Neuroanatomical distribution of oxytocin and vasopressin 1a receptors in the socially monogamous coppery titi monkey (Callicebus cupreus)

• Type of Material: Article
• Authors: Sara M. Freeman, Emory University; Hasse Walum, Emory University; Kiyoshi Inoue, Emory University; Aaron Smith, Emory University; Mark Goodman, Emory University; Karen L. Bales, University of California Davis; Larry J Young, Emory University
• Language: English
• Date: 2014-07-25
• Publisher: Elsevier: 12 months
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2014 IBRO.
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1016/j.neuroscience.2014.04.055
• Title of Journal or Parent Work: Neuroscience
• ISSN: 0306-4522
• Volume: 273
• Start Page: 12
• End Page: 23
• Grant/Funding Information: This work was supported by NIH grants MH090776 and 1P50MH100023 to LJY and NIH HD053555 and the Good Nature Institute to KLB.; Training support for SMF was provided by T32MH073525-06.; Additional support was provided by Office of Research Infrastructure Programs/OD P51OD011132 (formerly NCRR P51RR000165) to YNPRC and P51OD011107 to CNPRC.; Financial support to HW was provided by The Wenner-Gren Foundation.
• Keywords: pair bonding; PARTNER PREFERENCE; RHESUS-MONKEY; V-1A RECEPTOR; Neurosciences; NEURONAL-ACTIVITY; FLANK-MARKING BEHAVIOR; monogamy; HUMAN BRAIN; Science & Technology; neuropeptides; BINDING-SITES; Life Sciences & Biomedicine; nonhuman primate; MESSENGER-RNA; MATERNAL-BEHAVIOR; receptor binding; UPPER SPINAL-CORD; Neurosciences & Neurology; neuroanatomy
• Research Categories: Biology, Neuroscience; Sociology, Individual and Family Studies

Abstract

The coppery titi monkey (Callicebus cupreus) is a socially monogamous New World primate that has been studied in the field and the laboratory to investigate the behavioral neuroendocrinology of primate pair bonding and parental care. Arginine vasopressin has been shown to influence male titi monkey pair-bonding behavior, and studies are currently underway to examine the effects of oxytocin on titi monkey behavior and physiology. Here, we use receptor autoradiography to identify the distribution of arginine vasopressin 1a receptor (AVPR1a) and oxytocin receptors (OXTR) in hemispheres of titi monkey brain (n=5). AVPR1a are diffuse and widespread throughout the brain, but the OXTR distribution is much more limited, with the densest binding being in the hippocampal formation (dentate gyrus, CA1 field) and the presubiculum (layers I and III). Moderate OXTR binding was detected in the nucleus basalis of Meynert, pulvinar, superior colliculus, layer 4C of primary visual cortex, periaqueductal gray (PAG), pontine gray, nucleus prepositus, and spinal trigeminal nucleus. OXTR mRNA overlapped with OXTR radioligand binding, confirming that the radioligand was detecting OXTR protein. AVPR1a binding is present throughout the cortex, especially in cingulate, insular, and occipital cortices, as well as in the caudate, putamen, nucleus accumbens, central amygdala, endopiriform nucleus, hippocampus (CA4 field), globus pallidus, lateral geniculate nucleus, infundibulum, habenula, PAG, substantia nigra, olivary nucleus, hypoglossal nucleus, and cerebellum. Furthermore, we show that, in the titi monkey brain, the OXTR antagonist ALS-II-69 is highly selective for OXTR and that the AVPR1a antagonist SR49059 is highly selective for AVPR1a. Based on these results and the fact that both ALS-II-69 and SR49059 are non-peptide, small-molecule antagonists that should be capable of crossing the blood-brain barrier, these two compounds emerge as excellent candidates for the pharmacological manipulation of OXTR and AVPR1a in future behavioral experiments in titi monkeys and other primate species.