Neuroendocrine perspectives on social attachment and love

Sue Carter, C

doi:10.1016/s0306-4530(98)00055-9

Cited by 1,425Neuroendocrine regulation and behaviorAttachment and Relationship DynamicsStress Responses and Cortisol

Neuroendocrine perspectives on social attachment and love

Sue Carter, C·1998·Psychoneuroendocrinology

DOI 10.1016/s0306-4530(98)00055-9

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Abstract

The purpose of this paper is to review existing behavioral and neuroendocrine perspectives on social attachment and love. Both love and social attachments function to facilitate reproduction, provide a sense of safety, and reduce anxiety or stress. Because social attachment is an essential component of love, understanding attachment formation is an important step toward identifying the neurobiological substrates of love. Studies of pair bonding in monogamous rodents, such as prairie voles, and maternal attachment in precocial ungulates offer the most accessible animal models for the study of mechanisms underlying selective social attachments and the propensity to develop social bonds. Parental behavior and sexual behavior, even in the absence of selective social behaviors, are associated with the concept of love; the analysis of reproductive behaviors, which is far more extensive than our understanding of social attachment, also suggests neuroendocrine substrates for love. A review of these literatures reveals a recurrent association between high levels of activity in the hypothalamic pituitary adrenal (HPA) axis and the subsequent expression of social behaviors and attachments. Positive social behaviors, including social bonds, may reduce HPA axis activity, while in some cases negative social interactions can have the opposite effect. Central neuropeptides, and especially oxytocin and vasopressin have been implicated both in social bonding and in the central control of the HPA axis. In prairie voles, which show clear evidence of pair bonds, oxytocin is capable of increasing positive social behaviors and both oxytocin and social interactions reduce activity in the HPA axis. Social interactions and attachment involve endocrine systems capable of decreasing HPA reactivity and modulating the autonomic nervous system, perhaps accounting for health benefits that are attributed to loving relationships.

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Animal model research points to a strong relationship between socially monogamous attachment behaviors and the expression of oxytocin within the brain, along with vasopressin and dopamine.
“Animal model research points to a strong relationship between socially monogamous attachment behaviors and the expression of oxytocin within the brain—along with that of an affiliated peptide, vasopressin, and a suite of auxiliary hormones and neurotransmitters including dopamine.”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [35]
Anatomical investigations into the mating patterns of prairie voles and montane voles suggest that their dissimilar bonding strategies may turn upon systematic differences in the distribution of oxytocin and vasopressin receptor neurons in their brains.
“Notably, anatomical investigations into the mating patterns of two closely-related species of vole—the monogamous prairie vole (Microtus ochrogaster) and the polygamous montane vole (Microtus montanus)—suggest that their dissimilar bonding strategies may turn upon systematic differences in the distribution of oxytocin and vasopressin receptor neurons in their brains [35].”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [35]
Oxytocin is a nonapeptide hormone associated with affiliative bonding in mammals and mediates social behavior, pair-bonding, and parental attachment across species.
“OT is a nonapeptide hormone associated with affiliative bonding in mammals (Insel et al., 1997) that is known to mediate social behavior, pair-bonding, and parental attachment across a variety of species (Carter, 1998).”
From Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity (2012) · cites this paper as Carter, 1998
The current findings lend some support to evolutionary models that parental and romantic attachment share underlying mechanisms mediated by the oxytocinergic system.
“The current findings lend some support to evolutionary models suggesting that parental and romantic attachment share some underlying mechanisms and are mediated by the oxytocinergic system (Carter, 1998; Feldman, in press).”
From Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity (2012) · cites this paper as Carter, 1998
Positive effects of touch from others are likely mediated by increased secretion of oxytocin.
“positive effects are likely mediated by increased secretion of the neuropeptide oxytocin [6,[16], [17], [18], [19]].”
From Self-soothing touch and being hugged reduce cortisol responses to stress: A randomized controlled trial on stress, physical touch, and social identity (2021) · cites this paper as [16]

