The olfactory system plays an important role in controlling reproductive behavior in many animal species. The intimate connection between the olfactory system and reproductive development is illustrated by Kallmann syndrome, a severe condition in which gonadotropin-releasing hormone (GnRH) neurons fail to migrate, resulting in anosmia and hypogonadotropic hypogonadism in adults. 

GnRH is the hypothalamic neuropeptide that plays vital roles in vertebrate reproduction by controlling pituitary hormone production, and in turn sexual behavior including ovulation in females and sperm release in males. Although the significance of GnRH neurons for olfaction and courtship behavior is widely discussed, little is known about whether GnRH neurons can directly sense and transmit olfactory signals to modulate courtship behavior.

In a recent study published in Science China Life Sciences, a team led by Prof. HU Wei from the Institute of Hydrobiology (IHB) of the Chinese Academy of Sciences, collaborating with Prof. Vance L. Trudeau's team from the University of Ottawa, discovered that GnRH3 neurons in the olfactory epithelium of zebrafish are a type of crypt sensory neurons, which have a new function of directly sensing and transmitting sex pheromones, thereby inducing courtship behavior.

Through laser confocal three-dimensional imaging, the researchers reported a new model for the migration path and distribution pattern of GnRH3 neurons. GnRH3 neurons underwent bidirectional migration along the olfactory nerve. Cell bodies of some GnRH3 neurons were distributed within the olfactory epithelium of adult zebrafish. These findings challenge the view over the last three decades that vertebrate GnRH neurons migrate from olfactory placode to hypothalamus in a unidirectional manner.

Anatomical, behavioral and physiological data supported the researchers' proposal that a new, previously unidentified population of GnRH3 neurons in the olfactory epithelium are a type of crypt olfactory sensory neuron which directly senses the post-ovulatory sex pheromone prostaglandin F2α.

The researchers found that males harboring gnrh3 mutations exhibited a diminished GnRH3 neuronal firing rate and an impaired ability to sense and transduce female sex pheromone-encoded information critical to courtship behavior and reproductive success. These males were less attractive to females and less competitive than normal male fish.

These findings uncover a new role for GnRH neurons in courtship behavior through direct sensing of female sex pheromones. The olfactory GnRH neurons uncovered in this study act as a gating system transducing odor-encoded information critical to reproductive success. This study opens up a new path towards understanding the relationship between anosmia and gonadal dysfunction.

GnRH3 neurons initially distribute ventrally, beneath the olfactory placode. (Video by IHB)