The Challenge of Translation in Social Neuroscience: A Review of Oxytocin, Vasopressin, and Affiliative Behavior

Insel, Thomas R.

doi:10.1016/j.neuron.2010.03.005

Cited by 1,044Neuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on BehaviorHuman-Animal Interaction Studies

The Challenge of Translation in Social Neuroscience: A Review of Oxytocin, Vasopressin, and Affiliative Behavior

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Insel, Thomas R.·2010·Neuron

DOI 10.1016/j.neuron.2010.03.005PMC PMC2847497

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Abstract

Social neuroscience is rapidly exploring the complex territory between perception and action where recognition, value, and meaning are instantiated. This review follows the trail of research on oxytocin and vasopressin as an exemplar of one path for exploring the "dark matter" of social neuroscience. Studies across vertebrate species suggest that these neuropeptides are important for social cognition, with gender- and steroid-dependent effects. Comparative research in voles yields a model based on interspecies and intraspecies variation of the geography of oxytocin receptors and vasopressin V1a receptors in the forebrain. Highly affiliative species have receptors in brain circuits related to reward or reinforcement. The neuroanatomical distribution of these receptors may be guided by variations in the regulatory regions of their respective genes. This review describes the promises and problems of extrapolating these findings to human social cognition, with specific reference to the social deficits of autism.

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In animals, oxytocin increases social approach and social memory, both of which are impaired in persons with autism.
“In animals, oxytocin increases social approach and social memory,1 both of which are impaired in persons with autism.”
From Intranasal Oxytocin in Children and Adolescents with Autism Spectrum Disorder (2021) · cites this paper as [1]
OXT promotes the formation of pair-bonds in females, while arginine vasopressin is more important in males.
“Research on monogamous mammals, particularly prairie voles, has shown that the neuropeptide oxytocin (OXT) promotes the formation of pair-bonds in females, with a related peptide, argininevasopressin being more important in males (Donaldson and Young, 2008;Insel, 2010).”
From Oxytocin Modulates Social Distance between Males and Females (2012) · cites this paper as Insel, 2010
The oxytocin receptor has long been associated with the display of social behavior in rodents.
“The last candidate gene we examined, the oxytocin receptor, has long been associated with the display of social behavior in rodents [34].”
From Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice (2011) · cites this paper as [34]
These studies suggest that oxytocin facilitates affiliation and social attachment.
“These studies suggest that oxytocin facilitates affiliation and social attachment [548].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [548]
A contributive mechanism regulating in-group cooperation during intergroup conflicts in humans involves the neuropeptide hormone oxytocin.
“Studies suggest that a contributive mechanism regulating in-group cooperation during intergroup conflicts in humans involves the neuropeptide hormone oxytocin, known to influence trust, coordination, and social cognition, although evidence from natural settings is lacking.”
From Oxytocin reactivity during intergroup conflict in wild chimpanzees (2017) · cites this paper as [6]