In humans, parenting effort is promoted by long-term bonding between romantic partners, which is mediated by many of the same neurobiological mechanisms underlying parent-child attachment.
“In humans, parenting effort is promoted by long-term bonding between romantic partners, which in turn is mediated by many of the same neurobiological mechanisms underlying parent-child attachment (Carter, 1998; Lancaster and Kaplan, 2009; Pedersen et al., 2005)”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as Carter, 1998
Research has repeatedly implicated OT as one of the key hormones involved in parent-infant bonding in mammals, as well as in a range of social and affiliative behaviors.
“Research has repeatedly implicated the neuropeptide oxytocin (OT) as one of the key hormones involved in parent-infant bonding in mammals, as well as in a range of social and affiliative behaviors (3–7).”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [3]
Several studies in human mothers have shown that peripheral OT release during birth, breastfeeding, and skin-to-skin contact between mothers and newborns is related to higher maternal responsiveness, lower maternal stress, and more optimal mother-infant bond.
“Several studies in human mothers have shown that peripheral OT release during birth, breastfeeding, and skin-to-skin contact between mothers and newborns is related to higher maternal responsiveness, lower maternal stress, and more optimal motherinfant bond (3,26).”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [3]
The natural establishment of pairbonds in prairie voles is usually accompanied by extensive sexual behavior over one to two days, which also induces ovulation in females.
“The natural establishment of pairbonds in prairie voles is usually accompanied by extensive sexual behavior over one to two days (Carter 1998) which also induces ovulation in females.”
From Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins (2010) · cites this paper as Carter 1998
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 [26]
The neuropeptide oxytocin plays a central role in attachment formation, affiliation and social behavior.
“The neuropeptide oxytocin plays a central role in attachment formation, affiliation and social behavior (Carter, 1998).”
From Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal (2013) · cites this paper as Carter, 1998
OT may facilitate social interactions by lowering social vigilance and reducing social stress.
“Taken together, these findings suggest that OT may facilitate social interactions by lowering social vigilance and reducing social stress (Carter, 1998; Chang et al., 2013b; Ebitz et al., 2013; Neumann et al., 2000b; Uvnäs-Moberg et al., 1994).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Carter, 1998
Adult sociosexual bonds in socially monogamous species function not only to facilitate reproduction, but to also reduce potentially deleterious health outcomes due to stress/anxiety.
“Adult sociosexual bonds in socially monogamous species function not only to facilitate reproduction, but to also reduce potentially deleterious health outcomes due to stress/anxiety (Carter, 1998).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Carter, 1998

