Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network

Albers, H. Elliott

doi:10.1016/j.yfrne.2014.07.001

Cited by 200Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyOlfactory and Sensory Function Studies

Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network

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Albers, H. Elliott·2015·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2014.07.001PMC PMC4317378

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Abstract

Arginine-vasotocin (AVT)/arginine vasopressin (AVP) are members of the AVP/oxytocin (OT) superfamily of peptides that are involved in the regulation of social behavior, social cognition and emotion. Comparative studies have revealed that AVT/AVP and their receptors are found throughout the "social behavior neural network (SBNN)" and display the properties expected from a signaling system that controls social behavior (i.e., species, sex and individual differences and modulation by gonadal hormones and social factors). Neurochemical signaling within the SBNN likely involves a complex combination of synaptic mechanisms that co-release multiple chemical signals (e.g., classical neurotransmitters and AVT/AVP as well as other peptides) and non-synaptic mechanisms (i.e., volume transmission). Crosstalk between AVP/OT peptides and receptors within the SBNN is likely. A better understanding of the functional properties of neurochemical signaling in the SBNN will allow for a more refined examination of the relationships between this peptide system and species, sex and individual differences in sociality.

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ERβ is one component of a "four-gene micronet" regulating social recognition via the PVN, amygdala, and olfactory system.
“ERβ has also been identified as one component of a “four-gene micronet” regulating social recognition (7, 131) via the PVN, amygdala, and olfactory system.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [7]
Section 2 describes a social-behavior neural network that includes the extended amygdala, is involved in social recognition, and includes the olfactory system as a key node in rodents. It does not identify ERβ as part of a four-gene micronet or describe that micronet as regulating recognition via the PVN, amygdala, and olfactory system; searches for ERβ and “micronet” found no supporting passage. Page numbers were not available in our copy. (LLM, conf=0.78)
Experimental — accuracy not yet measured
The neuroendocrine pathways coordinating numerous social traits are highly conserved, including the coordinating roles of AVP and OT.
“Although no animal model can fully capture the sophisticated complexity of human social behavior, the neuroendocrine pathways coordinating numerous social traits are highly conserved (7, 42), including the coordinating roles of AVP and OT.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [7]
By this model, estradiol simultaneously acts through ERβ in the PVN to increase OT, and ERα in the amygdala to increase OTR expression.
“By this model, estradiol simultaneously acts through ERβ in the PVN to increase OT, and ERα in the amygdala to increase OTR expression.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [7]
Section 5.1 discusses estradiol’s effects on the AVP system, while section 9.1.5 discusses OT receptors in the central amygdala; neither describes the proposed estradiol–ERβ–PVN–OT and estradiol–ERα–amygdala–OTR pathways. Searches for ERβ, estrogen receptor alpha, and the proposed pathways found no passage addressing that model. Page numbers were not available in our copy. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Different patterns of OT and AVP receptor activation across structures within these networks could contribute to the regulation of the complex behaviors and physiological processes under their control.
“Different patterns of OT and AVP receptor activation across structures within these networks could contribute to the regulation of the complex behaviors and physiological processes under their control (see [8] for a review).”
From Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery (2018) · cites this paper as [8]
Vasopressin modulates territorial behavior.
“Vasopressin modulates social communication, social investigation, territorial behavior, and aggression, predominantly in males.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]