The interface between oxytocin and the dopaminergic reward system may contribute to the success of mother-infant and pair-bonding processes.
“It is thought that the interface between oxytocin and the dopaminergic reward system may contribute to the success of mother-infant and pair-bonding processes [18,[75][76][77].”
From Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees (2014) · cites this paper as [18]
Oxytocin receptor distributions are highly variable across species, and to some extent within species.
“However, oxytocin receptor distributions are highly variable across species, and to some extent within species (Insel, 2010), suggesting considerable functional variation is likely between species (Goodson and Thompson, 2010) and within species (Insel, 2010).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Insel, 2010
Considerable functional variation in oxytocin is likely between species and within species.
“However, oxytocin receptor distributions are highly variable across species, and to some extent within species (Insel, 2010), suggesting considerable functional variation is likely between species (Goodson and Thompson, 2010) and within species (Insel, 2010).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Insel, 2010
Oxytocin facilitates social cognition, enhances social memory, social recognition and attention, and operates in the reward centers of the brain.
“Furthermore, it facilitates social cognition, enhances social memory, social recognition and attention, and operates in the reward centers of the brain (Insel, 2010).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Insel, 2010
This is potentially a crucial feature of social bond formation and maintenance.
“This is potentially a crucial feature of social bond formation and maintenance (Broad et al., 2006; Insel, 2010).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Insel, 2010
Systemic loss of oxytocin or oxytocin receptors disrupts maternal nurturing behaviours in mice.
“Systemic loss of either oxytocin or oxytocin receptors (Oxt−/− and Oxtr−/−) disrupts maternal nurturing behaviours in mice7,8.”
From Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice (2019) · cites this paper as [7]
Clinical studies have linked autism and Asperger's disorders and attention-deficit/hyperactivity disorders to oxytocin deficiency.
“Clinical studies have linked autism and Asperger’s disorders and attention-deficit/hyperactivity disorders to oxytocin deficiency7,8,54, and the potential use of exogenous oxytocin to treat these conditions is being assessed in clinical trials10,11,54–57.”
From Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice (2019) · cites this paper as [7]
Oxytocin is crucial in many aspects of social behavior, including affiliation and reward.
“This neuropeptide is crucial in many aspects of social behavior, including affiliation6 and reward.7”
From Enhancement of anandamide-mediated endocannabinoid signaling corrects autism-related social impairment (2016) · cites this paper as [6]
OT appears to rescue some social deficits in individuals with psychopathological conditions.
“One of the most exciting findings from recent OT studies is that the peptide appears to rescue some social deficits in individuals with psychopathological conditions (for a review, see: Insel, 2010; Meyer-Lindenberg et al., 2011).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Insel, 2010

