Lambert Kelly G, Franssen Catherine L, Bardi Massimo, Hampton Joseph E, Hainley Leslie, Karsner Stephanie, Tu Eddie B, Hyer Molly M, Crockett Ashly, Baranova Anya, Ferguson Tajh, Ferguson Tenaj, Kinsley Craig H
Department of Psychology, Randolph-Macon College, Ashland, Va., USA.
Brain Behav Evol. 2011;77(3):159-75. doi: 10.1159/000326054. Epub 2011 May 6.
Rodent paternal models provide unique opportunities to investigate the emergence of affiliative social behavior in mammals. Using biparental and uniparental Peromyscus species (californicus and maniculatus, respectively) we assessed paternal responsiveness by exposing males to biological offspring, unrelated conspecific pups, or familiar brothers following a 24-hour separation. The putative paternal circuit we investigated included brain areas involved in fear/anxiety [cingulate cortex (Cg), medial amygdala (MeA), paraventricular nucleus of the hypothalamus (PVN), and lateral septum (LS)], parental motivation [medial preoptic area (MPOA)], learning/behavioral plasticity (hippocampus), olfaction [pyriform cortex (PC)], and social rewards (nucleus accumbens). Paternal experience in californicus males reduced fos immunoreactivity (ir) in several fear/anxiety areas; additionally, all californicus groups exhibited decreased fos-ir in the PC. Enhanced arginine vasopressin (AVP) and oxytocin (OT)-ir cell bodies and fibers, as well as increased neuronal restructuring in the hippocampus, were also observed in californicus mice. Multidimensional scaling analyses revealed distinct brain activation profiles differentiating californicus biological fathers, pup-exposed virgins, and pup-naïve virgins. Specifically, associations among MPOA fos, CA1 fos, dentate gyrus GFAP, CA2 nestin-, and PVN OT-ir characterized biological fathers; LS fos-, Cg fos-, and AVP-ir characterized pup-exposed virgins, and PC-, PVN-, and MeA fos-ir characterized pup-naïve virgins. Thus, whereas fear/anxiety areas characterized pup-naïve males, neurobiological factors involved in more diverse functions such as learning, motivation, and nurturing responses characterized fatherhood in biparental californicus mice. Less distinct paternal-dependent activation patterns were observed in uniparental maniculatus mice. These data suggest that dual neurobiological circuits, leading to the inhibition of social-dependent anxiety as well as the activation of affiliative responses, characterize the transition from nonpaternal to paternal status in californicus mice.
啮齿动物父本模型为研究哺乳动物亲和社会行为的出现提供了独特的机会。我们使用双亲及单亲的鹿鼠属物种（分别为加州鹿鼠和北美鹿鼠），在24小时分离后，将雄性个体暴露于亲生后代、无关的同物种幼崽或熟悉的兄弟面前，以此评估父本反应性。我们所研究的假定父本神经回路包括参与恐惧/焦虑的脑区[扣带回皮质（Cg）、内侧杏仁核（MeA）、下丘脑室旁核（PVN）和外侧隔区（LS）]、亲代动机[内侧视前区（MPOA）]、学习/行为可塑性（海马体）、嗅觉[梨状皮质（PC）]以及社会奖赏（伏隔核）。加州鹿鼠雄性个体的父本经历降低了几个恐惧/焦虑区域的fos免疫反应性（ir）；此外，所有加州鹿鼠组在梨状皮质中的fos-ir均降低。在加州鹿鼠中还观察到精氨酸加压素（AVP）和催产素（OT）-ir细胞体及纤维增强，以及海马体中神经元重构增加。多维尺度分析揭示了区分加州鹿鼠亲生父亲、接触幼崽的处女鼠和未接触幼崽的处女鼠的不同脑激活模式。具体而言，MPOA fos、CA1 fos、齿状回GFAP、CA2巢蛋白和PVN OT-ir之间的关联表征了亲生父亲；LS fos、Cg fos和AVP-ir表征了接触幼崽的处女鼠，而PC、PVN和MeA fos-ir表征了未接触幼崽的处女鼠。因此，虽然恐惧/焦虑区域表征了未接触幼崽的雄性个体，但在双亲的加州鹿鼠中，涉及学习、动机和养育反应等更多样化功能的神经生物学因素表征了父性。在单亲的北美鹿鼠中观察到的父本依赖性激活模式不太明显。这些数据表明，导致社会依赖性焦虑受到抑制以及亲和反应被激活的双重神经生物学回路，表征了加州鹿鼠从非父本状态到父本状态的转变。