Central vasopressin regulates social communication, territorial aggression, pair bonding, and mate guarding, especially in males.
“whereas central AVP has been shown to regulate social communication, territorial aggression, pair bonding, and mate guarding, especially in males (9,15,16).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]
Vasopressin modulates aggression, predominantly in males.
“Vasopressin modulates social communication, social investigation, territorial behavior, and aggression, predominantly in males.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]
Vasopressin modulates social communication.
“Vasopressin modulates social communication, social investigation, territorial behavior, and aggression, predominantly in males.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]
The behavioral effects of vasopressin are mediated primarily by V1aR and V1bR, while vasopressin acts on V2 to regulate fluid homeostasis in the kidney.
“The behavioral effects of AVP are mediated primarily by V1aR (or Avpr1a) and V1bR (16,37,38,49,68), while AVP acts on V2 to regulate fluid homeostasis in the kidney (69).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]
Vasopressin also plays a role in aggression in prairie voles and Syrian hamsters, sometimes in a sex-specific manner.
“AVP also plays a role in aggression in prairie voles and Syrian hamsters, sometimes in a sex-specific manner.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]
Pharmacological studies revealed that vasopressin in the anterior hypothalamus facilitates intermale aggression both in prairie voles and hamsters, while the opposite effect was found in female hamsters.
“For example, pharmacological studies revealed that AVP in the anterior hypothalamus facilitates intermale aggression both in prairie voles and hamsters (16,43,116), while the opposite effect was found in female hamsters (117).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [16]
OT and AVP regulate social behavior beyond the maternal context, including social attachments among adults, social cognition, and aggression.
“There is also a growing interest in OT and the related neurohypophyseal nonapetide arginine vasopressin (AVP) and their analogues in the regulation of social behavior beyond the maternal context, including social attachments among adults, social cognition, and aggression”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Albers, 2015
V1a-like receptors are the most common and widely distributed vasopressin receptor in the vertebrate brain.
“V1a-like receptors are the most common and widely distributed vasopressin receptor in the vertebrate brain (Albers, 2015)”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Albers, 2015
The distribution of OT-ergic and AVP-ergic neurons and cellular receptors for OT and AVP have been well characterized in rodents and other vertebrates, with substantial overlap with the social behavior network.
“The distribution of OT-ergic and AVP-ergic neurons, and cellular receptors for OT (OTR) and AVP (V1aR, V1bR, V2R) have been well characterized in rodents (Albers, 2015; Johnson and Young, 2015) and other vertebrates (Goodson and Kabelik, 2009; O’Connell and Hofmann, 2012, 2011), and this distribution includes substantial overlap with the social behavior network (SBN; Newman, 1999).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Albers, 2015
The important role of neuropeptide signaling in regulating a host of behavioral processes in invertebrate and especially vertebrate animals, especially in the social realm, has been firmly established.
“The important role of neuropeptide signaling in regulating a host of behavioral processes in invertebrate and especially vertebrate animals, especially in the social realm, has been firmly established (Albers, 2015; Caldwell and Young III, 2006; Donaldson and Young, 2008; Taghert and Nitabach, 2012; Wircer et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Albers, 2015
Many of the affected brain nuclei are part of the social behavioral network, which is comprised of interconnected nodes that express gonadal hormone receptors, appear to be influenced by oxytocin, and are important in the regulation of many types of social behaviors.
“What is particularly interesting about the aforementioned brain nuclei is that many of them are a part of the “social behavioral network,” which is comprised of neuroanatomical areas or “nodes” that are interconnected, express gonadal hormone receptors, appear to be influenced by Oxt, and are important in the regulation of many types of social behaviors (92, 93).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [93]