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Differential Localization of Estrogen Receptors in Various Vasopressin Synthesizing Nuclei of the Rat Brain
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Oxytocin Activation of Maternal Behavior in the Rata
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Hormonal and experiential factors influencing parental behaviour in male rodents: An integrative approach
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Evolutionary Precedents for Behavioral Actions of Oxytocin and Vasopressina
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Alterations in Hypothalamic‐ Pituitary Responsiveness during Lactation
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“Oxytocin and vasopressin differ from each other in two amino acids and may have evolved from a common ancestral peptide (Acher 1996).”
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Anatomy of Love
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Social stress in guinea pigs
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Oxytocin Receptor Binding in Female Prairie Voles: Endogenous and Exogenous Oestradiol Stimulation
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Species differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus).
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Social experience, behavior, and stress in guinea pigs
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The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia.
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Increased accumulation of oxytocin messenger ribonucleic acid in the hypothalamus of the female rat: induction by long term estradiol and progesterone administration and subsequent progesterone withdrawal
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The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia.
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Hormonal and attitudinal correlates of maternal behaviour during the early postpartum period in first-time mothers
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Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse, Peromyscus californicus
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Prenatal social stress masculinizes the females' behaviour in guinea pigs
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Behavioral and heart rate pattern differences between breast-fed and bottle-fed neonates.
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Motivational Properties of Oxytocin in the Conditioned Place Preference Paradigm
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OXYTOCIN RECEPTOR mRNA EXPRESSION IN RAT BRAIN: IMPLICATIONS FOR BEHAVIORAL INTEGRATION AND REPRODUCTIVE SUCCESS
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INTRODUCTION
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Perinatal Steroid Treatments Alter Alloparental and Affiliative Behavior in Prairie Voles
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Oxytocin binding sites in rat limbic and hypothalamic structures: Site-specific modulation by adrenal and gonadal steroids
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Oxytocin and Oxytocin Receptor Gene Expression in the Uterus
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Central Neural Mechanisms in Cardiovascular Regulation
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Sexual receptivity and exhaustion in the female golden hamster
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Neuropeptide co-expression in the magnocellular neurosecretory system of the female rat: Evidence for differential modulation by estrogen
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Brain Sexual Dimorphism and Sex Differences in Parental and Other Social Behaviorsa
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Stress and Coping in Time of War: Generalizations From the Israeli Experience
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Psychobiology of Early Social Attachment in Rhesus Monkeys Clinical Implications
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Prolactin Stimulates the Release of Oxytocin in Lactating Rats: Evidence for a Physiological Role via an Action at the Neural Lobe
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Sexual Behavior Differentiation
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Early Learning and the Social Bond
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Passionate love and anxiety in young adolescents
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Structure, processing and evolution of the neurohypophysial hormone-neurophysin precursors
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Oxytocin Concentrations during the Neonatal Period
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Changes in oxytocin content in the magnocellular neurons of the rat hypothalamus following water deprivation or estrogen treatment
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Molecular aspects of monogamy
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Central Oxytocin and Female Sexual Behaviora
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Oxytocin reinstates maternal olfactory cues for nipple orientation and attachment in rat pups
SINGH, P., & HOFER, M. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90317-7 · Cited by 51 · see citing works
Psychobiological Consequences of Social Relationshipsa
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Speculations Concerning the Physiological Significance of Central Oxytocin in Maternal Behavior
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Effects of intracerebroventricular infusions of naltrexone and phentolamine on central and peripheral oxytocin release and on maternal behaviour induced by vaginocervical stimulation in the ewe
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Neurogenesis of the sexually dimorphic vasopressin cells of the bed nucleus of the stria terminalis and amygdala of rats
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Regulatory Mechanisms of Oxytocin‐Mediated Sociosexual Behavior
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The Regulation of Oxytocin Receptor Binding in the Ventromedial Hypothalamic Nucleus by Gonadal Steroids
Johnson, A. E. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34367.x · Cited by 43 · see citing works
