Flexible neural control of transition points within the egg-laying behavioral sequence in Drosophila
Kevin M. Cury & Richard Axel
Nature Neuroscience (2023), doi.org/10.1038/s41593-023-01332-5
Organisms have evolved a repertoire of innate behaviors comprised of sequences of component actions that progress to satisfy drives essential for survival. I established egg-laying behavior in Drosophila as a model system to elucidate how the nervous system integrates sensory information to guide the progression of goal-directed behavioral sequences. During egg laying, females evaluate the local environment before expressing an ordered motor sequence that culminates in subterraneous egg deposition. I identified that this terminal motor sequence was remarkably plastic and could be flexibly adjusted to achieve subterraneous deposition across substrates of varying firmness. I also discovered and characterized three key elements of the neural circuit underlying this flexibility that regulate specific sequence transitions: distinct classes of tactile and proprioceptive sensory neurons and a pair of uterine motor neurons. Combining in-vivo calcium imaging and optogenetics, I revealed a causal mechanism by which the identified proprioceptors track the internal position of the egg to control the timing and direction of transitions from the terminal step in the motor sequence. Altogether, this study provides fundamental insight into how the nervous system organizes behavior, revealing both a behavioral logic and a neural basis for the sequential organization of goal-directed behavior.