Oxytocin and social affiliation in humans

Feldman, Ruth

doi:10.1016/j.yhbeh.2012.01.008

Cited by 767Neuroendocrine regulation and behaviorAttachment and Relationship DynamicsHuman-Animal Interaction Studies

Oxytocin and social affiliation in humans

Feldman, Ruth·2012·Hormones and Behavior

DOI 10.1016/j.yhbeh.2012.01.008

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Abstract

A conceptual model detailing the process of bio-behavioral synchrony between the online physiological and behavioral responses of attachment partners during social contact is presented as a theoretical and empirical framework for the study of affiliative bonds. Guided by an ethological behavior-based approach, we suggest that micro-level social behaviors in the gaze, vocal, affective, and touch modalities are dynamically integrated with online physiological processes and hormonal response to create dyad-specific affiliations. Studies across multiple attachments throughout life are presented and demonstrate that the extended oxytocin (OT) system provides the neurohormonal substrate for parental, romantic, and filial attachment in humans; that the three prototypes of affiliation are expressed in similar constellations of social behavior; and that OT is stable over time within individuals, is mutually-influencing among partners, and that mechanisms of cross-generation and inter-couple transmission relate to coordinated social behavior. Research showing links between peripheral and genetic markers of OT with concurrent parenting and memories of parental care; between administration of OT to parent and infant's physiological readiness for social engagement; and between neuropeptides and the online synchrony of maternal and paternal brain response in social-cognitive and empathy networks support the hypothesis that human attachment develops within the matrix of biological attunement and close behavioral synchrony. The findings have conceptual implications for the study of inter-subjectivity as well as translational implications for the treatment of social disorders originating in early childhood, such as autism spectrum disorders, or those associated with disruptions to early bonding, such as postpartum depression or child abuse and neglect. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.

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In humans, OXT has been implicated in attraction and bonding behavior in both men and women.
“In humans, OXT has also been implicated in attraction and bonding behavior in both men and women (Meyer-Lindenberg et al., 2011;Feldman, 2012;McCall and Singer, 2012).”
From Oxytocin Modulates Social Distance between Males and Females (2012) · cites this paper as Feldman, 2012
Oxytocin may influence not only long-term romantic partner and parent-infant bonds but also other kinds of social bonds.
“Consequently, OXT may not exclusively affect long-term romantic partner-and parent-infant bonds (37), but also influence other kinds of social bonds.”
From Oxytocin enhances brain reward system responses in men viewing the face of their female partner (2013) · cites this paper as [37]
Coordinated peripheral and central OT release during labor and nursing acts to induce bonding between mother and infant.
“The dual central and peripheral role for OT in the onset of maternal behavior, and particularly in the formation of mother-offspring attachments, suggests that coordinated peripheral and central OT release during labor and nursing act to induce bonding between mother and infant (Ross and Young 2009; Feldman 2012).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Feldman 2012
These studies support the hypothesis that OT release during human romantic activities induces formation of long-term bonds.
“These studies lend support to the hypothesis that OT release during human romantic activities serves to induce the formation of long-term bonds (Young et al 2005; Feldman 2012).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Feldman 2012
Samples were not collected if grooming or copulation also occurred within 60 min prior to urination, as both behaviours are likely to independently increase urinary oxytocin levels.
“In both conditions, samples were not collected if grooming or copulation also occurred within 60 min prior to urination, as both of these behaviours are likely to independently increase urinary oxytocin levels [39].”
From Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees (2014) · cites this paper as [39]

