Malone Candice L, Li Jiaxuan, Luebke Elsa M, Carreras-Simons Leykza, Treis Warren W, Hammond Emma R, Monari Patrick K, Marler Catherine A
Dept. of Psychology, University of Wisconsin-Madison, Madison, USA.
Biol Sex Differ. 2025 Aug 4;16(1):58. doi: 10.1186/s13293-025-00741-4.
The monogamous California mouse (Peromyscus californicus) exhibits distinct behavioral changes during pair bond formation. Using a detailed temporal behavioral analysis over seven days, we found a rapid decrease in aggression within 24 h of pair introduction in this highly territorial species. After this aggression reduction, the gradual increase in affiliative behaviors varied by type of affiliative behavior and ranged from one to seven days. We then measured neurobiological changes at three time points during this transition to uncover mechanisms that might govern this shift from aggressive to affiliative behavior, revealing novel sex differences that add to current research on biological mechanisms of social bonding. Specifically, we examined plasticity through mRNA expression of two perineuronal net (PNN) associated proteins, HAPLN and ACAN, in two brain regions implicated in affiliation, aggression, and social cognition: the ventral anterior cingulate cortex (vACC) and lateral septum (LS). The vACC in females exhibited higher expression levels of both of these PNN components relative to males. Additionally, we observed a decrease in ACAN mRNA expression in the vACC over the course of pair bond establishment, but no such change in the LS. Furthermore, oxytocin receptor (OXTR) and vasopressin receptor (AVPR) plasticity exhibited sex-specific patterns in the vACC during pair bond formation. Females displayed higher OXTR mRNA expression across the bonding period, whereas males expressed higher AVPR mRNA levels. We discuss how a decrease in PNNs could allow for an increase in receptor plasticity in the vACC as the pair bond is established. Moreover, we suggest that structural plasticity across this social transition may differ between males and females due to factors such as pre-pair sociality and aggression/territoriality changes.
实行一夫一妻制的加利福尼亚小鼠（加州林鼠）在配偶关系形成过程中表现出明显的行为变化。通过对七天内的行为进行详细的时间分析，我们发现，在引入配偶后的24小时内，这种具有高度领地意识的物种的攻击性迅速降低。在攻击性降低之后，亲和行为的逐渐增加因亲和行为的类型而异，持续时间从一天到七天不等。然后，我们在这一转变过程中的三个时间点测量了神经生物学变化，以揭示可能控制从攻击行为向亲和行为转变的机制，发现了新的性别差异，这为当前关于社会联系生物学机制的研究增添了内容。具体而言，我们通过两种与神经元周网（PNN）相关的蛋白HAPLN和ACAN的mRNA表达，研究了两个与亲和、攻击和社会认知相关的脑区——腹侧前扣带回皮质（vACC）和外侧隔区（LS）的可塑性。相对于雄性，雌性vACC中这两种PNN成分的表达水平更高。此外，我们观察到在配偶关系建立过程中，vACC中ACAN的mRNA表达下降，但LS中没有这种变化。此外，在配偶关系形成过程中，催产素受体（OXTR）和加压素受体（AVPR）的可塑性在vACC中表现出性别特异性模式。在整个配偶关系形成期，雌性的OXTR mRNA表达较高，而雄性的AVPR mRNA水平较高。我们讨论了随着配偶关系的建立，PNN的减少如何可能导致vACC中受体可塑性的增加。此外，我们认为，由于配对前的社交性以及攻击/领地性变化等因素，这种社会转变过程中的结构可塑性在雄性和雌性之间可能存在差异。
