Cited by 59Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyNeurotransmitter Receptor Influence on Behavior

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Comparing vasopressin and oxytocin fiber and receptor density patterns in the social behavior neural network: Implications for cross-system signaling

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Smith, Caroline J.W., DiBenedictis, Brett T., Veenema, Alexa H.·2019·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2019.02.001PMC PMC7469073

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Abstract

Vasopressin (AVP) and oxytocin (OXT) regulate social behavior by binding to their canonical receptors, the vasopressin V1a receptor (V1aR) and oxytocin receptor (OTR), respectively. Recent studies suggest that these neuropeptides may also signal via each other's receptors. The extent to which such cross-system signaling occurs likely depends on anatomical overlap between AVP/OXT fibers and V1aR/OTR expression. By comparing AVP/OXT fiber densities with V1aR/OTR binding densities throughout the rat social behavior neural network (SBNN), we propose the potential for cross-system signaling in four regions: the medial amygdala (MeA), bed nucleus of the stria terminalis (BNSTp), medial preoptic area, and periaqueductal grey. We also discuss possible implications of corresponding sex (higher in males versus females) and age (higher in adults versus juveniles) differences in AVP fiber and OTR binding densities in the MeA and BNSTp. Overall, this review reveals the need to unravel the consequences of potential cross-system signaling between AVP and OXT systems in the SBNN for the regulation of social behavior.

