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Animals must weigh competing needs and states to generate adaptive behavioral responses to the environment. Sensorimotor circuits are thus tasked with integrating diverse external and internal cues relevant to these needs to generate context-appropriate behaviors. However, the mechanisms that underlie this integration are largely unknown. Here, we show that a wide range of states and stimuli converge upon a single Caenorhabditis elegans olfactory neuron to modulate food-seeking behavior. Using an unbiased ribotagging approach, we find that the expression of olfactory receptor genes in the AWA olfactory neuron is influenced by a wide array of states and stimuli, including feeding state, physiological stress, and recent sensory cues. We identify odorants that activate these state-dependent olfactory receptors and show that altered expression of these receptors influences food-seeking and foraging. Further, we dissect the molecular and neural circuit pathways through which external sensory information and internal nutritional state are integrated by AWA. This reveals a modular organization in which sensory and state-related signals arising from different cell types in the body converge on AWA and independently control chemoreceptor expression. The synthesis of these signals by AWA allows animals to generate sensorimotor responses that reflect the animal’s overall state. Our findings suggest a general model in which sensory- and state-dependent transcriptional changes at the sensory periphery modulate animals’ sensorimotor responses to meet their ongoing needs and states. 

To adapt to their environments, animals must generate behaviors that are closely aligned to a rapidly changing sensory world. However, behavioral states such as foraging or courtship typically persist over long time scales to ensure proper execution. It remains unclear how neural circuits generate persistent behavioral states while maintaining the flexibility to select among alternative states when the sensory context changes. Here, we elucidate the functional architecture of a neural circuit controlling the choice between roaming and dwelling states, which underlie exploration and exploitation during foraging in C. elegans . By imaging ensemble-level neural activity in freely moving animals, we identify stereotyped changes in circuit activity corresponding to each behavioral state. Combining circuit-wide imaging with genetic analysis, we find that mutual inhibition between two antagonistic neuromodulatory systems underlies the persistence and mutual exclusivity of the neural activity patterns observed in each state. Through machine learning analysis and circuit perturbations, we identify a sensory processing neuron that can transmit information about food odors to both the roaming and dwelling circuits and bias the animal towards different states in different sensory contexts, giving rise to context-appropriate state transitions. Our findings reveal a potentially general circuit architecture that enables flexible, sensory-driven control of persistent behavioral states. 

Caenorhabditis elegans ’ behavioral states, like those of other animals, are shaped by its immediate environment, its past experiences, and by internal factors. We here review the literature on C. elegans behavioral states and their regulation. We discuss dwelling and roaming, local and global search, mate finding, sleep, and the interaction between internal metabolic states and behavior. 

Animals generate many different motor programs (such as moving, feeding and grooming) that they can alter in response to internal needs and environmental cues. These motor programs are controlled by dedicated brain circuits that act on specific muscle groups. However, little is known about how organisms coordinate these different motor programs to ensure that their resulting behavior is coherent and appropriate to the situation. This is difficult to investigate in large organisms with complex nervous systems, but with 302 brain cells that control 143 muscle cells, the small worm Caenorhabditis elegans provides a good system to examine this question. Here, Cermak, Yu, Clark et al. devised imaging methods to record each type of motor program in C. elegans worms over long time periods, while also dissecting the underlying neural mechanisms that coordinate these motor programs. This constitutes one of the first efforts to capture and quantify all the behavioral outputs of an entire organism at once. The experiments also showed that dopamine – a messenger molecule in the brain – links the neural circuits that control two motor programs: movement and egg-laying. A specific type of high-speed movement activates brain cells that release dopamine, which then transmits this information to the egg-laying circuit. This means that worms lay most of their eggs whilst traveling at high speed through a food source, so that their progeny can be distributed across a nutritive environment. This work opens up the possibility to study how behaviors are coordinated at the level of the whole organism – a departure from the traditional way of focusing on how specific neural circuits generate specific behaviors. Ultimately, it will also be interesting to look at the role of dopamine in behavior coordination in a wide range of animals.