Mating Increases Neuronal Tyrosine Hydroxylase Expression and Selectively Gates Transmission of Male Chemosensory Information in Female Mice

Gillian A Matthews,Alison Walsh,Ronak Patel,Joana Martínez-Ricós,Owain Davies,Peter A Brennan,Hiroaki Matsunami

doi:10.1371/journal.pone.0069943

Gillian A Matthews, Alison Walsh + Show 5 more

Open Access

https://doi.org/10.1371/journal.pone.0069943

Copy DOI

Journal: PloS one	Publication Date: Jul 25, 2013
Citations: 9	License type: CC BY 4.0

Affiliation: University of Bristol, University of Valencia

Abstract

Exposure to chemosensory signals from unfamiliar males can terminate pregnancy in recently mated female mice. The number of tyrosine hydroxylase-positive neurons in the main olfactory bulb has been found to increase following mating and has been implicated in preventing male-induced pregnancy block during the post-implantation period. In contrast, pre-implantation pregnancy block is mediated by the vomeronasal system, and is thought to be prevented by selective inhibition of the mate’s pregnancy blocking chemosignals, at the level of the accessory olfactory bulb. The objectives of this study were firstly to identify the level of the vomeronasal pathway at which selective inhibition of the mate’s pregnancy blocking chemosignals occurs. Secondly, to determine whether a post-mating increase in tyrosine hydroxylase-positive neurons is observed in the vomeronasal system, which could play a role in preventing pre-implantation pregnancy block. Immunohistochemical staining revealed that mating induced an increase in tyrosine-hydroxylase positive neurons in the arcuate hypothalamus of BALB/c females, and suppressed c-Fos expression in these neurons in response to mating male chemosignals. This selective suppression of c-Fos response to mating male chemosignals was not apparent at earlier levels of the pregnancy-blocking neural pathway in the accessory olfactory bulb or corticomedial amygdala. Immunohistochemical staining revealed an increase in the number of tyrosine hydroxylase-positive neurons in the accessory olfactory bulb of BALB/c female mice following mating. However, increased dopamine-mediated inhibition in the accessory olfactory bulb is unlikely to account for the prevention of pregnancy block to the mating male, as tyrosine hydroxylase expression did not increase in females of the C57BL/6 strain, which show normal mate recognition. These findings reveal an association of mating with increased dopaminergic modulation in the pregnancy block pathway and support the hypothesis that mate recognition prevents pregnancy block by suppressing the activation of arcuate dopamine release.

Highlights

Mice learn to recognise their mate’s chemosignals during a sensitive period for memory formation contingent on mating [1]
Mate recognition during the pre-implantation period can be explained by the selective inhibition of the response to mating male chemosignals, at the level of the accessory olfactory bulb (AOB), suppressing their effectiveness in eliciting dopamine release from the arcuate hypothalamus [1]. Consistent with this hypothesis, both electrophysiological recordings and analysis of c-Fos expression have revealed a selective suppression of responses in the medial amygdala following exposure to mating male compared to unfamiliar male chemosignals [6,7]
Our study found a selective suppression of c-Fos response to the mating male pheromones in the tyrosine hydroxylase (TH)-positive dopaminergic neurons in the arcuate hypothalamus, but not at other levels of the pregnancy blocking pathway

Summary

Introduction

Mice learn to recognise their mate’s chemosignals during a sensitive period for memory formation contingent on mating [1]. The neural changes underlying mate recognition are thought to occur in the accessory olfactory bulb (AOB), which projects, via the corticomedial amygdala, to the arcuate hypothalamus [3] Activation of this pregnancy-blocking pathway by unfamiliar male chemosignals results in the release of dopamine from the arcuate hypothalamus, which inhibits prolactin release from the pituitary, thereby removing luteotrophic support and resulting in implantation failure [4,5]. Mate recognition during the pre-implantation period can be explained by the selective inhibition of the response to mating male chemosignals, at the level of the AOB, suppressing their effectiveness in eliciting dopamine release from the arcuate hypothalamus [1] Consistent with this hypothesis, both electrophysiological recordings and analysis of c-Fos expression have revealed a selective suppression of responses in the medial amygdala following exposure to mating male compared to unfamiliar male chemosignals [6,7]. We found that mating was associated with an increase in the number of TH-positive neurons in the arcuate nucleus

Objectives

Results

Conclusion