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Caldwell, H. K., & Young, W. S. (2006) · Handbook of Neurochemistry and Molecular Neurobiology · doi:10.1007/978-0-387-30381-9_25 · Cited by 113 · see citing works
A V1-like receptor mediates vasopressin-induced flank marking behavior in hamster hypothalamus
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Distribution of vasopressin and oxytocin binding sites in the brain and upper spinal cord of the common marmoset
Schorscher-Petcu, A., Dupré, A., & Tribollet, E. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.06.016 · Cited by 111 · see citing works
Vasopressin‐induced intracellular Ca2+ increase in isolated rat supraoptic cells.
Dayanithi, G., Widmer, H., & Richard, P. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021180 · Cited by 111 · see citing works
Physiology of invertebrate oxytocin and vasopressin neuropeptides
Gruber, C. W. (2014) · Experimental Physiology · doi:10.1113/expphysiol.2013.072561 · Cited by 110 · see citing works
Oxytocin Inhibits Aggression in Female Syrian Hamsters
Harmon, A. C., Huhman, K. L., Moore, T. O., & Albers, H. E. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00863.x · Cited by 108 · see citing works
Self-citation
Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus)
Buijs, R. M., Pévet, P., Masson‐Pévet, M., Pool, C. W., Vries, G. J. D., Canguilheim, B., & VIVIEN‐ROELS, B. (1986) · Brain Research · doi:10.1016/0006-8993(86)90829-2 · Cited by 106 · see citing works
Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty
Kelly, A. M., Kingsbury, M. A., Hoffbuhr, K., Schrock, S. E., Waxman, B., Kabelik, D., Thompson, R. R., & Goodson, J. L. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.01.012 · Cited by 106 · see citing works
Hormonal Basis of Social Conflict and Communication
Albers, H. E., Huhman, K. L., & Meisel, R. L. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50008-1 · Cited by 105 · see citing works
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Vasopressin in the septal area of the golden hamster controls scent marking and grooming
Irvin, R. W., Szot, P., Dorsa, D. M., Potegal, M., & Ferris, C. F. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90213-n · Cited by 105 · see citing works
Identification of multiple vasotocin receptor cDNAs in teleost fish: Sequences, phylogenetic analysis, sites of expression, and regulation in the hypothalamus and gill in response to hyperosmotic challenge
Lema, S. C. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.02.015 · Cited by 103 · see citing works
Double duty for sex differences in the brain
De Vries, G. J., & Boyle, P. A. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00192-7 · Cited by 103 · see citing works
Overview of cellular electrophysiological actions of vasopressin
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Of Domestic and Wild Guinea Pigs: Studies in Sociophysiology, Domestication, and Social Evolution
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Diurnal and Seasonal Rhythms of Neuronal Activity in the Suprachiasmatic Nucleus of Humans
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Quantitative Analysis of Oxytocin and Vasopressin Messenger Ribonucleic Acids in Single Magnocellular Neurons Isolated from Supraoptic Nucleus of Rat Hypothalamus
Xi, D., Kusano, K., & Gainer, H. (1999) · Endocrinology · doi:10.1210/endo.140.10.7054 · Cited by 101 · see citing works
The vasopressin 1b receptor and the neural regulation of social behavior
Stevenson, E. L., & Caldwell, H. K. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.009 · Cited by 100 · see citing works
Galanin immunoreactive neurons in the human hypothalamus: Colocalization with vasopressin‐containing neurons