Experiential and Hormonal Correlates of Care-Giving in Rhesus Macaques
Holman, S. D., & Goy, R. W. (2015) · KARGER eBooks · doi:10.1159/000424491 · Cited by 42 · see citing works
Glucocorticoid regulation of hippocampal oxytocin receptor binding
Liberzon, I., Chalmers, D. T., Mansour, A., López, J. F., Watson, S. J., & Young, E. A. (1994) · Brain Research · doi:10.1016/0006-8993(94)91798-1 · Cited by 39 · see citing works
Cardiac, neuroendocrine, and behavioral effects of central amygdaloid vasopressinergic and oxytocinergic mechanisms under stress-free conditions in rats
Roozendaal, B., Schoorlemmer, G. H. M., Koolhaas, J. M., & Bohus, B. (1993) · Brain Research Bulletin · doi:10.1016/0361-9230(93)90157-7 · Cited by 38 · see citing works
Vasopressin modulates male squirrel monkeys' behavior during social separation
Winslow, J., & Insel, T. R. (1991) · European Journal of Pharmacology · doi:10.1016/0014-2999(91)90671-c · Cited by 37 · see citing works
Affiliative behavior in voles: Effects of morphine, naloxone, and cross-fostering
Shapiro, L. E., Meyer, M. E., & Dewsbury, D. A. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90357-0 · Cited by 37 · see citing works
Interrelationships between Sexual Responsiveness, Birth, and Breast Feeding
Newton, N. R. (1992) · Pre- and Peri-natal Psychology Journal · Cited by 30 · see citing works
Sexual differentiation in prairie voles: the effects of corticosterone and testosterone
Roberts, R. L., Zullo, A. S., & Carter, C. S. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00365-x · Cited by 30 · see citing works
Self-citation
From learning to love : the selected papers of H.F. Harlow
Harlow, H. F., & Harlow, C. M. (1986) · Praeger eBooks · Cited by 28 · see citing works
Electrophysiology of Oxytocin Actions on Central Neuronsa
Dreifuss, J. J., Dubois‐Dauphin, M., Widmer, H., & Raggenbass, M. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34345.x · Cited by 28 · see citing works
Physiological aspects of adult attachment.
Reite, M. L., & Boccia, M. L. (1994) · Cited by 28 · see citing works
Mild sustained effects of neonatal vasopressin and oxytocin treatment on brain growth and behavior of the rat
Boer, G. J., Quak, J., de Vries, M. C., & Heinsbroek, R. P. W. (1994) · Peptides · doi:10.1016/0196-9781(94)90007-8 · Cited by 27 · see citing works
Presence of Calcitonin-Like Peptide in Rat Milk: Possible Physiological Role in Regulation of Neonatal Prolactin Secretion*
Shah, G. V., Kacsoh, B. Z., SESHADRI, R., GROSVENOR, C. E., & Crowley, W. R. (1989) · Endocrinology · doi:10.1210/endo-125-1-61 · Cited by 26 · see citing works
Contemporary sexual behavior: critical issues in the 1970s
Zubin, J., & Money, J. (1973) · DigitalGeorgetown (Georgetown University Library) · Cited by 24 · see citing works
Exploratory Behavior Correlates with Social Organization and Is Responsive to Peptide Injections in Prairie Voles
Dharmadhikari, A., LEE, Y. S., Roberts, R. L., & Carter, C. S. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51982.x · Cited by 23 · see citing works
Chronic oxytocin treatment during late gestation and lactation impairs development of rat offspring
Boer, G. J. (1993) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(93)90055-s · Cited by 23 · see citing works
Neuropeptides and brain development. Current perils and future potential.
Swaab, D. F., & Gj, B. (1983) · PubMed · Cited by 20 · see citing works
Oxytocin Pretreatment Enhances Arginine Vasopressin‐lnduced Motor Disturbances and Arginine Vasopressin‐lnduced Phosphoinositol Hydrolysis in Rat Septum: A Cross‐Sensitization Phenomenon
Poulin, P., & Pittman, Q. J. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00361.x · Cited by 19 · see citing works
Neurochemical Changes Accompanying the Reproductive Process: Their Significance for Maternal Care in Primates and Other Mammals
Keverne, E. B. (2015) · KARGER eBooks · doi:10.1159/000424489 · Cited by 19 · see citing works
Corticosteroid Regulation of Gene Expression and Binding Characteristics of Vasopressin Receptors in the Rat Brain
Patchev, V. K., & Almeida, O. F. X. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01153.x · Cited by 18 · see citing works
Affiliation and Neuropsychiatric Disorders: The Deficit Syndrome of Schizophreniaa
Kirkpatrick, B. W. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51939.x · Cited by 17 · see citing works
Distribution of Oxytocinergic Glucocorticoid Target Neurons in the Rat Hypothalamus
Jirikowski, G. F., McGimsey, W. C., Caldwell, J. D., & Sar, M. (1993) · Hormone and Metabolic Research · doi:10.1055/s-2007-1002171 · Cited by 16 · see citing works
Neonatal vasopressin antagonist treatment facilitates adult copulatory behavior in female rats and increases hypothalamic vasopressin content
Meyerson, B. J., Höglund, U., Johansson, C., Blomqvist, A. G., & Ericson, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)90864-5 · Cited by 15 · see citing works
Effects of Feeding Method on Infant Temperament
Worobey, J. (1993) · Advances in child development and behavior · doi:10.1016/s0065-2407(08)60299-2 · Cited by 13 · see citing works
Vasopressin, maternal behavior, and pup well-being
Wideman, C. H., & Murphy, H. (1990) · Current Psychology · doi:10.1007/bf02686866 · Cited by 11 · see citing works
Differential Fos Expression Following Microinjection of Oxytocin or Vasopressin in the Prairie Vole Brain
Gingrich, B., HOUT, R. L., Wang, Z., & Insel, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51952.x · Cited by 8 · see citing works
Role of Vasopressin in Central Cardiovascular Regulation
Berecek, K. H. (1992) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-9184-5_1 · Cited by 8 · see citing works
Patterns of Infant Feeding, the Mother-Infant Interaction and Stress Management
Field, T. M., Mccabe, P., & Schneiderman, N. (2013) · Psychology Press eBooks · doi:10.4324/9781315825489-8 · Cited by 8 · see citing works
Mother Love Revisited: On the Use of Animal Models
Klopfer, P. H. (1996) · American Scientist · Cited by 5 · see citing works
Heterosexual Interactions Promote Oxytocin Secretion in Sexually Naive, but Not Experienced, Male Wistar Ratsa
Hillegaart, V., Alster, P., Uvnäs‐Moberg, K., & Ahlénius, S. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51959.x · Cited by 3 · see citing works

