Olfactory GnRH3 crypt sensory neurons transduce sex pheromone signals to induce male courtship behavior in zebrafish.

Olfactory activation of neuroendocrine pathways plays vital roles in many organisms for reproduction and survival. The importance of gonadotropin-releasing hormone (GnRH) neurons for reproduction is well-established but little is known about whether they can directly sense and transmit sex pheromone signals. We have uncovered the migration path and distribution pattern of a new GnRH neuronal population that fulfills this role. GnRH3 neurons arise from the region located beneath olfactory placode, undergo bidirectional migration along the olfactory nerve, and cell bodies lie within the olfactory epithelium, olfactory bulb and hypothalamus. These olfactory epithelial GnRH3 neurons express ora4, the olfactory receptor that detects pheromones. GnRH3-OB neurons with olfactory epithelial GnRH3 neurons ablation failed to respond to the waterborne post-ovulatory sex pheromone prostaglandin F2α (PGF2α). GnRH3 neurons in gnrh3-/- mutants have a reduced basal firing rate leading to abnormal responses to PGF2α. Male gnrh3-/- zebrafish exhibit deficiencies in courtship behavior and a decreased capacity to compete and spawn with females. These findings indicate that GnRH3-OE neurons function as crypt sensory neurons transducing sex pheromone-encoded information critical to reproductive success.