The social context is the setting in which OT exerts its cross-generational effects in mammals.
“The social context is the setting in which OT exerts its cross-generational effects in mammals (3,28)”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
Such overarching involvement of OT in social and affiliative processes is thought to stem from the hormone's central involvement in the formation of the parent-infant bond, which, in turn, enhances physiological and behavioral systems that underpin human social engagement throughout life.
“Such overarching involvement of OT in social and affiliative processes is thought to stem from the hormone's central involvement in the formation of the parent-infant bond, which, in turn, enhances physiological and behavioral systems that underpin human social engagement throughout life (3,26,27).”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
The expression of these parenting behaviors predicts greater empathy, prosocial orientation, and emotion regulation in childhood and adolescence.
“The expression of these behaviors has been shown to predict greater empathy, prosocial orientation, and emotion regulation in childhood and adolescence (3,38).”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
Peripheral oxytocin and respiratory sinus arrhythmia are associated with higher levels of infant social behavior.
“Peripheral OT and RSA have been associated with higher levels of infant social behavior (3,35)”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
Oxytocin is a neurohormonal system that dynamically engages body and brain, organism and environment, and separate partners within an attachment relationship.
“Oxytocin is a neurohormonal system that dynamically engages body and brain, organism and environment, and separate partners within an attachment relationship (3).”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
Touch within close relationships is associated with baseline oxytocin and the oxytocin response.
“Touch within close relationships has been repeatedly associated with baseline OT and the OT response (3)”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
Oxytocin is thought to induce a physiological state that provides the neurobiological substrate for social engagement.
“Thus, OT is thought to induce a physiological state that provides the neurobiological substrate for social engagement (3,59).”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [3]
There are genetic associations between several polymorphisms of OTR gene and CD38 gene and human parenting behavior.
“There are also genetic associations between several polymorphisms of OTR gene and CD38 gene and human parenting behavior (Feldman 2012; Riem et al. 2011, 2012).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Feldman 2012
OXT plays a critical role in the facilitation of social bonding and prosocial behavior toward a social partner.
“Oxytocin (OXT), a neuromodulatory nonapeptide, plays a critical role in the facilitation of social bonding and prosocial behavior toward a social partner (Feldman, 2012).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Feldman, 2012
Oxytocin enhances social cognitive functioning in humans and is important in interpersonal behavior and affiliation.
“The neuropeptide oxytocin (OT) enhances social cognitive functioning in humans and is important in interpersonal behavior and affiliation [1], [2].”
From A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli (2013) · cites this paper as [1]