Flagged first, then by citations

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Sorted by citations

Oxytocin increases trust in humans
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690 · see citing works
The polyvagal perspective.
Porges, S. W. (2007) · Biological Psychology · doi:10.1016/j.biopsycho.2006.06.009 · Cited by 3,415 · see citing works
Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight.
Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A. R., & Updegraff, J. A. (2000) · Psychological Review · doi:10.1037/0033-295x.107.3.411 · Cited by 3,308 · see citing works
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
Compassion: an evolutionary analysis and empirical review
Goetz, J. L., Keltner, D., & Simon-Thomas, E. (2010) · Psychological Bulletin · doi:10.1037/a0018807 · Cited by 2,200 · see citing works
Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress
Heinrichs, M., Baumgartner, T., Kirschbaum, C., & Ehlert, U. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00465-7 · Cited by 2,091 · see citing works
Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity
BOYCE, W. T., & ELLIS, B. J. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050145 · Cited by 2,078 · see citing works
Compassionate mind training for people with high shame and self-criticism: Overview and pilot study of a group therapy approach
Gilbert, P., & Procter, S. (2006) · Clinical Psychology & Psychotherapy · doi:10.1002/cpp.507 · Cited by 1,822 · see citing works
Why Does Social Exclusion Hurt? The Relationship Between Social and Physical Pain.
MacDonald, G., & Leary, M. R. (2005) · Psychological Bulletin · doi:10.1037/0033-2909.131.2.202 · Cited by 1,712 · see citing works
The polyvagal theory: phylogenetic substrates of a social nervous system.
Porges, S. W. (2001) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(01)00162-3 · Cited by 1,582 · see citing works
Social effects of oxytocin in humans: context and person matter
Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.002 · Cited by 1,572 · see citing works
The neural correlates of maternal and romantic love
Bartels, A., & Zeki, S. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.11.003 · Cited by 1,448 · see citing works
Introducing compassion-focused therapy
Gilbert, P. (2009) · Advances in Psychiatric Treatment · doi:10.1192/apt.bp.107.005264 · Cited by 1,435 · see citing works
The Adaptive Calibration Model of stress responsivity
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.11.007 · Cited by 1,373 · see citing works
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
Oxytocin improves “mind-reading” in humans
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.015 · Cited by 1,298 · see citing works
Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.009 · Cited by 1,258 · see citing works
Self-compassion and Psychological Resilience Among Adolescents and Young Adults
Neff, K. D., & McGehee, P. (2010) · Self and Identity · doi:10.1080/15298860902979307 · Cited by 1,232 · see citing works
Affective consciousness: core emotional feelings in animals and humans.
Panksepp, J. (2005) · Consciousness and Cognition · doi:10.1016/j.concog.2004.10.004 · Cited by 1,217 · see citing works
Discriminative and affective touch: Sensing and feeling.
McGlone, F., Wessberg, J., & Olausson, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.001 · Cited by 1,112 · see citing works
Oxytocin: The Great Facilitator of Life
Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037 · see citing works
Neural correlates of conscious self-regulation of emotion
Beauregard, M., Lévesque, J., & Bourgouin, P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-j0001.2001 · Cited by 1,033 · see citing works
a neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Psychosocial and psychophysiological effects of human-animal interactions: the possible role of oxytocin
Beetz, A., Uvnäs-Moberg, K., Julius, H., & Kotrschal, K. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00234 · Cited by 904 · see citing works
“That the OT system plays a major role in social bonds has been documented by several studies (e.g., Carter, 1998; Carter and Keverne, 2002; Bales et al., 2007).”
The science of interpersonal touch: An overview
