Cited by 153Neuroendocrine regulation and behaviorPrimate Behavior and EcologyNeuropeptides and Animal Physiology

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

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Freeman, S.M., Walum, H., Inoue, K., Smith, A.L., Goodman, M.M., Bales, K.L., Young, L.J.·2014·Neuroscience

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.

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Crossref · 10.1016/j.neuroscience.2014.04.055

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  • OT receptors are concentrated in cholinergic brain regions regulating visual and auditory attention in nonhuman primates.

    “OT receptors are concentrated in cholinergic brain regions regulating visual and auditory attention in nonhuman primates (6, 42, 43)”

    From Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies (2016) · cites this paper as [43]

    Discussion §4.2 reports OXTR in the nucleus basalis of Meynert across several primates and identifies it as important for visual attention; §4.5 says OXTR is consistently concentrated in visual-processing and attention areas. The paper does not establish that OXTR is concentrated in cholinergic regions regulating auditory attention. Its mention of audition in §4.5 concerns a broader evolutionary shift in social-information processing, not auditory attention. (LLM, conf=0.84)

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  • The optimized and reliable method for measuring OXTR and AVPR1a has been previously validated in nonhuman primate and human brain tissue to selectively reveal OXTR or AVPR1a.

    “we measured both OXTR and AVPR1a with an optimized and reliable method previously validated in nonhuman primate and human brain tissue34,37,38.”
  • OXT acting at OXTR in the NBM could modulate the activity of an extensive network of brain areas and influence social behavioral processes like social visual attention, gaze direction, and social decision making.

    “Based on this connectivity of the NBM, we and others have postulated that OXT acting at OXTR in the NBM could modulate the activity of an extensive network of brain areas (which may themselves lack OXTR) and influence social behavioral processes like social visual attention, gaze direction, and social decision making38,39,64,65.”
  • Monogamous titi monkeys have remarkably dense oxytocin receptor binding in the dentate gyrus of the hippocampus.

    “In monogamous titi monkeys, there is remarkably dense OXTR binding in the dentate gyrus of the hippocampus (35), although the function of this population of OXTR is unknown.”
  • The authors mapped oxytocin receptors and vasopressin receptor 1a in the brain of the socially monogamous coppery titi monkey.

    “Additionally, we have mapped OXTR and AVPR1a in the brain of the socially monogamous coppery titi monkey (Callicebus cupreus) (35).”

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References 72 · Cited by 153

Research works printed but not linked: 1

  1. Manocha SL Shantha TR Bourne GH 1968 A stereotaxic atlas of the brain of the Cebus monkey (Cebus apella) Clarendon Press

Authors
Freeman, S. M., Walum, H., Inoue, K., Smith, A. L., Goodman, M. M., Bales, K. L., & Young, L. J.
Affiliations
  • Emory University (US)
  • University of California, Davis (US)
Corresponding author
Freeman, S.M.
Venue
Neuroscience
Publisher
Elsevier BV
Published
2014-07
Volume
273
Pages
12-23
ISSN
0306-4522 (ISSN-L)
OpenAlex
W2078245733
Cited by
153
References
72
Citations by year
2026: 4 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 9 · 2021: 14 · 2020: 24 · 2019: 5 · 2018: 24 · 2017: 15 · 2016: 24 · 2015: 13 · 2014: 5
FWCI
28.19
Type
journal article
Language
en
Open access
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
Funders
  • National Institutes of Health (5t32mh073525-05, P51OD011107, P51OD011132)
  • National Institute of Mental Health (T32-MH073525, R21MH090776, T32MH073525-06, P50MH100023, MH090776)
  • National Center for Research Resources (P51RR000165)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD053555, HD053555)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords
oxytocin receptor, Callicebus cupreus, pair bonding, receptor distribution, vasopressin receptor antagonists, neuroendocrinology, hippocampus, presubiculum
MeSH terms
Acetylcholine, Animals, Autoradiography, Brain, Female, Indoles, Male, Pair Bond, Pyrrolidines, RNA, Messenger, Species Specificity, Quinolones, In Situ Hybridization, Receptors, Vasopressin, Receptors, Oxytocin, Pitheciidae, Antidiuretic Hormone Receptor Antagonists

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