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Sensitive Parenting Is Associated with Plasma Oxytocin and Polymorphisms in the OXTR and CD38 Genes
Feldman, R., Zagoory-Sharon, O., Weisman, O., Schneiderman, I., Gordon, I., Maoz, R., Shalev, I., & Ebstein, R. P. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.12.025 · Cited by 393 · see citing works
Self-citation
Breastfeeding, brain activation to own infant cry, and maternal sensitivity
Kim, P., Feldman, R., Mayes, L. C., Eicher, V., Thompson, N., Leckman, J. F., & Swain, J. E. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2011.02406.x · Cited by 386 · see citing works
Self-citation
Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial
Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M., van IJzendoorn, M. H., & Rombouts, S. A. R. B. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.006 · Cited by 366 · see citing works
Parent–infant synchrony: a biobehavioral model of mutual influences in the formation of affiliative bonds
Feldman, R. (2012) · Monographs of the Society for Research in Child Development · doi:10.1111/j.1540-5834.2011.00660.x · Cited by 360 · see citing works
Self-citation
Social Competence in Developmental Perspective
Schneider, B. H., Attili, G., Nadel, J., & Weissberg, R. P. (1989) · Springer eBooks · doi:10.1007/978-94-009-2442-0 · Cited by 354 · see citing works
Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition
Lerer, E., Levi, S., Salomon, S., Darvasi, A., Yirmiya, N., & Ebstein, R. P. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002087 · Cited by 349 · see citing works
Plasma oxytocin concentration during pregnancy is associated with development of postpartum depression
Skrundz, M., Bolten, M., Nast, I., Hellhammer, D. H., & Meinlschmidt, G. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.74 · Cited by 349 · see citing works
Maternal postpartum behavior and the emergence of infant-mother and infant-father synchrony in preterm and full-term infants: The role of neonatal vagal tone
Feldman, R., & Eidelman, A. I. (2007) · Developmental Psychobiology · doi:10.1002/dev.20220 · Cited by 348 · see citing works
Self-citation
Culture, distress, and oxytocin receptor polymorphism (OXTR) interact to influence emotional support seeking
Kim, H. S., Sherman, D. K., Sasaki, J. Y., Xu, J., Chu, T. Q., Ryu, C., Suh, E. M., Graham, K., & Taylor, S. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010830107 · Cited by 341 · see citing works
Bio-behavioral Synchrony: A Model for Integrating Biological and Microsocial Behavioral Processes in the Study of Parenting
Feldman, R. (2012) · Parenting · doi:10.1080/15295192.2012.683342 · Cited by 324 · see citing works
Self-citation
Sociobiological Perspectives on Human Development
MacDonald, K. B. (1988) · Springer eBooks · doi:10.1007/978-1-4612-3760-0 · Cited by 323 · see citing works
Wider than the sky : the phenomenal gift of consciousness
Edelman, G. M. (2004) · Cited by 322 · see citing works
Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles
Ross, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity
Schneiderman, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.12.021 · Cited by 317 · cited 1× · see citing works
“…further corroborate our proposition that both parental and romantic attachment is supported by similar OT-based neuroendocrine mechanisms and is expressed in a similar behavioral repertoire including gaze, touch, affect, and vocalizations and their online coordination (Schneiderman et al., 2012).”
BackgroundSelf-citation
Oxytocin during pregnancy and early postpartum: Individual patterns and maternal-fetal attachment
Levine, A., Zagoory-Sharon, O., Feldman, R., & Weller, A. (2007) · Peptides · doi:10.1016/j.peptides.2007.04.016 · Cited by 315 · see citing works
Self-citation
Neural control of maternal behaviour and olfactory recognition of offspring
Kendrick, K. M., Da Costa, A. P. C., Broad, K. D., Ohkura, S., Guevara, R., Lévy, F., & Keverne, E. B. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00218-9 · Cited by 311 · see citing works
From biological rhythms to social rhythms: physiological precursors of mother-infant synchrony.
Feldman, R. (2006) · Developmental Psychology · doi:10.1037/0012-1649.42.1.175 · Cited by 311 · see citing works
Self-citation
Philosophie als strenge Wissenschaft
Edmund, E. (2009) · Felix Meiner Verlag eBooks · doi:10.28937/978-3-7873-2394-4 · Cited by 305 · see citing works
Mother rats bar-press for pups: effects of lesions of the mpoa and limbic sites on maternal behavior and operant responding for pup-reinforcement
Lee, A. M., Clancy, S., & Fleming, A. S. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00109-0 · Cited by 301 · see citing works
Romantic love and sexual desire in close relationships
Gonzaga, G. C., Turner, R. A., Keltner, D., Campos, B., & Altemus, M. (2006) · Emotion · doi:10.1037/1528-3542.6.2.163 · Cited by 292 · cited 2× · see citing works