Gallace, A., & Spence, C. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.10.004 · Cited by 879 · see citing works
The Relationship Context of Human Behavior and Development
Reis, H. T., Collins, W. A., & Berscheid, E. (2000) · Psychological Bulletin · doi:10.1037/0033-2909.126.6.844 · Cited by 853 · see citing works
Oxytocin, vasopressin, and human social behavior
Heinrichs, M., von Dawans, B., & Domes, G. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.005 · Cited by 799 · see citing works
Oxytocin attenuates amygdala responses to emotional faces regardless of valence
Domes, G., Heinrichs, M., Gläscher, J., Büchel, C., Braus, D. F., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.03.025 · Cited by 774 · see citing works
Intranasal Oxytocin Increases Positive Communication and Reduces Cortisol Levels During Couple Conflict
Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.011 · Cited by 784 · see citing works
Oxytocin and social affiliation in humans
Feldman, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.008 · Cited by 767 · see citing works
Tend and Befriend: Biobehavioral Bases of Affiliation Under Stress
Taylor, S. E. (2006) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2006.00451.x · Cited by 755 · see citing works
Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739 · see citing works
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
Self-citation
Sociosexuality from Argentina to Zimbabwe: A 48-nation study of sex, culture, and strategies of human mating
Schmitt, D. P. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000051 · Cited by 974 · see citing works
Sudarshan Kriya Yogic Breathing in the Treatment of Stress, Anxiety, and Depression: Part I—Neurophysiologic Model
Brown, R. P., & Gerbarg, P. L. (2005) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2005.11.189 · Cited by 655 · see citing works
Beyond sexual orientation: integrating gender/sex and diverse sexualities via sexual configurations theory
van Anders, S. M. (2015) · Archives of Sexual Behavior · doi:10.1007/s10508-015-0490-8 · Cited by 651 · 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
Social buffering: relief from stress and anxiety
Kikusui, T., Winslow, J. T., & Mori, Y. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1941 · Cited by 635 · see citing works
Comparison of Skin-to-Skin (Kangaroo) and Traditional Care: Parenting Outcomes and Preterm Infant Development
Feldman, R., Eidelman, A. I., Sirota, L., & Weller, A. (2002) · PEDIATRICS · doi:10.1542/peds.110.1.16 · Cited by 634 · see citing works
The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences
Olff, M., Frijling, J. L., Kubzansky, L. D., Bradley, B., Ellenbogen, M. A., Cardoso, C., Bartz, J. A., Yee, J. R., & van Zuiden, M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.019 · Cited by 620 · see citing works
Sex, attachment, and the development of reproductive strategies
Giudice, M. D. (2009) · Behavioral and Brain Sciences · doi:10.1017/s0140525x09000016 · Cited by 602 · see citing works
Oxytocin is associated with human trustworthiness
ZAK, P., KURZBAN, R., & MATZNER, W. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.07.009 · Cited by 595 · see citing works
Positive social interactions and the human body at work: Linking organizations and physiology
Heaphy, E. D., & Dutton, J. E. (2008) · Academy of Management Review · doi:10.5465/amr.2008.27749365 · Cited by 578 · see citing works
Pharmacological treatment of schizophrenia: a critical review of the pharmacology and clinical effects of current and future therapeutic agents
Miyamoto, S., Miyake, N., Jarskog, L. F., Fleischhacker, W. W., & Lieberman, J. A. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.47 · Cited by 576 · see citing works
Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior
Fries, A. B. W., Ziegler, T. E., Kurian, J. R., Jacoris, S., & Pollak, S. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504767102 · Cited by 570 · see citing works
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
What does sexual orientation orient? A biobehavioral model distinguishing romantic love and sexual desire.
Diamond, L. M. (2003) · Psychological Review · doi:10.1037/0033-295x.110.1.173 · Cited by 547 · see citing works
