A neurobiological basis of social attachment.
Abstract
OBJECTIVE: Although an inability to form normal social attachments characterizes many forms of psychopathology, there has been little study of the neural basis of social bond formation. The primary purpose of this article is to describe a novel approach to the neurobiology of attachment. METHOD: The author reviews animal research on two closely related neuropeptides, oxytocin and vasopressin, implicated in the central mediation of attachment behaviors. These neuropeptides appear to be important for the initiation of pair bonds and parental behaviors as well as the infant's response to social separation. RESULTS: Both cellular and molecular studies have begun to reveal the mechanisms by which oxytocin and vasopressin neural pathways are regulated, leading to a preliminary understanding of how these hormones act within the brain to influence complex social behaviors. CONCLUSIONS: Although their function in the human brain has yet to be demonstrated, the available evidence suggests that oxytocin and vasopressin may prove to be important in the pathophysiology of clinical disorders, such as autism, characterized by an inability to form normal social attachments.
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Relationship discord is the most frequent cause of emotional distress.
“In contrast, relationship discord has been found to be the most frequent cause of emotional distress [19]”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [19]
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 [5]
Oxytocin may specifically facilitate the transition from avoidance of pups to caring for them.
“For instance, hypothalamic lesions block the initiation, but not the maintenance, of maternal behaviors in rats (18), suggesting that OXT may specifically facilitate the transition from avoidance of pups to caring for them (19,20).”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [19]
Pre-existing primers are necessary to induce oxytocin-facilitated social bonding in monogamous Prairie voles; these primers can be gonadal hormones (e.g., estrogen), mating behaviors, or prolonged pre-exposure to a former stranger (Insel, 1997).
“Similarly, pre-existing ‘primers’ are necessary to induce oxytocin-facilitated social bonding in monogamous Prairie voles, and, depending on the study designs, these primers can be gonadal hormones (e.g. estrogen), mating behaviors, or prolonged pre-exposure to a former stranger (for an early review, (Insel, 1997)).”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Insel, 1997
Cites
Attachment and Loss. Vol. 1. Attachment
Rever, G. W. (1972) · Psychosomatic Medicine · doi:10.1097/00006842-197211000-00011 · Cited by 8,446 · see citing works
Atlas of estradiol‐concentrating cells in the central nervous system of the female rat
Pfaff, D. W., & Keiner, M. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901510204 · Cited by 1,494 · see citing works
Kleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436 · see citing works
Prenatal maternal speech influences newborns' perception of speech sounds
DeCasper, A. J., & Spence, M. J. (1986) · Infant Behavior and Development · doi:10.1016/0163-6383(86)90025-1 · Cited by 1,106 · see citing works
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · see citing works
Pedersen, C. A., & Prange, A. J. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6661 · Cited by 841 · see citing works
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Insel, T. R., & Shapiro, L. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5981 · Cited by 833 · see citing works
Oxytocin is required for nursing but is not essential for parturition or reproductive behavior.
Nishimori, K., Young, L. J., Guo, Q., Wang, Z., Insel, T. R., & Matzuk, M. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11699 · Cited by 734 · see citing works
(1971) · Annals of Internal Medicine · doi:10.7326/0003-4819-75-4-654_2 · Cited by 714 · see citing works
Physiological substrates of mammalian monogamy: The prairie vole model
Sue Carter, C., Courtney Devries, A., & Getz, L. L. (1995) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)00070-h · Cited by 615 · see citing works
Primate Social Relationships: an Integrated Approach
Hinde, R. A. (1983) · Medical Entomology and Zoology · Cited by 583 · see citing works
Insel, T. R., & Hulihan, T. J. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.782 · Cited by 528 · see citing works
Keverne, E. B., Martensz, N. D., & Tuite, B. (1989) · Psychoneuroendocrinology · doi:10.1016/0306-4530(89)90065-6 · Cited by 525 · see citing works
Insel, T. R. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90073-g · Cited by 487 · see citing works
Williams, J. R., Insel, T. R., Harbaugh, C. R., & Carter, C. S. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00579.x · Cited by 483 · see citing works
Relationships as Regulators: A Psychobiologic Perspective on Bereavement*
Hofer, M. A. (1984) · Psychosomatic Medicine · doi:10.1097/00006842-198405000-00001 · Cited by 476 · see citing works
Pedersen, C. A., Caldwell, J. D., Walker, C., Ayers, G., & Mason, G. A. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.6.1163 · Cited by 475 · see citing works
THE CHARACTERISTICS AND CONTEXT OF IMPRINTING
Bateson, P. (1966) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1966.tb01489.x · Cited by 471 · see citing works