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Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications
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Widespread release of peptides in the central nervous system: Quantitation of tannic acid‐captured exocytoses
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Evidence for the Co‐Expression of Oxytocin and Vasopressin Messenger Ribonucleic Acids in Magnocellular Neurosecretory Cells: Simultaneous Demonstration of Two Neurohypophysin Messenger Ribonucleic Acids by Hybridization Histochemistry
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Effect of photoperiod on vasopressin-induced aggression in Syrian hamsters
Caldwell, H. K., & Albers, H. E. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.04.006 · Cited by 97 · see citing works
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Evolutionary insights into the regulation of courtship behavior in male amphibians and reptiles
Woolley, S. C., Sakata, J. T., & Crews, D. P. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.021 · Cited by 97 · see citing works
Opposite effects of oxytocin and vasopressin on the emotional expression of the fear response
VIVIANI, D., & STOOP, R. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00418-4 · Cited by 96 · see citing works
Variation in the vasopressin V1a receptor promoter and expression: implications for inter‐ and intraspecific variation in social behaviour*
Hammock, E. A. D., & Young, L. J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02083.x · Cited by 95 · see citing works
Behavioural impact of intraseptally released vasopressin and oxytocin in rats
Englemann, M., Wotjak, C. T., Ebner, K., & Landgraf, R. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00015.x · Cited by 94 · see citing works
Differential routing of coexisting neuropeptides in vasopressin neurons
Landry, M., Vila‐Porcile, É., Hökfelt, T., & Calas, A. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02472.x · Cited by 93 · see citing works
Colocalization of γ‐aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus
Buijs, R. M., Wortel, J., & Hou, Y. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903580304 · Cited by 93 · see citing works
Dual modulation of inward rectifier potassium currents in olfactory neuronal cells by promiscuous G protein coupling of the oxytocin receptor
Gravati, M., Busnelli, M., Bulgheroni, E., Reversi, A., Spaiardi, P., Parenti, M. D., Toselli, M., & Chini, B. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06861.x · Cited by 92 · see citing works
A novel form of oxytocin in New World monkeys
Lee, A. G., Cool, D. R., Grunwald, W. C., Neal, D. E., Buckmaster, C. L., Cheng, M. Y., Hyde, S. A., Lyons, D. M., & Parker, K. J. (2011) · Biology Letters · doi:10.1098/rsbl.2011.0107 · Cited by 91 · see citing works
Oxytocin Receptor Binding in Female Prairie Voles: Endogenous and Exogenous Oestradiol Stimulation
Witt, D. M., Carter, C. S., & Lnsel, T. R. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00258.x · Cited by 91 · see citing works
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).
Wang, Z. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.2.305 · Cited by 91 · see citing works
Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes
Goodson, J. L., Evans, A. K., & Wang, Y. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.03.005 · Cited by 90 · see citing works
[3H]-[Thr4,Gly7]OT: a highly selective ligand for central and peripheral OT receptors
Elands, J., Barberis, C., & Jard, S. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.254.1.e31 · Cited by 88 · see citing works
Multiple mechanisms of phenotype development in the bluehead wrasse
Semsar, K., & Godwin, J. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.01.003 · Cited by 88 · see citing works