Evolution and Cognition
Kamil, A. C. (2001) · Evolution and Human Behavior · doi:10.1016/s1090-5138(01)00068-x · Cited by 548 · see citing works
Clinical handbook of mindfulness
(2009) · doi:10.1007/978-0-387-09593-6 · Cited by 543 · see citing works
Cellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523 · see citing works
Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women
Ditzen, B., Neumann, I. D., Bodenmann, G., von Dawans, B., Turner, R. A., Ehlert, U., & Heinrichs, M. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.03.011 · Cited by 525 · see citing works
The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster)
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529 · see citing works
Vasopressin: Behavioral roles of an “original” neuropeptide
Caldwell, H. K., Lee, H.-J., Macbeth, A. H., & Young, W. S. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.10.007 · Cited by 504 · see citing works
Interpersonal Flourishing: A Positive Health Agenda for the New Millennium
Ryff, C. D., & Singer, B. H. (2000) · Personality and Social Psychology Review · doi:10.1207/s15327957pspr0401_4 · Cited by 509 · see citing works
Putting together phylogenetic and ontogenetic perspectives on empathy
Decety, J., & Svetlova, M. (2012) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.003 · Cited by 508 · see citing works
Emotional sounds and the brain: the neuro-affective foundations of musical appreciation
Panksepp, J., & Bernatzky, G. (2002) · Behavioural Processes · doi:10.1016/s0376-6357(02)00080-3 · Cited by 498 · see citing works
Empathy toward strangers triggers oxytocin release and subsequent generosity
Barraza, J. A., & Zak, P. J. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04504.x · Cited by 489 · see citing works
Social modulation of stress responses
DeVries, A. C., Glasper, E. R., & Detillion, C. E. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00152-5 · Cited by 482 · see citing works
Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans
HEINRICHS, M., & DOMES, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00428-7 · Cited by 479 · see citing works
Modulating social behavior with oxytocin: How does it work? What does it mean?
Churchland, P. S., & Winkielman, P. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.003 · Cited by 464 · see citing works
Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2008) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsn004 · Cited by 474 · see citing works
Social buffering of the stress response: diversity, mechanisms, and functions
Hennessy, M. B., Kaiser, S., & Sachser, N. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.06.001 · Cited by 477 · see citing works
Influence of a “Warm Touch” Support Enhancement Intervention Among Married Couples on Ambulatory Blood Pressure, Oxytocin, Alpha Amylase, and Cortisol
Holt-Lunstad, J., Birmingham, W. A., & Light, K. C. (2008) · Psychosomatic Medicine · doi:10.1097/psy.0b013e318187aef7 · Cited by 473 · see citing works
Plasticity of Cortical Excitatory-Inhibitory Balance
Froemke, R. C. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034002 · Cited by 458 · see citing works
Social Engagement and Attachment: A Phylogenetic Perspective
PORGES, S. W. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.004 · Cited by 472 · see citing works
More frequent partner hugs and higher oxytocin levels are linked to lower blood pressure and heart rate in premenopausal women
Light, K. C., Grewen, K. M., & Amico, J. A. (2005) · Biological Psychology · doi:10.1016/j.biopsycho.2004.11.002 · Cited by 470 · see citing works
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469 · see citing works
The emergence of social cognitive neuroscience.
Ochsner, K. N., & Lieberman, M. D. (2001) · American Psychologist · doi:10.1037/0003-066x.56.9.717 · Cited by 536 · see citing works
Developmental neurobiology of childhood stress and trauma
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., & Navalta, C. P. (2002) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(01)00003-x · Cited by 607 · see citing works
“Laughing” rats and the evolutionary antecedents of human joy?
Panksepp, J., & Burgdorf, J. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00159-8 · Cited by 462 · see citing works
