Rogers Christina N, Ross Amy P, Sahu Shweta P, Siegel Ethan R, Dooyema Jeromy M, Cree Mary Ann, Stopa Edward G, Young Larry J, Rilling James K, Albers H Elliott, Preuss Todd M
Department of Anthropology, Emory University, Atlanta, Georgia.
Yerkes National Primate Research Center, Atlanta, Georgia.
Am J Primatol. 2018 Oct;80(10):e22875. doi: 10.1002/ajp.22875. Epub 2018 May 24.
Oxytocin (OT) and arginine-vasopressin (AVP) are involved in the regulation of complex social behaviors across a wide range of taxa. Despite this, little is known about the neuroanatomy of the OT and AVP systems in most non-human primates, and less in humans. The effects of OT and AVP on social behavior, including aggression, mating, and parental behavior, may be mediated primarily by the extensive connections of OT- and AVP-producing neurons located in the hypothalamus with the basal forebrain and amygdala, as well as with the hypothalamus itself. However, OT and AVP also influence social cognition, including effects on social recognition, cooperation, communication, and in-group altruism, which suggests connectivity with cortical structures. While OT and AVP V1a receptors have been demonstrated in the cortex of rodents and primates, and intranasal administration of OT and AVP has been shown to modulate cortical activity, there is to date little evidence that OT-and AVP-containing neurons project into the cortex. Here, we demonstrate the existence of OT- and AVP-containing fibers in cortical regions relevant to social cognition using immunohistochemistry in humans, chimpanzees, and rhesus macaques. OT-immunoreactive fibers were found in the straight gyrus of the orbitofrontal cortex as well as the anterior cingulate gyrus in human and chimpanzee brains, while no OT-immunoreactive fibers were found in macaque cortex. AVP-immunoreactive fibers were observed in the anterior cingulate gyrus in all species, as well as in the insular cortex in humans, and in a more restricted distribution in chimpanzees. This is the first report of OT and AVP fibers in the cortex in human and non-human primates. Our findings provide a potential mechanism by which OT and AVP might exert effects on brain regions far from their production site in the hypothalamus, as well as potential species differences in the behavioral functions of these target regions.
催产素(OT)和精氨酸加压素(AVP)参与多种生物分类群复杂社会行为的调节。尽管如此,在大多数非人类灵长类动物中,关于OT和AVP系统的神经解剖学知之甚少,而在人类中了解更少。OT和AVP对社会行为的影响,包括攻击、交配和育儿行为,可能主要由位于下丘脑的OT和AVP产生神经元与基底前脑和杏仁核以及下丘脑本身的广泛连接介导。然而,OT和AVP也影响社会认知,包括对社会识别、合作、交流和群体内利他行为的影响,这表明它们与皮质结构存在连接。虽然在啮齿动物和灵长类动物的皮质中已证实存在OT和AVP V1a受体,并且鼻内给予OT和AVP已被证明可调节皮质活动,但迄今为止几乎没有证据表明含OT和AVP的神经元投射到皮质中。在这里,我们使用免疫组织化学方法在人类、黑猩猩和恒河猴中证明了与社会认知相关的皮质区域中存在含OT和AVP的纤维。在人类和黑猩猩大脑的眶额皮质直回以及前扣带回中发现了OT免疫反应性纤维,而在猕猴皮质中未发现OT免疫反应性纤维。在所有物种的前扣带回中均观察到AVP免疫反应性纤维,在人类的岛叶皮质中也观察到,在黑猩猩中的分布更局限。这是人类和非人类灵长类动物皮质中OT和AVP纤维的首次报道。我们的研究结果提供了一种潜在机制,通过该机制OT和AVP可能对远离其在下丘脑产生部位的脑区发挥作用,以及这些靶区域行为功能的潜在物种差异。