Vasopressin (V1a) Receptor Binding, mRNA Expression and Transcriptional Regulation by Androgen in the Syrian Hamster Brain
Young, L. J., Wang, Z., Cooper, T. T., & Albers, H. E. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00573.x · Cited by 88 · see citing works
Self-citation
Arginine‐vasopressin and the regulation of aggression in female Syrian hamsters (Mesocricetus auratus)
Gutzler, S. J., Karom, M., Erwin, W. D., & Albers, H. E. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07190.x · Cited by 86 · see citing works
Self-citation
Sexually dimorphic effects of a prenatal immune challenge on social play and vasopressin expression in juvenile rats
Taylor, P. V., Veenema, A. H., Paul, M. J., Bredewold, R., Isaacs, S., & de Vries, G. J. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-15 · Cited by 86 · see citing works
Vasopressin in the brain of the golden hamster: The distribution of vasopressin binding sites and of immunoreactivity to the vasopressin‐related glycopeptide
Dubois‐Dauphin, M., Pevet, P., Triboilet, E., & Dreif'Uss, J. J. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.903000408 · Cited by 85 · cited 1× · see citing works
“In Syrian hamsters, a relatively ‘‘asocial’’ species, there is a nearly complete lack of AVP containing cell bodies in the extended amygdala as well as an absence of AVP fibers in the LS (Dubois-Dauphin et al., 1990; Albers et al., 1991; Ferris et al., 1995).”
Background
The oxytocin/vasopressin receptor family has at least five members in the gnathostome lineage, inclucing two distinct V2 subtypes
Daza, D. O., Lewicka, M., & Larhammar, D. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.10.011 · Cited by 85 · see citing works
Distribution and developmental changes in vasopressin V2 receptor mRNA in rat brain
Kato, Y., Igarashi, N., Hirasawa, A., Tsujimoto, G., & Kobayashi, M. (1995) · Differentiation · doi:10.1046/j.1432-0436.1995.5930163.x · Cited by 82 · see citing works
Neuroendocrinology of social behavior
Adkins-Regan, E. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.5 · Cited by 81 · see citing works
The Vasopressin Receptors Colocalize with Vasopressin in the Magnocellular Neurons of the Rat Supraoptic Nucleus and Are Modulated by Water Balance
Hurbin, A., Orcel, H., Alonso, G., Moos, F., & Rabié, A. (2002) · Endocrinology · doi:10.1210/endo.143.2.8643 · Cited by 80 · see citing works
Effects of isolation/grouping on endocrine function and fighting behavior in male and female golden hamsters (Mesocricetus auratus waterhouse)
Brain, P. F. (1972) · Behavioral Biology · doi:10.1016/s0091-6773(72)80106-8 · Cited by 79 · see citing works
Role of V1a vasopressin receptors in the control of aggression in Syrian hamsters
Elliott Albers, H., Dean, A., Karom, M. C., Smith, D., & Huhman, K. L. (2006) · Brain Research · doi:10.1016/j.brainres.2005.12.081 · Cited by 78 · see citing works
Distribution and developmental change of vasopressin V1A and V2 receptor mRNA in rats
Hirasawa, A., Hashimoto, K., & Tsujimoto, G. (1994) · European Journal of Pharmacology Molecular Pharmacology · doi:10.1016/0922-4106(94)90226-7 · Cited by 78 · see citing works
A polymorphic indel containing the RS3 microsatellite in the 5′ flanking region of the vasopressin V1a receptor gene is associated with chimpanzee (Pan troglodytes) personality
Hopkins, W. D., Donaldson, Z. R., & Young, L. J. (2012) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2012.00799.x · Cited by 78 · see citing works
Distribution of vasopressin and oxytocin receptors in the rat spinal cord: sex-related differences and effect of castration in pudendal motor nuclei
Tribollet, E., Barberis, C., & Arsenijévic, Y. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00591-x · Cited by 76 · see citing works