“communication, affiliation, and emotional support between partners (Gonzaga et al., 2006; Grewen et al., 2005).”
Background
Philosophie als Strenge Wissenschaft
Husserl, E. (1987) · Husserliana. Documente/Husserliana · doi:10.1007/978-94-009-4349-0_1 · Cited by 292 · see citing works
The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task
Israel, S., Lerer, E., Shalev, I., Uzefovsky, F., Riebold, M., Laiba, E., Bachner-Melman, R., Maril, A., Bornstein, G., Knafo, A., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005535 · Cited by 278 · see citing works
Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin systems in the hypothalamus and the bed nucleus of the stria terminalis of the rat: Implications for balancing stress and affect
Dabrowska, J., Hazra, R., Ahern, T. H., Guo, J.-D., McDonald, A. J., Mascagni, F., Muller, J. F., Young, L. J., & Rainnie, D. G. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.003 · Cited by 274 · see citing works
Attachment and bonding: A new synthesis.
Carter, C. S., Ahnert, L., Grossmann, K. E., Hrdy, S. B., Lamb, M. E., Porges, S. W., & Sachser, N. (2005) · Cited by 271 · see citing works
The cross-generation transmission of oxytocin in humans
Feldman, R., Gordon, I., & Zagoory-Sharon, O. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.005 · Cited by 256 · see citing works
Self-citation
Are plasma oxytocin in women and plasma vasopressin in men biomarkers of distressed pair-bond relationships?
Taylor, S. E., Saphire-Bernstein, S., & Seeman, T. E. (2010) · Psychological Science · doi:10.1177/0956797609356507 · Cited by 256 · see citing works
Parenting stress, infant emotion regulation, maternal sensitivity, and the cognitive development of triplets: A model for parent and child influences in a unique ecology
Feldman, R., Eidelman, A. I., & Rotenberg, N. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00816.x · Cited by 253 · see citing works
Self-citation
Second nature: brain science and human knowledge
(2007) · Choice Reviews Online · doi:10.5860/choice.44-3854 · Cited by 238 · see citing works
Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress
Gordon, I., Zagoory‐Sharon, O., Schneiderman, I., Leckman, J. F., Weller, A., & Feldman, R. (2008) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00649.x · Cited by 232 · see citing works
Self-citation
Sex differences in the parental behavior of rodents
Lonstein, J. S., & De Vries, G. J. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00036-1 · Cited by 226 · see citing works
Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin
Atzil, S., Hendler, T., Zagoory-Sharon, O., Winetraub, Y., & Feldman, R. (2012) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2012.06.008 · Cited by 225 · see citing works
Self-citation
Analysis of whole genome biomarker expression in blood and brain
Rollins, B. L., Martin, M. V., Morgan, L. Z., & Vawter, M. P. (2010) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.31062 · Cited by 217 · see citing works
Oxytocin and social motivation
Gordon, I., Martin, C., Feldman, R., & Leckman, J. F. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.007 · Cited by 211 · see citing works
Self-citation
Oxytocin Receptor Gene Polymorphism (rs2254298) Interacts with familial risk for psychopathology to predict symptoms of depression and anxiety in adolescent girls
Thompson, R. J., Parker, K. J., Hallmayer, J. F., Waugh, C. E., & Gotlib, I. H. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.07.003 · Cited by 211 · see citing works
Direct and indirect effects of breast milk on the neurobehavioral and cognitive development of premature infants
Feldman, R., & Eidelman, A. I. (2003) · Developmental Psychobiology · doi:10.1002/dev.10126 · Cited by 210 · see citing works
Second Nature: Brain Science and Human Knowledge
Edelman, G. M. (2006) · Cited by 203 · see citing works
Mother-infant synchrony and the development of moral orientation in childhood and adolescence: Direct and indirect mechanisms of developmental continuity.
Feldman, R. (2007) · American Journal of Orthopsychiatry · doi:10.1037/0002-9432.77.4.582 · Cited by 194 · see citing works
Self-citation
The relational basis of adolescent adjustment: trajectories of mother–child interactive behaviors from infancy to adolescence shape adolescents' adaptation
Feldman, R. (2010) · Attachment & Human Development · doi:10.1080/14616730903282472 · Cited by 192 · see citing works
Self-citation
No Laughing Matter: Intranasal Oxytocin Administration Changes Functional Brain Connectivity during Exposure to Infant Laughter
Riem, M. M. E., van IJzendoorn, M. H., Tops, M., Boksem, M. A. S., Rombouts, S. A. R. B., & Bakermans-Kranenburg, M. J. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.313 · Cited by 191 · see citing works
