Wataru Yamamoto, Rafael Yuste
Hydra vulgaris is one of the few cnidarian species that live in freshwater environments. To understand this adaptation, we studied Hydra's mechanisms of osmoregulation. Behavioral imaging showed that Hydra accumulates water in its gastric cavity over time and periodically excretes it through the mouth. Comparative genetic analysis revealed unique aquaporin water-channel expression in Hydra's endodermal epithelium, where ultrastructural data demonstrated small clear vesicles near the gastric cavity, suggesting a potential water-release pathway. We further found that endodermal rhythmic potential 2 (RP2) neurons increase their activity before water excretion, until a threshold activity level is reached, when the mouth opens, and their activity abruptly declines. The ramping of RP2 activity, well modeled by spike-count and leaky-integration algorithms with a 30 s integration time window, leads to the specific activation of epithelial muscle cells near the mouth region before mouth opening. Confirming a causal role of RP2 in the behavior, two-photon activation of RP2 neurons induces water excretion, while ablating RP2 neurons alters it. Consistent with this, GLWamide peptides, synthesized by RP2 neurons, induce water excretion. We conclude that activation of RP2 neurons and subsequent release of GLWamide-family peptides promote water excretion and propose a circuit model for the temporal integration and sequential unfolding of this osmoregulatory cycle. Our work demonstrates that neural integration algorithms and peptide-based signaling can be used by simple nervous systems to coordinate a behavioral and physiological program.