Flagged first, then by citations

2 of the 334 references couldn’t be matched to a known paper.

Research works printed but not linked: 3

Bales KL Plotsky PM Young LJ Lim MM Grotte N Ferrer E Carter CS Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors Neuroscience 2007b 144 1 38 45 17055176 PMC1774559
Dhakar MB Stevenson EL Caldwell HK Choleris E Pfaff DW Kavaliers M Oxytocin, vasopressin, and their interplay with gonadal hormones Oxytocin, vasopressin and related peptides in the regulation of behavior 2013 Cambridge: Cambridge 3 26
Maruska KP Mizobe MH Tricas TC Sex and seasonal co-variation of arginine vasotocin (AVT) and gonadotropin-releasing hormone (GnRH) neurons in the brain of the halfspotted goby Comp Biochem Physiol A Mol Integr Physiol 2007b 147 1 129 144 17276115

Sorted by citations

Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“…neuropeptides vasopressin (VP) and oxytocin (OT) are involved in the regulation of diverse social behaviors such as social recognition, pair-bonding, and social cognition in mammals, including humans (Veenema & Neumann, 2008; Ross & Young, 2009; MeyerLindenberg et al., 2011; Albers, 2014).”
BackgroundInfluential
Is oxytocin “nature’s medicine”
Carter, C. S., Kenkel, W. M., MacLean, E. L., Wilson, S. R., Perkeybile, A. M., Yee, J. R., Ferris, C. F., Nazarloo, H. P., Porges, S. W., Davis, J. M., et al. (2020) · Pharmacological Reviews · doi:10.1124/pr.120.019398 · Cited by 394 · see citing works
Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery
Song, Z., & Albers, H. E. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.10.004 · Cited by 244 · see citing works
Self-citation
Oxytocin and vasopressin neural networks: Implications for social behavioral diversity and translational neuroscience
Johnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242 · see citing works
Oxytocin and vasopressin: powerful regulators of social behavior
Caldwell, H. K. (2017) · The Neuroscientist · doi:10.1177/1073858417708284 · Cited by 216 · see citing works
Amygdala, neuropeptides, and chronic pain-related affective behaviors
Neugebauer, V., Mazzitelli, M., Cragg, B., Ji, G., Navratilova, E., & Porreca, F. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108052 · Cited by 216 · see citing works
Status-Dependent Vasotocin Modulation of Dominance and Subordination in the Weakly Electric Fish Gymnotus omarorum
Perrone, R., & da Silva, A. C. R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00001 · Cited by 210 · see citing works
Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
Rigney, N., de Vries, G. J., Petrulis, A., & Young, L. J. (2022) · Endocrinology · doi:10.1210/endocr/bqac111 · Cited by 191 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
The Oxytocin–Vasopressin Pathway in the Context of Love and Fear
Carter, C. S. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00356 · Cited by 162 · see citing works
Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues
Yao, S., Bergan, J., Lanjuin, A., & Dulac, C. (2017) · eLife · doi:10.7554/elife.31373 · Cited by 151 · see citing works
Age and sex differences in oxytocin and vasopressin V1a receptor binding densities in the rat brain: focus on the social decision-making network
Smith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1260-7 · Cited by 143 · see citing works
The neuroscience of social feelings: mechanisms of adaptive social functioning
Eslinger, P. J., Anders, S., Ballarini, T., Boutros, S., Krach, S., Mayer, A. V., Moll, J., Newton, T. L., Schroeter, M. L., de Oliveira-Souza, R., et al. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.028 · Cited by 130 · see citing works
Oxytocin, vasopressin, and the motivational forces that drive social behaviors
Caldwell, H. K., & Albers, H. E. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_390 · Cited by 129 · see citing works
Self-citation
Serotonin and arginine–vasopressin mediate sex differences in the regulation of dominance and aggression by the social brain
Terranova, J. I., Song, Z., Larkin, T. E., Hardcastle, N., Norvelle, A., Riaz, A., & Albers, H. E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610446113 · Cited by 123 · see citing works
Self-citation
Sex-dependent regulation of social reward by oxytocin: an inverted U hypothesis
Borland, J. M., Rilling, J. K., Frantz, K. J., & Albers, H. E. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-018-0129-2 · Cited by 116 · see citing works
Self-citation
The dynamics of GABA signaling: Revelations from the circadian pacemaker in the suprachiasmatic nucleus
Albers, H. E., Walton, J. C., Gamble, K. L., McNeill, J. K., & Hummer, D. L. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.11.003 · Cited by 113 · see citing works
Self-citation
Behavioural, hormonal and neurobiological mechanisms of aggressive behaviour in human and nonhuman primates
de Almeida, R. M. M., Cabral, J. C. C., & Narvaes, R. F. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.02.053 · Cited by 108 · see citing works
The Role of Oxytocin and Vasopressin in Attachment
Carter, C. S. (2017) · Psychodynamic Psychiatry · doi:10.1521/pdps.2017.45.4.499 · Cited by 105 · see citing works
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
Song, Z., Borland, J. M., Larkin, T. E., O’Malley, M., & Albers, H. E. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.001 · Cited by 101 · see citing works
Self-citation
Arginine vasopressin (AVP): a review of its historical perspectives, current research and multifunctional role in the hypothalamo-hypophysial system