Parent-specific reciprocity from infancy to adolescence shapes children's social competence and dialogical skills
Feldman, R., Bamberger, E., & Kanat‐Maymon, Y. (2013) · Attachment & Human Development · doi:10.1080/14616734.2013.782650 · Cited by 185 · see citing works
Self-citation
Two genetic variants of CD38 in subjects with autism spectrum disorder and controls
Munesue, T., Yokoyama, S., Nakamura, K., Anitha, A., Yamada, K., Hayashi, K., Asaka, T., Liu, H.-X., Jin, D., Koizumi, K., et al. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.03.004 · Cited by 177 · see citing works
Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioral variables
Maestripieri, D., Hoffman, C. L., Anderson, G. M., Carter, C. S., & Higley, J. D. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.12.016 · Cited by 174 · see citing works
Oxytocin, cortisol, and triadic family interactions
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.008 · Cited by 158 · see citing works
Self-citation
The Social Insects
Wheeler, W. M. (1928) · K. Paul, Trench, Trubner eBooks · Cited by 152 · see citing works
Prolactin, Oxytocin, and the development of paternal behavior across the first six months of fatherhood
Gordon, I., Zagoory‐Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.04.007 · Cited by 148 · see citing works
Self-citation
Hormones Associated with Non-Maternal Infant Care: A Review of Mammalian and Avian Studies
Ziegler, T. E. (2000) · Folia Primatologica · doi:10.1159/000021726 · Cited by 142 · see citing works
Species-Typical Behavior of Hamsters Deprived from Birth of the Neocortex
Murphy, M. R., MacLean, P. D., & Hamilton, S. C. (1981) · Science · doi:10.1126/science.7244642 · Cited by 142 · see citing works
Plasticity in the maternal circuit: Effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat.
Fleming, A. S., & Korsmit, M. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.3.567 · Cited by 136 · see citing works
Hypothalamic Vasopressin Gene Expression Increases in Both Males and Females Postpartum in a Biparental Rodent
Wang, Z., Liu, Y., Young, L. J., & Insel, T. R. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00435.x · Cited by 134 · see citing works
Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins
Snowdon, C. T., Pieper, B. A., Boe, C. Y., Cronin, K. A., Kurian, A. V., & Ziegler, T. E. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.014 · Cited by 133 · cited 2× · see citing works
“…1995): intracerebroventricular infusion of OT facilitates partner's attachment in female prairie voles (Williams et al., 1994), blockade of OT receptors impairs bond formation (Cho et al., 1999), and peripheral levels of OT correlate with partners' affiliative behavior (Snowdon et al., 2010).”
Background
Role of midline frontolimbic cortex in production of the isolation call of squirrel monkeys
MacLean, P. D., & Newman, J. D. (1988) · Brain Research · doi:10.1016/0006-8993(88)91550-8 · Cited by 130 · see citing works
Central control of penile erection: A re-visitation of the role of oxytocin and its interaction with dopamine and glutamic acid in male rats
Melis, M. R., & Argiolas, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.014 · Cited by 129 · see citing works
Oxytocin-messages via the cerebrospinal fluid: Behavioral effects; a review
Veening, J. G., A, T. R. D. J., & Barendregt, H. P. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.05.004 · Cited by 126 · see citing works
On the origins of background emotions: From affect synchrony to symbolic expression.
Feldman, R. (2007) · Emotion · doi:10.1037/1528-3542.7.3.601 · Cited by 125 · see citing works
Self-citation
The Narrative Approach to Moral Development: From the Epistemic Subject to Dialogical Selves
Day, J. M., & Tappan, M. B. (2010) · Human Development · doi:10.1159/000278410 · Cited by 119 · see citing works
Oxytocin indexes relational distress following interpersonal harms in women
Tabak, B. A., McCullough, M. E., Szeto, A., Mendez, A. J., & McCabe, P. M. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.07.004 · Cited by 116 · see citing works
The function of the median cerebral cortex in maternal behavior of rats.
Stamm, J. S. (1955) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0042977 · Cited by 112 · see citing works
Plasticity in the maternal circuit: Effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat.
Fleming, A. S., & Korsmit, M. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.3.567 · Cited by 111 · see citing works
No Association between Oxytocin Receptor (OXTR) Gene Polymorphisms and Experimentally Elicited Social Preferences
Apicella, C. L., Cesarini, D. A., Johannesson, M., Dawes, C. T., Lichtenstein, P., Wallace, B., Beauchamp, J. P., & Westberg, L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011153 · Cited by 110 · see citing works
Evolutionary Theory and the Human Family