Small Bioactive Peptides for Biomaterials Design and Therapeutics
Hamley, I. W. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00522 · Cited by 461 · see citing works
Oxytocin can hinder trust and cooperation in borderline personality disorder
Bartz, J., Simeon, D., Hamilton, H., Kim, S., Crystal, S., Braun, A., Vicens, V., & Hollander, E. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq085 · Cited by 452 · see citing works
Neural correlates of long-term intense romantic love
Acevedo, B. P., Aron, A., Fisher, H. E., & Brown, L. L. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq092 · Cited by 441 · see citing works
“Since then, studies have applied attachment theory to adult romantic relationships (Hazan and Shaver, 1987; Mikulincer and Shaver, 2007) with some researchers suggesting that pair-bonds and parent–infant bonds share common biological substrates (Fisher, 1992; Carter, 1998).”
Background
Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
CARTER, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.025 · Cited by 432 · see citing works
Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: A review of single administration studies
Bos, P. A., Panksepp, J., Bluthé, R.-M., & Honk, J. V. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.01.002 · Cited by 429 · see citing works
Coregulation, Dysregulation, Self-Regulation: An Integrative Analysis and Empirical Agenda for Understanding Adult Attachment, Separation, Loss, and Recovery
Sbarra, D. A., & Hazan, C. (2008) · Personality and Social Psychology Review · doi:10.1177/1088868308315702 · Cited by 427 · see citing works
Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism
Jacob, S., Brune, C. W., Carter, C. S., Leventhal, B. L., Lord, C., & Cook, E. H. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.02.001 · Cited by 425 · see citing works
Self-citation
Oxytocin Makes a Face in Memory Familiar
Rimmele, U., Hediger, K., Heinrichs, M., & Klaver, P. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4260-08.2009 · Cited by 402 · see citing works
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
Developing Sustainable Leaders Through Coaching and Compassion
Boyatzis, R. E., Smith, M. L., & Blaize, N. (2006) · Academy of Management Learning & Education · doi:10.5465/amle.2006.20388381 · Cited by 389 · see citing works
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
BPD's Interpersonal Hypersensitivity Phenotype: A Gene-Environment-Developmental Model
Gunderson, J. G., & Lyons-Ruth, K. (2008) · Journal of Personality Disorders · doi:10.1521/pedi.2008.22.1.22 · Cited by 511 · see citing works
Oxytocin, vasopressin and sociality
CARTER, C., GRIPPO, A., POURNAJAFINAZARLOO, H., RUSCIO, M., & PORGES, S. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00427-5 · Cited by 380 · see citing works
Self-citation
Influence of different positive emotions on persuasion processing: A functional evolutionary approach.
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Authors: Sue Carter, C.
Venue: Psychoneuroendocrinology
Publisher: Elsevier BV
Published: 1998-11
Volume: 23
Issue: 8
Pages: 779-818
ISSN: 0306-4530 (ISSN-L)
DOI: 10.1016/s0306-4530(98)00055-9
OpenAlex: W2171095353
Cited by: 1,425
References: 203
Citations by year: 2026: 14 · 2025: 38 · 2024: 34 · 2023: 42 · 2022: 29 · 2021: 44 · 2020: 56 · 2019: 48 · 2018: 45 · 2017: 103 · 2016: 70 · 2015: 85 · 2014: 76 · 2013: 82 · 2012: 82
FWCI: 32.58
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Psychoneuroendocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: social attachment, love, neuroendocrinology, pair bonding, Microtus ochrogaster, maternal attachment, hypothalamic-pituitary-adrenal axis, oxytocin, vasopressin, social bonding, reproductive behavior, autonomic nervous system, stress reduction, monogamy
MeSH terms: Animals, Child, Biological Evolution, Female, Humans, Hypothalamo-Hypophyseal System, Love, Male, Neurosecretory Systems, Object Attachment, Pair Bond, Parent-Child Relations, Pituitary-Adrenal System, Sexual Behavior, Social Behavior

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Neuroendocrine perspectives on social attachment and love

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