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Vasopressin regulates social recognition in juvenile and adult rats of both sexes, but in sex- and age-specific ways
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Oxytocin, vasopressin, and the motivational forces that drive social behaviors
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Sex differences in vasopressin neurons in the bed nucleus of the stria terminalis by in situ hybridization
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Sexually dimorphic expression of oxytocin binding sites in forebrain and spinal cord of the rat
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Decline of vasopressin immunoreactivity and mRNA levels in the bed nucleus of the stria terminalis following castration
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Early life stress impairs social recognition due to a blunted response of vasopressin release within the septum of adult male rats
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Topography of the oxytocin receptor system in rat brain: an autoradiographical study with a selective radioiodinated oxytocin antagonist.
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Site of origin of and sex differences in the vasopressin innervation of the mouse ( Mus musculus ) brain
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“…et al., 1981; Caffe et al., 1987) as well as of other rodent species with higher AVP-ir fiber density in adult males versus adult females in mice (Rood et al., 2013), gerbils (Crenshaw et al., 1992), European hamsters (Buijs et al., 1986) and prairie, pine, meadow and montane voles (Table 2;…”
Background
Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis
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Oxytocin but not vasopressin facilities social recognition following injection into the medial preoptic area of the rat brain
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Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor
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Extrahypothalamic vasopressin and oxytocin in the human brain; presence of vasopressin cells in the bed nucleus of the stria terminalis
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A V1-like receptor mediates vasopressin-induced flank marking behavior in hamster hypothalamus
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Human Myometrium during Pregnancy Contains and Responds to VI Vasopressin Receptors as well as Oxytocin Receptors*
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Oxytocin induces social communication by activating arginine-vasopressin V1a receptors and not oxytocin receptors
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Medial preoptic area oxytocin and female sexual receptivity.
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Changes in the intensity of maternal aggression and central oxytocin and vasopressin V1a receptors across the peripartum period in the rat
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Sex Differences in Vasopressin and Other Neurotransmitter Systems in the Brain
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Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus)
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Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions
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Coping with stress in rats and mice: Differential peptidergic modulation of the amygdala-lateral septum complex
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Sexual dimorphism in the vasotocin system of the bullfrog (Rana catesbeiana)
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Species differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus).
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Sexually dimorphic effects of a prenatal immune challenge on social play and vasopressin expression in juvenile rats
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Oxytocin receptor dynamics in the brain across development and species
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Vasopressin in the brain of the golden hamster: The distribution of vasopressin binding sites and of immunoreactivity to the vasopressin‐related glycopeptide
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Comparative analysis of the vasotocinergic and mesotocinergic cells and fibers in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii
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A radioiodinated linear vasopressin antagonist: A ligand with high affinity and specificity for V1a receptors
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Autoradiographic localization of V1 vasopressin binding sites in rat brain and kidney
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Immunocytochemical demonstration of vasopressin and oxytocin in the rat brain by light and electron microscopy.
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Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice
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Histoautoradiographic detection of oxytocin‐ and vasopressin‐binding sites in the telencephalon of the rat
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Involvement of the oxytocin system in the bed nucleus of the stria terminalis in the sex-specific regulation of social recognition
Dumais, K. M., Alonso, A. G., Immormino, M. A., Bredewold, R., & Veenema, A. H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.007 · Cited by 79
Social Novelty Investigation in the Juvenile Rat: Modulation by the μ‐Opioid System
Smith, C. J. W., Wilkins, K. B., Mogavero, J. N., & Veenema, A. H. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12301 · Cited by 77
Androgen and Estrogen Effects on Vasopressin Messenger RNA Expression in the Medial Amygdaloid Nucleus in Male and Female Rats
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Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice
Ho, J. M., Murray, J. H., Demas, G. E., & Goodson, J. L. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.021 · Cited by 76
The distribution of hypothalamic and extrahypothalamic vasotocinergic cells and fibers in the brain of a lizard, Gekko gecko: Presence of a sex difference
Stoll, C., & Voorn, P. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902390206 · Cited by 74
Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network
DiBenedictis, B. T., Nussbaum, E. R., Cheung, H. K., & Veenema, A. H. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24216 · Cited by 74 · cited 41×
“We chose to focus on the adult male rat because of available data on AVP and OXT fiber densities as well as V1aR and OTR binding densities (DiBenedictis et al., 2017; Smith et al., 2017) and the well-known roles of AVP/OXT and their receptors in regulating diverse social behaviors in adult male…”
BackgroundMethodResultInfluential
Are age and sex differences in brain oxytocin receptors related to maternal and infanticidal behavior in naïve mice?
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Sex differences in the brain of goldfish: gonadotropin-releasing hormone and vasotocinergic neurons
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Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat
Gil, M., Bhatt, R., Picotte, K. B., & Hull, E. M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.12.012 · Cited by 70 · cited 1×
“In the MPOA, OXT administration facilitates both sexual behavior (Gil et al., 2011) and social recognition (Popik & van Ree, 1991) in adult male rats.”
Method
Oxytocin–Oxytocin Receptor Systems Facilitate Social Defeat Posture in Male Mice
Nasanbuyan, N., Yoshida, M., Takayanagi, Y., Inutsuka, A., Nishimori, K., Yamanaka, A., & Onaka, T. (2017) · Endocrinology · doi:10.1210/en.2017-00606 · Cited by 70
Vasopressin Differentially Modulates Non-NMDA Receptors in Vasopressin and Oxytocin Neurons in the Supraoptic Nucleus
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Activation of Supraoptic Oxytocin Neurons by Secretin Facilitates Social Recognition
Takayanagi, Y., Yoshida, M., Takashima, A., Takanami, K., Yoshida, S., Nishimori, K., Nishijima, I., Sakamoto, H., Yamagata, T., & Onaka, T. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.11.021 · Cited by 69
Oxytocin and vasopressin flatten dominance hierarchy and enhance behavioral synchrony in part via anterior cingulate cortex
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Differential expression of oxytocin receptor mRNA in the developing rat brain
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Binding of the Non-Peptide Vasopressin V1a Receptor Antagonist SR-49059 in the Rat Brain: An in vitro and in vivo Autoradiographic Study
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Castration reduces vasopressin receptor binding in the hamster hypothalamus
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Comparative Analysis of Vasotocin-Like Immunoreactivity in the Brain of the Turtle Pseudemys scripta elegan s and the Snake Python regius (Part 1 of 2)
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Sex differences among oxytocin-immunoreactive neuronal systems in the mouse hypothalamus.
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Vasopressin, gonadal steroids and social recognition
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Insights into the molecular evolution of oxytocin receptor ligand binding
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The distribution of an AVT V1a receptor in the brain of a sex changing fish, Epinephelus adscensionis
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Ontogeny of vasopressin and oxytocin binding sites in the brain of Wistar and Brattleboro rats as demonstrated by lightmicroscopical autoradiography.
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Mesotocin and vasotocin in the brain of the lizard Gekko gecko
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Seasonal changes in vasopressin in the brain of the garden dormouse (Eliomys quercinus L.)
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Vasopressin and oxytocin excite MCH neurons, but not other lateral hypothalamic GABA neurons
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Oxytocin in the periaqueductal grey regulates nociception in the rat
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Oxytocin (OT) and arginine-vasopressin (AVP) act on OT receptors and not AVP V1a receptors to enhance social recognition in adult Syrian hamsters (Mesocricetus auratus)
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Appearance and Transient Expression of Vasopressin and Oxytocin Receptors in the Rat Brain
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Effects of lordosis-relevant neuropeptides on midbrain periaqueductal gray neuronal activity in vitro
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Neonatal Gonadectomy and Adult Testosterone Replacement Suggest an Involvement of Limbic Arginine Vasopressin and Androgen Receptors in the Organization of the Hypothalamic-Pituitary-Adrenal Axis
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Septal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles
Anacker, A. M. J., Christensen, J. D., LaFlamme, E. M., Grunberg, D. M., & Beery, A. K. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.02.025 · Cited by 44
The role of the vasopressin V1A receptor in oxytocin modulation of methamphetamine primed reinstatement
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Extending the socio-sexual brain: arginine-vasopressin immunoreactive circuits in the telencephalon of mice
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Authors: Smith, C. J. W., DiBenedictis, B. T., & Veenema, A. H.
Affiliations: Boston College (US)
Corresponding author: Smith, Caroline J.W.
ORCID: Smith, Caroline J.W.
DiBenedictis, Brett T.
Veenema, Alexa H.
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2019-04
Volume: 53
Pages: 100737
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2019.02.001
PMC: PMC7469073
OpenAlex: W2911777171
Cited by: 59
References: 222
Citations by year: 2026: 5 · 2025: 10 · 2024: 3 · 2023: 4 · 2022: 6 · 2021: 9 · 2020: 19 · 2019: 3
FWCI: 1.43
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (am, 419 d)
Locations: Frontiers in Neuroendocrinology (acceptedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (R01MH102456)
National Science Foundation (IOS1253385)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: vasopressin, oxytocin, vasopressin V1a receptor, oxytocin receptor, receptor binding density, medial amygdala, bed nucleus of the stria terminalis, medial preoptic area, periaqueductal gray, sex differences, age differences, rats
MeSH terms: Animals, Humans, Nerve Net, Oxytocin, Social Behavior, Vasopressins, Receptors, Vasopressin, Receptors, Oxytocin

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Comparing vasopressin and oxytocin fiber and receptor density patterns in the social behavior neural network: Implications for cross-system signaling

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