Davis, J. N., & Daly, M. (1997) · The Quarterly Review of Biology · doi:10.1086/419953 · Cited by 96 · see citing works
Problems in the bio-psychology of social organization.
Schneirla, T. C. (1946) · Journal of Abnormal & Social Psychology · doi:10.1037/h0055210 · Cited by 96 · see citing works
Sexual dimorphism in the vasopressin system: Lack of an altered behavioral phenotype in female V1a receptor knockout mice
Bielsky, I. F., Hu, S.-B., & Young, L. J. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.005 · Cited by 91 · see citing works
Differential involvement of nucleus accumbens shell and core subregions in maternal memory in postpartum female rats.
Li, M., & Fleming, A. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.3.426 · Cited by 90 · see citing works
Maternal imprints and the origins of variation
Champagne, F. A. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.016 · Cited by 74 · see citing works
Antenatal origins of individual differences in heart rate
DiPietro, J. A., Costigan, K. A., Pressman, E. K., & Doussard-Roosevelt, J. A. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2000)37:4 · Cited by 71 · see citing works
Love: Neuroscience reveals all
Young, L. J. (2009) · Nature · doi:10.1038/457148a · Cited by 71 · see citing works
Chapter 15 Perinatal development of human circadian rhythms
Mirmiran, M., & Lunshof, S. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)60410-0 · Cited by 63 · see citing works
Parental and romantic attachment shape brain processing of infant cues
Weisman, O., Feldman, R., & Goldstein, A. (2012) · Biological Psychology · doi:10.1016/j.biopsycho.2011.11.008 · Cited by 50 · see citing works
Self-citation
Mothers' concentrations of oxytocin following close, physical interactions with biological and nonbiological children
Bick, J. R., & Dozier, M. (2009) · Developmental Psychobiology · doi:10.1002/dev.20411 · Cited by 48 · see citing works
High vagal tone is associated with more efficient regulation of homeostasis in low-risk human fetuses
Groome, L. J., Loizou, P. C., Holland, S. B., Smith, L. A., & Hoff, C. J. (1999) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199907)35:1 · Cited by 46 · see citing works
The transition to oral feeding in low-risk premature infants: Relation to infant neurobehavioral functioning and mother–infant feeding interaction
Silberstein, D., Geva, R., Feldman, R., Gardner, J. M., Karmel, B. Z., Rozen, H., & Kuint, J. (2008) · Early Human Development · doi:10.1016/j.earlhumdev.2008.07.006 · Cited by 44 · see citing works
Self-citation
Oxytocin both increases proliferative response of peripheral blood lymphomonocytes to phytohemagglutinin and reverses immunosuppressive estrogen activity.
Macciò, A., Madeddu, C., Chessa, P., Panzone, F., Lissoni, P., & Mantovani, G. (2010) · PubMed · Cited by 40 · see citing works
Love alters autonomic reactivity to emotions.
Schneiderman, I., Zilberstein-Kra, Y., Leckman, J. F., & Feldman, R. (2011) · Emotion · doi:10.1037/a0024090 · Cited by 33 · see citing works
Self-citation
Interest in infants by female rhesus monkeys with neonatal lesions of the amygdala or hippocampus
Toscano, J. E., Bauman, M. D., Mason, W. A., & Amaral, D. G. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.05.056 · Cited by 31 · see citing works
Maternal touch and the developing infant.
Feldman, R. (2011) · Cited by 30 · see citing works
Self-citation
Advances in Vasopressin and Oxytocin — From Genes to Behaviour to Disease
(2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00453-6 · Cited by 28 · see citing works
Influence of postpartum onset on the course of mood disorders
Serretti, A., Olgiati, P., & Colombo, C. (2006) · BMC Psychiatry · doi:10.1186/1471-244x-6-4 · Cited by 28 · see citing works
Temporal changes in functional magnetic resonance imaging activation of heterosexual couples for visual stimuli of loved partners
Kim, W., Kim, S., Jeong, J., Lee, K.-U., Ahn, K.-J., Chung, Y.-A., Hong, K.-Y., & Chae, J.-H. (2009) · Psychiatry Investigation · doi:10.4306/pi.2009.6.1.19 · Cited by 28 · see citing works
Dopaminergic stimulation of oxytocin concentrations in the plasma of male and female monkeys by apomorphine and a D2 receptor agonist
Cameron, J. L., Pomerantz, S., Layden, L. M., & Amico, J. A. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.75.3.1355489 · Cited by 20 · see citing works
Thymic Transcription of Neurohypophysial and Insulin‐Related Genes: Impact Upon T‐Cell Differentiation and Self‐Tolerance
Hansenne, I. (2005) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2005.01301.x · Cited by 19 · see citing works
Preface
Neumann, I. D., & LANDGRAF, R. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00448-2 · Cited by 18 · see citing works
The Evolution of Paternal Care
Salgado, M. (2013) · Lecture notes in computer science · doi:10.1007/978-3-642-37210-0_1 · Cited by 11 · see citing works