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Forebrain peptides modulate sexually polymorphic vocal circuitry
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Molecular cloning, sequencing, and functional expression of a cDNA encoding the human V1a vasopressin receptor.
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Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli
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Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism
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Post-learning intranasal oxytocin modulates human memory for facial identity
Savaskan, E., Ehrhardt, R., Schulz, A., Walter, M., & Schächinger, H. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.12.004 · Cited by 262 · see citing works
Actions of Estrogens and Progestins on Nerve Cells
Pfaff, D. W., & McEwen, B. S. (1983) · Science · doi:10.1126/science.6297008 · Cited by 260 · see citing works
Mesotocin and nonapeptide receptors promote estrildid flocking behavior
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Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills.
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Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata
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Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans
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An intrinsic vasopressin system in the olfactory bulb is involved in social recognition
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The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice
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Functional Magnetic Resonance Imaging Shows Oxytocin Activates Brain Regions Associated with Mother–Pup Bonding during Suckling
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Species differences in V₁a receptor gene expression in monogamous and nonmonogamous voles: Behavioral consequences.
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Association of the oxytocin receptor (OXTR) gene polymorphisms with autism spectrum disorder (ASD) in the Japanese population
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Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats
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“Adult virgin females primed with estrogen and injected centrally with OT were reported to exhibit full maternal behavior, including nest building and crouching over pups in a nursing posture (Fahrbach et al., 1984; Pedersen et al., 1982; although also see Rubin et al., 1983).”
Oxytocin Facilitation of Maternal Behavior in Sheepa
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Genome-wide and Ordered-Subset linkage analyses provide support for autism loci on 17q and 19p with evidence of phenotypic and interlocus genetic correlates
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Regional Changes in Brain Oxytocin Receptors Post‐Partum: Time‐Course and Relationship to Maternal Behaviour
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Anatomy and neurochemistry of the pair bond
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Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex
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Sex, parturition and motherhood without oxytocin?
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Receptor and behavioral pharmacology of WAY-267464, a non-peptide oxytocin receptor agonist
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Structural and functional evolution of the vasopressin/oxytocin superfamily: vasopressin-related conopressin is the only member present in Lymnaea, and is involved in the control of sexual behavior
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Neuropeptides and the social brain: potential rodent models of autism
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Infant's response to social separation reflects adult differences in affiliative behavior: A comparative developmetal study in prairie and montane voles
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Evolution of the vasopressin/oxytocin superfamily: characterization of a cDNA encoding a vasopressin-related precursor, preproconopressin, from the mollusc Lymnaea stagnalis.
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Molecular genetic studies of the arginine vasopressin 1a receptor (AVPR1a) and the oxytocin receptor (OXTR) in human behaviour: from autism to altruism with some notes in between
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Dopamine regulation of social choice in a monogamous rodent species
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Co-evolution of Ligand-Receptor Pairs in the Vasopressin/Oxytocin Superfamily of Bioactive Peptides
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Distribution of vasopressin and oxytocin binding sites in the brain and upper spinal cord of the common marmoset
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The effects of peptides on partner preference formation are predicted by habitat in prairie voles
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A genome-wide search for alleles and haplotypes associated with autism and related pervasive developmental disorders on the Faroe Islands
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The Neurobiology of Social Bonds
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A genomic element within the third intron of the human oxytocin receptor gene may be involved in transcriptional suppression
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Intracerebroventricular administration of oxytocin and maternal behavior in rats after prolonged and acute steroid pretreatment
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Vasopressin in the forebrain of common marmosets (Callithrix jacchus): studies with in situ hybridization, immunocytochemistry and receptor autoradiography
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Dopamine and monogamy
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Oxytocin receptors in brain cortical regions are reduced in haploinsufficient (+/−) reeler mice
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Chapter 4 Oxytocin: who needs it?
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Evolution of a behavior-linked microsatellite-containing element in the 5' flanking region of the primate AVPR1A gene
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On switches and knobs, microsatellites and monogamy
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Neuropeptides and non‐human primate social deficits associated with pathogenic rearing experience
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What's in a Face?
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Targeted Reduction of Oxytocin Expression Provides Insights into its Physiological Roles
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Distribution of Corticotropin-Releasing Factor and Urocortin 1 in the Vole Brain
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The role of neurohypophyseal peptides in the central mediation of complex social processes — evidence from comparative studies
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A 9‐year‐old male with a duplication of chromosome 3p25.3p26.2: Clinical report and gene expression analysis
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Opposing Regulation of Pair Bond Formation by cAMP Signaling within the Nucleus Accumbens Shell
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Mating system and avpr1a promoter variation in primates
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Identification of an orally active, nonpeptidyl oxytocin antagonist.
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Minor disturbances in central nervous system function in familial neurohypophysial diabetes insipidus
Bruins, J., Kovács, G. L., Abbes, A. P., Burbach, J. P. H., van den Akker, E. L. T., Engel, H., FRANKEN, A., & de Wied, D. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.06.001 · Cited by 23 · see citing works
Genetics of vasopressin receptors
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The 5′ flanking region of the monogamous prairie vole oxytocin receptor gene directs tissue-specific expression in transgenic mice
