Behavioral Transition from Attack to Parenting in Male Mice: A Crucial Role of the Vomeronasal System

Behavioral Transition from Attack to Parenting in Male Mice: A Crucial Role of the Vomeronasal System
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DOI:
10.1523/jneurosci.2364-12.2013
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发表时间:
2013-03-20
影响因子:
5.3
通讯作者:
Kuroda, Kumi O.
Kuroda, Kumi O.
中科院分区:
医学1区
文献类型:
--
作者:
Tachikawa, Kashiko S.;Yoshihara, Yoshihiro;Kuroda, Kumi O.

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性幼稚的雄性老鼠对幼崽表现出强烈的攻击性行为。然而,在交配后与怀孕的雌性小鼠同居两周后,表现出幼崽定向攻击性的雄性小鼠的比例下降。随后,在成为父亲后,它们表现出父母对幼崽的行为,类似于母亲的母性行为。为了阐明这种行为转变背后的神经机制,我们使用c-Fos表达作为神经元激活的标记,研究了性行为幼稚的雄性和父亲在接触幼崽后大脑区域的差异激活。我们发现,在幼崽暴露后,在性幼稚的雄性中,沿着犁鼻神经通路的神经元亚群--包括犁鼻感觉神经元、副嗅球、杏仁内侧核、终纹床核的后内侧分裂和下丘脑前区--比父亲更强烈地激活。值得注意的是,在幼崽暴露后,没有观察到c-Fos在父亲的犁鼻感觉神经元中的诱导。对性欲幼稚的雄性进行手术切除犁鼻器,可以消除幼崽的攻击行为,同时诱导父母的行为。这些结果表明,诱发幼崽攻击的化学线索被犁鼻感觉神经元接收,并在性幼稚的雄性小鼠中激活犁鼻神经通路,而在父亲身上则不激活。因此,下调幼鼠信息素诱导的犁鼻系统的激活对于雄性小鼠从攻击到育儿的行为转变可能是重要的。
Sexually naive male mice show robust aggressive behavior toward pups. However, the proportion of male mice exhibiting pup-directed aggression declines after cohabitation with a pregnant female for 2 weeks after mating. Subsequently, on becoming fathers, they show parental behavior toward pups, similar to maternal behavior by mothers. To elucidate the neural mechanisms underlying this behavioral transition, we examined brain regions differentially activated in sexually naive males and fathers after exposure to pups, using c-Fos expression as a neuronal activation marker. We found that, after pup exposure, subsets of neurons along the vomeronasal neural pathway-including the vomeronasal sensory neurons, the accessory olfactory bulb, the posterior medial amygdala, the medioposterior division of the bed nucleus of stria terminalis, and the anterior hypothalamic area-were more strongly activated in sexually naive males than in fathers. Notably, c-Fos induction was not observed in the vomeronasal sensory neurons of fathers after pup exposure. Surgical ablation of the vomeronasal organ in sexually naive males resulted in the abrogation of pup-directed aggression and simultaneous induction of parental behavior. These results suggest that chemical cues evoking pup-directed aggression are received by the vomeronasal sensory neurons and activate the vomeronasal neural pathway in sexually naive male mice but not in fathers. Thus, the downregulation of pup pheromone-induced activation of the vomeronasal system might be important for the behavioral transition from attack to parenting in male mice.