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Sorted by citations

The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839 · see citing works
Self-citation
Oxytocin pathways and the evolution of human behavior
Carter, C. S. (2014) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115110 · Cited by 714 · see citing works
Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life
Feldman, R., Rosenthal, Z., & Eidelman, A. I. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.08.012 · Cited by 632 · see citing works
Self-citation
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
The biology of mammalian parenting and its effect on offspring social development
Rilling, J. K., & Young, L. J. (2014) · Science · doi:10.1126/science.1252723 · Cited by 452 · see citing works
The adaptive human parental brain: implications for children's social development
Feldman, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.004 · Cited by 419 · see citing works
Self-citation
Sniffing around oxytocin: Review and meta-analyses of trials in healthy and clinical groups with implications for pharmacotherapy
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.34 · Cited by 383 · see citing works
Father’s brain is sensitive to childcare experiences
Abraham, E., Hendler, T., Shapira-Lichter, I., Kanat-Maymon, Y., Zagoory-Sharon, O., & Feldman, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402569111 · Cited by 343 · see citing works
Self-citation
Oxytocin Pathway Genes: Evolutionary Ancient System Impacting on Human Affiliation, Sociality, and Psychopathology
Feldman, R., Monakhov, M., Pratt, M., & Ebstein, R. P. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.008 · Cited by 352 · see citing works
Self-citation
Oxytocin enhances brain reward system responses in men viewing the face of their female partner
Scheele, D., Wille, A., Kendrick, K. M., Stoffel-Wagner, B., Becker, B., Güntürkün, O., Maier, W., & Hurlemann, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314190110 · Cited by 345 · see citing works
Neuroendocrine regulation of maternal behavior
Bridges, R. S. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.11.007 · Cited by 346 · see citing works
Does Oxytocin Increase Trust in Humans? A Critical Review of Research
Nave, G., Camerer, C., & McCullough, M. (2015) · Perspectives on Psychological Science · doi:10.1177/1745691615600138 · Cited by 309 · see citing works
The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“…eral role for OT in the onset of maternal behavior , and particularly in the formation of mother – offspring attach - ments , suggests that coordinated peripheral and central OT release during labor and nursing act to induce bonding between mother and infant ( Ross and Young 2009 ; Feldman 2012 ) .”
Influential
Oxytocin Modulates Social Distance between Males and Females
Scheele, D., Striepens, N., Güntürkün, O., Deutschländer, S., Maier, W., Kendrick, K. M., & Hurlemann, R. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2755-12.2012 · Cited by 298 · see citing works
“In humans, OXT has also been implicated in attraction and bonding behavior in both men and women (Meyer-Lindenberg et al., 2011; Feldman, 2012; McCall and Singer, 2012).”
Background
Sensitive periods in human social development: New insights from research on oxytocin, synchrony, and high-risk parenting
Feldman, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000048 · Cited by 271 · see citing works
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“Social bonds such as the close and enduring attachments between parents and infants or between opposite sex mates in monogamous mammals can play a critical role in promoting mental and physical well-being (Feldman, 2012).”
Background
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Untitled work
(n.d.) · Progress in Neuro-Psychopharmacology and Biological Psychiatry / PsyPost · doi:10.1016/j.pnpbp.2026.111679

Authors: Feldman, R.
Affiliations: Bar-Ilan University (IL)
Corresponding author: Feldman, Ruth
ORCID: Feldman, Ruth
Venue: Hormones and Behavior
Publisher: Elsevier BV
Published: 2012-03
Volume: 61
Issue: 3
Pages: 380-391
ISSN: 0018-506X (ISSN-L)
DOI: 10.1016/j.yhbeh.2012.01.008
OpenAlex: W2062278675
Semantic Scholar: 13800d1cd34f2a706a8c2e6289476618c1de2ebe
Cited by: 767
References: 156
Citations by year: 2026: 42 · 2025: 48 · 2024: 42 · 2023: 54 · 2022: 41 · 2021: 55 · 2020: 51 · 2019: 66 · 2018: 40 · 2017: 82 · 2016: 59 · 2015: 65 · 2014: 52 · 2013: 53 · 2012: 16
FWCI: 8.42
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Hormones and Behavior (publishedVersion)
PubMed (publishedVersion)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
Keywords: oxytocin, social affiliation, attachment, parental attachment, romantic attachment, dyadic interaction, social bonding, intergenerational transmission, social cognition, intersubjectivity, autism spectrum disorder, postpartum depression, child abuse, neuropeptides, vasopressin
MeSH terms: Animals, Autistic Disorder, Humans, Love, Maternal Behavior, Object Attachment, Oxytocin, Paternal Behavior, Social Behavior, Friends

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Oxytocin and social affiliation in humans

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