Neural dynamics of a multi-timescale social behavior

The brain of any animal has to operate on multiple timescales at once. In the long term, it has to evaluate the trade-offs between feeding, mating or conserving energy. In the medium term, the animal uses those calculations to create a plan — a hungry worm, for example, might choose to feed where it is rather than to go off in search of better food or mates. In the near term, animals have to make immediate decisions about where to go, such as turning left or right or continuing on the current path. Studying how animals plan over these different timescales has been challenging, in large part because it requires many brain areas operating at once, and neuroscientists have lacked the tools to observe neural activity over broad swaths of the brain. To overcome this technical limitation, we will study the mating behavior of a simple animal, the tiny roundworm C. elegans. Roundworms find a mate by launching a systematic search of the environment, integrating scent and tactile information. Once the worm has found a potential mate, it begins a rudimentary sequence of actions that include turning, forward and backward movement, making contact, and finally copulation. The animal’s behavior is modified by long-term factors, such as natural cycles of activity and rest, whether its hungry or full, and the quality of food in the environment. We have developed a custom microscope to track the activity of almost every neuron in the roundworm’s head — here, we will perform the first whole-brain recordings in any animal during social interactions. Using this data, we will map the neural activity underlying long-term, internal states, such as hunger, and examine how that influences neural activity linked to medium-term behaviors, such as mating. We will combine neural activity and behavioral data with knowledge of the worm’s neural wiring to construct computer and mathematical models, from which we will learn how behavior is generated by neuronal activity, and how neuronal activity arises from neuronal network architectures. Because the wiring differs between the two sexes, we can also observe how sex-specific versus non-sex-specific behaviors arise in two variants of a nervous system. Our work in the lowly roundworm will shed light on how the nervous system processes information over multiple timescales with relevance for larger animals, including humans.