Rotondo, F., Butz, H., Syro, L. V., Yousef, G. M., Di Ieva, A., Restrepo, L. M., Quintanar-Stephano, A., Berczi, I., & Kovacs, K. (2016) · Pituitary · doi:10.1007/s11102-015-0703-0 · Cited by 93 · see citing works
Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses
Zuloaga, D. G., Heck, A., Guzman, R. M. D., & Handa, R. J. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-00319-2 · Cited by 96 · see citing works
Sex differences in the regulation of offensive aggression and dominance by arginine-vasopressin
Terranova, J. I., Ferris, C. F., & Albers, H. E. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00308 · Cited by 85 · see citing works
Self-citation
The Monogamy Paradox: What Do Love and Sex Have to Do With It?
Carter, C. S., & Perkeybile, A. M. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00202 · Cited by 85 · see citing works
Oxytocin and behavior: lessons from knockout mice
Caldwell, H. K., Aulino, E. A., Freeman, A. R., Miller, T. V., & Witchey, S. K. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22431 · Cited by 79 · see citing works
Oxytocin during Development: Possible Organizational Effects on Behavior
Miller, T. V., & Caldwell, H. K. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00076 · Cited by 79 · see citing works
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 72 · see citing works
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 · see citing works
“Vasopressin (AVP) and oxytocin (OT) have garnered considerable attention for their essential role in the regulation of various social behaviors in humans, rodents, and other animals (reviewed in Veenema & Neumann, 2008; Ross & Young, 2009; Heinrichs, von Dawans, & Domes, 2009; Albers, 2015; Caldwell & Albers, 2015).”
Background
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
The Biology of Vasopressin
Sparapani, S., Millet-Boureima, C., Oliver, J., Mu, K., Hadavi, P., Kalostian, T., Ali, N., Avelar, C. M., Bardies, M., Barrow, B., et al. (2021) · Biomedicines · doi:10.3390/biomedicines9010089 · Cited by 63 · see citing works
Navigating Monogamy: Nonapeptide Sensitivity in a Memory Neural Circuit May Shape Social Behavior and Mating Decisions
Ophir, A. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00397 · Cited by 62 · see citing works
Modulation of social behavior by distinct vasopressin sources
Rigney, N., Vries, G. J. D., & Petrulis, A. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1127792 · Cited by 61 · see citing works
Comparing vasopressin and oxytocin fiber and receptor density patterns in the social behavior neural network: implications for cross-system signaling
Smith, C. J. W., DiBenedictis, B. T., & Veenema, A. H. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.001 · Cited by 59 · see citing works
Brain transcriptomics of agonistic behaviour in the weakly electric fish Gymnotus omarorum, a wild teleost model of non-breeding aggression
Eastman, G., Valiño, G., Radío, S., Young, R. L., Quintana, L., Zakon, H. H., Hofmann, H. A., Sotelo-Silveira, J. R., & da Silva, A. C. R. (2020) · Scientific Reports · doi:10.1038/s41598-020-66494-9 · Cited by 59 · see citing works
Sex-dependent effects of social isolation on the regulation of arginine-vasopressin (AVP) V1a, oxytocin (OT) and serotonin (5HT) 1a receptor binding and aggression
Ross, A. P., McCann, K. E., Larkin, T. E., Song, Z., Grieb, Z. A., Huhman, K. L., & Albers, H. E. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104578 · Cited by 57 · see citing works
Self-citation
Social instability stress in adolescent male rats reduces social interaction and social recognition performance and increases oxytocin receptor binding
Hodges, T. E., Baumbach, J. L., Marcolin, M. L., Bredewold, R., Veenema, A. H., & McCormick, C. M. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.07.032 · Cited by 56 · see citing works
Animal models of endocrine disruption
Patisaul, H. B., Fenton, S. E., & Aylor, D. L. (2018) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2018.03.011 · Cited by 57 · see citing works
Endocrine Disruption of Vasopressin Systems and Related Behaviors
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“The anatomical and functional features of AVP/ OT neuronal subpopulations are beyond the scope of this review and detailed elsewhere (6, 7).”
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Authors: Albers, H. E.
Affiliations: Georgia State University (US)
Corresponding author: Albers, H. Elliott
ORCID: Albers, H. Elliott
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2015-01
Volume: 36
Pages: 49-71
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2014.07.001
PMC: PMC4317378
OpenAlex: W2007630334
Cited by: 200
References: 334
Citations by year: 2026: 17 · 2025: 11 · 2024: 12 · 2023: 8 · 2022: 12 · 2021: 14 · 2020: 19 · 2019: 13 · 2018: 33 · 2017: 26 · 2016: 24 · 2015: 11
FWCI: 2.91
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Frontiers in Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIH
NSF (IOS-092330)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Keywords: arginine vasotocin, vasopressin, oxytocin, social behavior, species differences, sex differences, individual differences, volume transmission, CO release, peptide receptors, gonadal hormones, sociality
MeSH terms: Animals, Brain, Humans, Individuality, Nerve Net, Sex Characteristics, Social Behavior, Species Specificity, Vasopressins, Vasotocin, Signal Transduction

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Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network

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