Brain-wide representations of olfactory behavior in C. elegans

Abstract

Olfactory navigation emerges from dynamic interactions between sensory input, brain activity state and the animal's own movements. In C. elegans, a compact nervous system enables brain-wide imaging in behaving animals exposed to controlled olfactory environments, with an undulatory locomotion that reduces navigation to transitions among forward runs, reversals, and turns. Here, we used tracking microscopy to record and compare brain-wide neural activity in crawling worms navigating spatial odor gradients or isotropic environments, and in immobilized worms responding to temporal odor pulses. Across conditions, we identified strongly correlated brain-wide activity patterns spanning olfactory sensory neurons, interneurons, and premotor interneurons. Comparisons between navigation in odor gradients and exploration in isotropic environments revealed a compact functional circuit linking olfactory sensory neurons, interneurons, and premotor neurons. Comparisons between different odors distinguished sensory activity relationships associated with odor identity from a shared sensorimotor circuit for navigational movement. Comparisons between crawling and immobilized animals revealed profound differences in motor-state transitions and brain-wide correlation structure, further demonstrating the dependence of sensory representations and motor decision-making on behavioral context. Our findings reveal a functional organization linking olfactory sensory activity to navigational movement and show how this organization depends on behavioral state and environmental context.