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Variation of the oxytocin/neurophysin I (OXT) gene in four human populations
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Wang (1996) · doi:10.1002/(sici)1096-9861(19960318)366:4
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The origins and nature of compassion focused therapy
Gilbert, P. (2014) · British Journal of Clinical Psychology · doi:10.1111/bjc.12043 · Cited by 1,593 · see citing works
Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy
Millan, M. J., Agid, Y., Brüne, M., Bullmore, E. T., Carter, C. S., Clayton, N. S., Connor, R., Davis, S., Deakin, B., DeRubeis, R. J., et al. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3628 · Cited by 1,292 · see citing works
The neurochemistry of music
Chanda, M. L., & Levitin, D. J. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.02.007 · Cited by 1,136 · see citing works
Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors
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“…in response to sensory stimulation via a network of OT-containing nerves (Landgraf and Neumann, 2004; Ross et al., 2009), e.g., during breastfeeding, labor, sex, but also touch, warmth, and stroking, usually in the context of trusting relationships (for reviews see Uvnäs-Moberg, 2003; Insel, 2010).”
Advancing the understanding of autism disease mechanisms through genetics
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Oxytocin enables maternal behaviour by balancing cortical inhibition
Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C. (2015) · Nature · doi:10.1038/nature14402 · Cited by 744 · see citing works
Oxytocin and social affiliation in humans
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Oxytocin-Mediated GABA Inhibition During Delivery Attenuates Autism Pathogenesis in Rodent Offspring
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Music and social bonding: â€œself-otherâ€ merging and neurohormonal mechanisms
Tarr, B., Launay, J., & Dunbar, R. I. M. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01096 · Cited by 548 · see citing works
Serotonin selectively influences moral judgment and behavior through effects on harm aversion
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Putting together phylogenetic and ontogenetic perspectives on empathy
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Social re-orientation and brain development: An expanded and updated view
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Oxytocin and Vasopressin Agonists and Antagonists as Research Tools and Potential Therapeutics
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Common liability to addiction and “gateway hypothesis”: Theoretical, empirical and evolutionary perspective
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“Research on monogamous mammals, particularly prairie voles, has shown that the neuropeptide oxytocin (OXT) promotes the formation of pair-bonds in females, with a related peptide, argininevasopressin being more important in males (Donaldson and Young, 2008; Insel, 2010).”
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Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques ( Macaca mulatta )
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Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism
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Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement
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Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees
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A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors
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Oxytocin and vasopressin: linking pituitary neuropeptides and their receptors to social neurocircuits
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Oxytocin promotes social bonding in dogs
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“spectrum disorder (ASD) and schizophrenia (12-17), and one report suggests that OXTR expression may be reduced in ASD (18).”
Synchrony as an Adaptive Mechanism for Large‐Scale Human Social Bonding
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Functional Selective Oxytocin-derived Agonists Discriminate between Individual G Protein Family Subtypes
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No Laughing Matter: Intranasal Oxytocin Administration Changes Functional Brain Connectivity during Exposure to Infant Laughter
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Environmental risk, Oxytocin Receptor Gene (OXTR) methylation and youth callous-unemotional traits: a 13-year longitudinal study
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Mitigation of Sociocommunicational Deficits of Autism Through Oxytocin-Induced Recovery of Medial Prefrontal Activity: A Randomized Trial
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Developmental Perspectives on Oxytocin and Vasopressin
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Interpersonal Stress Regulation and the Development of Anxiety Disorders: An Attachment-Based Developmental Framework
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The Use of Oxytocin to Improve Feeding and Social Skills in Infants With Prader–Willi Syndrome
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Impact of early adversity on glucocorticoid regulation and later mental disorders
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Human neuroimaging of oxytocin and vasopressin in social cognition
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Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice
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Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice
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“Finally we examined mRNA for the oxytocin receptor because it has been implicated in a variety of social behaviors [34,35].”
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Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors
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Oxytocin transforms firing mode of CA2 hippocampal neurons
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From genes to social communication: molecular sensing by the vomeronasal organ.
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Oxytocin and Vasopressin in Children and Adolescents With Autism Spectrum Disorders: Sex Differences and Associations With Symptoms
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From fundamental research to clinical translation: The neural modulation of social behavior by oxytocin and vasopressin
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Oxytocin and vasopressin: linking pituitary neuropeptides and their receptors to social neurocircuits
Baribeau, D. A., & Anagnostou, E. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00335 · Cited by 229 · see citing works
Oxytocin, vasopressin, and the neurogenetics of sociality
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Authors: Insel, T. R.
Affiliations: National Institutes of Health (US)
Corresponding author: Insel, Thomas R.
ORCID: Insel, Thomas R.
Venue: Neuron
Publisher: Elsevier BV
Published: 2010-03
Volume: 65
Issue: 6
Pages: 768-779
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2010.03.005
PMC: PMC2847497
OpenAlex: W2166273490
Cited by: 1,044
References: 140
Citations by year: 2026: 30 · 2025: 30 · 2024: 32 · 2023: 53 · 2022: 57 · 2021: 64 · 2020: 68 · 2019: 65 · 2018: 73 · 2017: 72 · 2016: 76 · 2015: 75 · 2014: 98 · 2013: 80 · 2012: 89
FWCI: 9.90
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1270 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (Z99 MH999999)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
Keywords: oxytocin, vasopressin, affiliative behavior, social cognition, oxytocin receptor, vasopressin V1a receptor, voles, social behavior genetics, reward systems, autism spectrum disorder, gender differences, steroid hormones, neuropeptides
MeSH terms: Animals, Humans, Nerve Net, Neurosciences, Oxytocin, Social Behavior, Protein Biosynthesis, Vasopressins

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The Challenge of Translation in Social Neuroscience: A Review of Oxytocin, Vasopressin, and Affiliative Behavior

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