Oxytocin- and arginine vasopressin-containing fibers in the cortex of humans, chimpanzees, and rhesus macaques

• Type of Material: Article
• Authors: Christina N. Rogers, Emory University; Amy P. Ross, Georgia State University; Shweta P. Sahu, Yerkes National Primate Research Center; Ethan R. Siegel, Yerkes National Primate Research Center; Jeromy M. Dooyema, Yerkes National Primate Research Center; Mary Ann Cree, Yerkes National Primate Research Center; Edward G. Stopa, Brown University; Larry J. Young, Emory University; James K. Rilling, Emory University; H. Elliott Albers, Georgia State University; Todd M. Preuss, Emory University
• Language: English
• Date: 2018-05-24
• Publisher: John Wiley and Sons
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2018 Wiley Periodicals, Inc.
• Final Published Version (URL): https://doi.org/10.1002/ajp.22875
• Title of Journal or Parent Work: American Journal of Primatology
• Volume: 80
• Issue: 10
• Start Page: e22875
• Grant/Funding Agency: The Leakey Foundation; The Templeton Foundation; NIH
• Grant/Funding Information: This research was supported by funding from The Leakey Foundation (#38217) to CR and The Templeton Foundation (#40463) to HEA, LJY, JKR, and TMP. Additional support was provided by NIH grants P50MH100023 to LJY and by NIH OD P51OD11132 to YNPRC.
• Keywords: cingulate; insula; primates; neuropeptides; axons
• Subject - Topics: Comparative neuroscience; Neuroanatomy; Behavioral neuroscience

Abstract

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.