Animals live in complex environments in which decisions about external stimuli are influenced by sensory feedback of internal state, for example hunger, developmental age, or reproductive drive. Our understanding of how animals integrate external and internal sensory information to elicit a context-appropriate, unilateral decision remains incomplete for many such behaviors. This work explores the transition between inactive and active states of egg laying in Caenorhabditis elegans. During egg-laying active states, cells of the egg-laying circuit show rhythmic calcium activity that directs egg release. The HSN command neurons show peak activity ~2 s before egg release, followed by the VC motor neurons and the vulval muscles, both of which show peak activity coincident with egg release. However, the signal that initiates these active states remains unknown. Here we test the hypothesis that feedback of egg accumulation in the uterus provides the ultimate initiating signal. We show that acute microinjections mimic the accumulation of eggs, inducing vulval muscle contractility, egg release, and an immediate activation of the other cells of the egg-laying circuit. Surprisingly, injections into double mutants defective in synaptic transmission from the HSNs and the VCs show a normal induction of vulval muscle calcium activity and egg release. Similarly, injections into
unc-13 and
unc-31 mutants defective in small clear and dense core vesicle release also show a normal induction of vulval muscle calcium activity and egg release, consistent with the idea that the postsynaptic vulval muscles themselves are the proximal target of the acute microinjection response. The injection-induced response in the vulval muscle is dependent on L-type voltage-gated calcium channels, as injections into
egl-19 mutants or into animals treated with nemadipine, an EGL-19 channel blocker, show a greatly diminished calcium response. We show that direct prodding of the vulval muscles induces a localized calcium response, suggesting the vulval muscles themselves are directly sensitive to mechanical input. Together our results suggest that the post-synaptic egg-laying vulval muscles detect egg accumulation and signal via retrograde feedback to the presynaptic cells in the circuit to initiate and sustain the active egg-laying behavior state.