Getz, L. L., Carter, C. S., & Gavish, L. (1981) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299829 · Cited by 466 · see citing works
Insel, T., Wang, Z., & Ferris, C. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05381.1994 · Cited by 454 · see citing works
Carter, C. S. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80176-9 · Cited by 417 · see citing works
Vasopressin and oxytocin receptors in the central nervous system
Tribollet, E., & Barberis, C. (1996) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v10.i1.60 · Cited by 399 · see citing works
Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
Wang, Z., Ferris, C. F., & De Vries, G. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.400 · Cited by 381 · see citing works
Loup, F., Tribollet, E., Dubois-Dauphin, M., & Dreifuss, J. J. (1991) · Brain Research · doi:10.1016/0006-8993(91)90345-v · Cited by 378 · see citing works
Argiolas, A., & GESSA, G. L. (1991) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80002-8 · Cited by 364 · see citing works
A psychobiological theory of attachment
Kraemer, G. W. (1992) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00069752 · Cited by 359 · see citing works
Social organization of the prairie vole (Microtus ochrogaster)
Getz, L. L., McGuire, B., Pizzuto, T., Hofmann, J. E., & Frase, B. (1993) · Journal of Mammalogy · doi:10.2307/1381904 · Cited by 350 · see citing works
A Defect in Nurturing in Mice Lacking the Immediate Early Gene fosB
Brown, J. R., Ye, H., Bronson, R. T., Dikkes, P., & Greenberg, M. E. (1996) · Cell · doi:10.1016/s0092-8674(00)80101-4 · Cited by 339 · see citing works
Central Nervous System Effects of the Neurohypophyseal Hormones and Related Peptides
de Wied, D., Diamant, M., & Fodor, M. (1993) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1993.1009 · Cited by 327 · see citing works
Changes in oxytocin and vasopressin secretion during sexual activity in men
MURPHY, M. R., SECKL, J. R., BURTON, S., CHECKLEY, S. A., & LIGHTMAN, S. L. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-4-738 · Cited by 318 · see citing works
The Evolution of Monogamy in Large Primates: a New Hypothesis and Some Crucial Tests
van Schaik, C. P., & Dunbar, R. (1990) · Behaviour · doi:10.1163/156853990x00284 · Cited by 280 · see citing works
Harlow, H. F., & Suomi, S. J. (1970) · American Psychologist · doi:10.1037/h0029383 · Cited by 263 · see citing works
Social organization in free-living prairie voles, Microtus ochrogaster
Getz, L. L., & Hofmann, J. E. (1986) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00300004 · Cited by 239 · see citing works
Sensory Deprivation Stress and Supplemental Stimulation in the Rat Pup and Preterm Human Neonate
Schanberg, S. M., & Field, T. M. (1987) · Child Development · doi:10.2307/1130683 · Cited by 233 · see citing works
Endogenous opiates regulate oxytocin but not vasopressin secretion from the neurohypophysis
Bicknell, R. J., & Leng, G. (1982) · Nature · doi:10.1038/298161a0 · Cited by 229 · see citing works
Tribollet, E., Charpak, S., Schmidt, A., Dubois-Dauphin, M., & Dreifuss, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01764.1989 · Cited by 228 · see citing works
Sex Differences in Neurotransmitter Systems
Vries, G. J. D. (1990) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1990.tb00385.x · Cited by 226 · see citing works
Evidence for a Physiological Role for Oxytocin in the Control of Prolactin Secretion*
Samson, W. K., Lumpkin, M. D., & McCann, S. M. (1986) · Endocrinology · doi:10.1210/endo-119-2-554 · Cited by 219 · see citing works
Vasopressin and oxytocin release in the brain – a synaptic event
Buijs, R. M., & Heerikhuize, J. J. V. (1982) · Brain Research · doi:10.1016/0006-8993(82)90979-9 · Cited by 218 · see citing works
Mating in the monogamous male: Behavioral consequences
Insel, T. R., Preston, S., & Winslow, J. T. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00362-9 · Cited by 215 · see citing works
Hansen, S., Harthon, C., Waslin, E., Löfberg, L., & al, E. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.4.588 · Cited by 211 · see citing works
Whitnall, M., Key, S., Ben-Barak, Y., Ozato, K., & Gainer, H. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-01-00098.1985 · Cited by 209 · see citing works
McGuire, B., & Novak, M. A. (1984) · Animal Behaviour · doi:10.1016/s0003-3472(84)80229-8 · Cited by 207 · see citing works
Oliveras, D. M., & Novak, M. A. (1986) · Animal Behaviour · doi:10.1016/s0003-3472(86)80120-8 · Cited by 196 · see citing works
Hansen, S., Harthon, C., Wallin, E., et al. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.4.588 · Cited by 186 · see citing works
Central administration of oxytocin modulates the infant rats response to social isolation
Insel, T. R., & Winslow, J. (1991) · European Journal of Pharmacology · doi:10.1016/0014-2999(91)90806-2 · Cited by 185 · see citing works
Insel, T. R. (1990) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1990.tb00445.x · Cited by 164 · see citing works
Bamshad, M., Novak, M. A., & de Vries, G. J. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90238-0 · Cited by 162 · see citing works
Mendoza, S. P., & Mason, W. A. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90045-4 · Cited by 153 · see citing works
Chemokine Receptors and HIV-1: An Attractive Pair?
