Muscle-directed mechanosensory feedback activates egg-laying circuit activity and behavior inC. elegans

Abstract

SummaryMechanosensory feedback of internal reproductive state drives decisions about when and where to reproduce.1For instance, stretch in theDrosophilareproductive tract produced by artificial distention or from accumulated eggs regulates the attraction to acetic acid to ensure optimal oviposition.2How such mechanosensory feedback modulates neural circuits to coordinate reproductive behaviors is incompletely understood. We previously identified a stretch-dependent homeostat that regulates egg laying inCaenorhabditis elegans. Sterilized animals lacking eggs show reduced Ca2+transient activity in the presynaptic HSN command motoneurons that drive egg-laying behavior while animals forced to accumulate extra eggs show dramatically increased circuit activity that restores egg laying.3Interestingly, genetic ablation or electrical silencing of the HSNs delays, but does not abolish, the onset of egg laying3–5with animals recovering vulval muscle Ca2+transient activity upon egg accumulation.6Using an acute gonad microinjection technique to mimic changes in pressure and stretch resulting from germline activity and egg accumulation, we find that injection rapidly stimulates Ca2+activity in both neurons and muscles of the egg-laying circuit. Injection-induced vulval muscle Ca2+activity requires L-type Ca2+channels but is independent of presynaptic input. Conversely, injection-induced neural activity is disrupted in mutants lacking the vulval muscles, suggesting ‘bottom-up’ feedback from muscles to neurons. Direct mechanical prodding activates the vulval muscles, suggesting they are the proximal targets of the stretch-dependent stimulus. Our results show that egg-laying behavior inC. elegansis regulated by a stretch-dependent homeostat that scales postsynaptic muscle responses with egg accumulation in the uterus.