Paternal Retrieval Behavior Regulated by Brain Estrogen Synthetase (Aromatase) in Mouse Sires that Engage in Communicative Interactions with Pairmates.

Shirin Akther,Olga Lopatina,Shigeru Yokoyama,Zhiqi Huang,Haruhiro Higashida,Mie Matsuo,Takahiro Tsuji,Jing Zhong,Chiharu Higashida,Azam A K M Fakhrul,Teruko Yuhi,Alla B Salmina,Mingkun Liang

doi:10.3389/fnins.2015.00450

Shirin Akther, Olga Lopatina + Show 11 more

Open Access

https://doi.org/10.3389/fnins.2015.00450

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Abstract

Parental behaviors involve complex social recognition and memory processes and interactive behavior with children that can greatly facilitate healthy human family life. Fathers play a substantial role in child care in a small but significant number of mammals, including humans. However, the brain mechanism that controls male parental behavior is much less understood than that controlling female parental behavior. Fathers of non-monogamous laboratory ICR mice are an interesting model for examining the factors that influence paternal responsiveness because sires can exhibit maternal-like parental care (retrieval of pups) when separated from their pups along with their pairmates because of olfactory and auditory signals from the dams. Here we tested whether paternal behavior is related to femininity by the aromatization of testosterone. For this purpose, we measured the immunoreactivity of aromatase [cytochrome P450 family 19 (CYP19)], which synthesizes estrogen from androgen, in nine brain regions of the sire. We observed higher levels of aromatase expression in these areas of the sire brain when they engaged in communicative interactions with dams in separate cages. Interestingly, the number of nuclei with aromatase immunoreactivity in sires left together with maternal mates in the home cage after pup-removing was significantly larger than that in sires housed with a whole family. The capacity of sires to retrieve pups was increased following a period of 5 days spent with the pups as a whole family after parturition, whereas the acquisition of this ability was suppressed in sires treated daily with an aromatase inhibitor. The results demonstrate that the dam significantly stimulates aromatase in the male brain and that the presence of the pups has an inhibitory effect on this increase. These results also suggest that brain aromatization regulates the initiation, development, and maintenance of paternal behavior in the ICR male mice.

Highlights

A stable and well-functioning human family that comprises two parents with a child or children is most secure, wherein the role of the father is highly significant in addition to the essential role of the mother (Waldfogel et al, 2010)
We examined the aromatase immunoreactivity levels in the medial preoptic area (mPOA) region of the sire because it is known that aromatase is abundant in this area, and it is modified rapidly after social stimulation in the mPOA of mice (Veney and Rissman, 2000; Trainor et al, 2003)
These results show that the aromatase immunoreactivity can be modified by social stimulation such as father–mother interaction under the parent–pup separation condition

Summary

Introduction

A stable and well-functioning human family that comprises two parents with a child or children is most secure, wherein the role of the father is highly significant in addition to the essential role of the mother (Waldfogel et al, 2010). Aromatase is located in the hypothalamus and limbic system, including the medial preoptic area (mPOA), bed nucleus of the stria terminalis, ventromedial hypothalamus, medial amygdala (AMY), and many other areas (Beyer et al, 1994; Shinoda et al, 1994; Veney and Rissman, 2000) These studies suggest that brain aromatase may have versatile functions in addition to regulating sex behavior, such as brain sexual dimorphism (Hutchison et al, 1995; Yang et al, 2013) and parental behavior in response to social stimuli (Trainor and Marler, 2002; Cornil et al, 2006; Honda et al, 2011)

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