Tsuneoka Yousuke, Tokita Kenichi, Yoshihara Chihiro, Amano Taiju, Esposito Gianluca, Huang Arthur J, Yu Lily M Y, Odaka Yuri, Shinozuka Kazutaka, McHugh Thomas J, Kuroda Kumi O
Laboratory for Affiliative Social Behavior, RIKEN Brain Science Institute, Saitama, Japan Department of Anatomy, School of Medicine Toho University, Tokyo, Japan.
Laboratory for Affiliative Social Behavior, RIKEN Brain Science Institute, Saitama, Japan.
EMBO J. 2015 Nov 3;34(21):2652-70. doi: 10.15252/embj.201591942. Epub 2015 Sep 30.
Paternal behavior is not innate but arises through social experience. After mating and becoming fathers, male mice change their behavior toward pups from infanticide to paternal care. However, the precise brain areas and circuit mechanisms connecting these social behaviors are largely unknown. Here we demonstrated that the c-Fos expression pattern in the four nuclei of the preoptic-bed nuclei of stria terminalis (BST) region could robustly discriminate five kinds of previous social behavior of male mice (parenting, infanticide, mating, inter-male aggression, solitary control). Specifically, neuronal activation in the central part of the medial preoptic area (cMPOA) and rhomboid nucleus of the BST (BSTrh) retroactively detected paternal and infanticidal motivation with more than 95% accuracy. Moreover, cMPOA lesions switched behavior in fathers from paternal to infanticidal, while BSTrh lesions inhibited infanticide in virgin males. The projections from cMPOA to BSTrh were largely GABAergic. Optogenetic or pharmacogenetic activation of cMPOA attenuated infanticide in virgin males. Taken together, this study identifies the preoptic-BST nuclei underlying social motivations in male mice and reveals unexpected complexity in the circuit connecting these nuclei.
父性行为并非天生,而是通过社会经验形成的。交配成为父亲后,雄性小鼠对幼崽的行为会从杀婴转变为父性照料。然而,连接这些社会行为的精确脑区和神经回路机制在很大程度上尚不清楚。在此,我们证明视前区-终纹床核(BST)区域四个核团中的c-Fos表达模式能够可靠地区分雄性小鼠之前的五种社会行为(育儿、杀婴、交配、雄性间攻击、独居对照)。具体而言,内侧视前区中部(cMPOA)和BST的菱形核(BSTrh)中的神经元激活能够以超过95%的准确率追溯检测到父性和杀婴动机。此外,cMPOA损伤使父亲的行为从父性转变为杀婴,而BSTrh损伤则抑制了未交配雄性的杀婴行为。从cMPOA到BSTrh的投射主要是γ-氨基丁酸能的。对cMPOA进行光遗传学或药物遗传学激活可减少未交配雄性的杀婴行为。综上所述,本研究确定了雄性小鼠社会动机背后的视前区-BST核团,并揭示了连接这些核团的神经回路中意想不到的复杂性。