Research Article: GnRH-mediated olfactory and visual inputs promote mating-like behaviors in male zebrafish

Date Published: March 22, 2017

Publisher: Public Library of Science

Author(s): Lei Li, Jennifer L. Wojtowicz, John H. Malin, Tao Huang, Eric B. Lee, Zijiang Chen, Hiroaki Matsunami.

http://doi.org/10.1371/journal.pone.0174143

Abstract

The engagement of sexual behaviors is regulated by a number of factors which include gene expression, hormone circulation, and multi-sensory information integration. In zebrafish, when a male and a female are placed in the same container, they show mating-like behaviors regardless of whether they are kept together or separated by a net. No mating-like behaviors are observed when same-sex animals are put together. Through the olfacto-visual centrifugal pathway, activation of the terminalis nerve in the olfactory bulb increases GnRH signaling in the brain and triggers mating-like behaviors between males. In zebrafish mutants or wild-type fish in which the olfacto-visual centrifugal pathway is impaired or chemically ablated, in response to odor stimulation the mating-like behaviors between males are no longer evident. Together, the data suggest that the combination of olfactory and visual signals alter male zebrafish’s mating-like behaviors via GnRH signaling.

Partial Text

The engagement of sexual behaviors is regulated by a number of factors, such as the expression of specific gene in sex-related cellular pathways, activation of hormone receptors, and stimulation of sensory cells [1–4]. Genetic loci that regulate the sexual behaviors have been identified. In flies (Drosophila melanogaster), for example, the expression of fruitless is required for initiating the courtship behaviors between the male and female animals; when the expression of fruitless is interrupted, the males alter their sexual behaviors [5,6]. Functional expression of fruitless in a variety of neural and non-neural tissues (e.g., olfactory bulb, visual cortex, auditory cells, and the gustatory system) is required for normal sexual behaviors [2, 7, 8].

It is known that the circulation of GnRH is regulated by different genetic and cellular events [36]. However, the effect of environmental input on the regulation of synthesis and release of GnRH and how external modulation of GnRH signaling transduction impacts the sexual behaviors remain to be examined. Zebrafish provide a model system for addressing these issues. Zebrafish possess two distinctive forms of GnRH, which include cGnRH and sGnRH [37–41]. Previous studies have shown that the increase of cGnRH signaling promotes animals’ survival functions, such as food intake, whereas the modulation of sGnRH signaling transduction directly affects animals’ sexual activity and reproduction. In zebrafish, the olfactory TNs synthesize and release sGnRH [19]. Previously, we demonstrated that through the olfacto-visual centrifugal pathway, activation of the olfactory neurons decreases the release of dopamine from retinal DA-IPCs. This leads to two consequences: First, it increases the coupling between horizontal cells in the outer retina [42, 43]. Second, it lifts the inhibition of dopaminergic signaling on RGCs, thereby increasing inner retinal activity [44]. Together, the integration of olfacto-visual sensory information increases visual perception and retinal sensitivity. The increase of visual perception and retinal sensitivity directly impacts the animal’s social behaviors, which include sexual mating [45, 46].

 

Source:

http://doi.org/10.1371/journal.pone.0174143

 

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