Abstract:

To achieve goals, animals string together elemental units of behavior into purposeful sequences. Importantly, to accommodate natural variability in the environment, these sequences need not be rigid and stereotyped but require a margin of flexibility as they progress from step to step. I use egg-laying behavior in Drosophila as a model system to understand how the nervous system orchestrates goal-directed behavioral sequences that are plastic and adaptive to the external world.

Drosophila do not brood their young, and so it is essential for the survival of the species that eggs are deposited properly and in a suitable environment. During egg laying, females evaluate the local environment prior to expressing an ordered motor sequence – abdominal bending, ovipositor burrowing, and egg expulsion – that culminates in egg deposition subterraneously within a nutritive substrate. I characterized the structure of this sequence in detail and observed that transitions between component actions are variable in timing and direction (i.e., flies can revert to an earlier step). Critically, variability in the sequence increased on less suitable substrates, supporting the notion that this intrinsic variability is purposeful, affording the fly adaptive flexibility.

To explore this possibility, I focused on transitions surrounding the penultimate behavioral element in the sequence, ovipositor burrowing. Using a combination of high-resolution behavioral observations, in-vivo calcium imaging, and action-triggered optogenetics, I uncovered the logic of an interoceptive feedback mechanism that governs both the timing and direction of sequence transitions from burrowing. This mechanism is based on a newly discovered cluster of interoceptive neurons that encircle the uterus and monitor the internal position of the egg during deposition. Most broadly, these findings advance our understanding of how the nervous system assembles elemental component actions into complex sequences – a fundamental process that forms the basis of nearly all goal-directed behavior.