behaviors that are elicited by feeding inhibition. Our
results indicate that sensory neurons responsive to both internal and
external cues play an integrative role in arousal and foraging decisions.