Bates, P. F. (1996) · Cell · doi:10.1016/s0092-8674(00)80070-7 · Cited by 147 · see citing works
Maternal contact inhibits pituitary‐adrenal stress responses in preweanling rats
Stanton, M. E., Wallstrom, J., & Levine, S. D. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200204 · Cited by 146 · see citing works
Winslow, J., & Insel, T. (1991) · The Journal of Neuroscience · doi:10.1523/jneurosci.11-07-02032.1991 · Cited by 145 · see citing works
Wang, Z., Smith, W., Major, D. E., & Vries, G. J. D. (1994) · Brain Research · doi:10.1016/0006-8993(94)91784-1 · Cited by 141 · see citing works
Ontogeny of oxytocin receptors in rat forebrain: A quantitative study
Shapiro, L. E., & Insel, T. R. (1989) · Synapse · doi:10.1002/syn.890040312 · Cited by 131 · see citing works
CARTER, C. (1987) · Hormones and Behavior · doi:10.1016/0018-506x(87)90032-8 · Cited by 130 · see citing works
Shapiro, L. E., & Insel, T. R. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230502 · Cited by 128 · see citing works
Tribollet, E., Goumaz, M., Raggenbass, M., Dubois‐Dauphin, M., & Dreifuss, J. J. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90232-8 · Cited by 124 · see citing works
Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats
Giordano, A. L., Johnson, A. E., & Rosenblatt, J. S. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90288-f · Cited by 123 · see citing works
The comparative psychology of monogamy.
Dewsbury, D. A. (1987) · PubMed · Cited by 121 · see citing works
Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups.
Nelson, E. E., & Panksepp, J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.3.583 · Cited by 113 · see citing works
Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups.
Nelson, E., & Panksepp, J. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.3.583 · Cited by 113 · see citing works
Central Nervous System Distribution of Vasopressin, Oxytocin, and Neurophysin
Sofroniew, M. V., & Weindl, A. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-474980-1.50022-2 · Cited by 110 · see citing works
Breton, C., Péchoux, C., Morel, G., & Zingg, H. H. (1995) · Endocrinology · doi:10.1210/endo.136.7.7540544 · Cited by 104 · see citing works
Effects of central vasopressin administration to infant rats
Winslow, J., & Insel, T. R. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90354-k · Cited by 98 · see citing works
Opiate regulation of maternal behavior in the rat
Grimm, C. T., & Bridges, R. S. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90336-2 · Cited by 97 · see citing works
Shapiro, L. E., & Dewsbury, D. A. (1990) · Journal of comparative psychology · doi:10.1037/0735-7036.104.3.268 · Cited by 95 · see citing works
Crowley, R. S., Insel, T. R., O’Keefe, J. A., Kim, N. B., & Amico, J. A. (1995) · Endocrinology · doi:10.1210/endo.136.1.7828535 · Cited by 89 · see citing works
Johnson, A. E., Ball, G. F., Coirini, H., Harbaugh, C. R., McEwen, B. S., & Insel, T. R. (1989) · Endocrinology · doi:10.1210/endo-125-3-1414 · Cited by 87 · see citing works
The Human Model : Primate Perspectives
Harlow, H. F., & Mears, C. (1979) · University of Toronto eBooks · Cited by 79 · see citing works
Winslow, J. T., & Insel, T. R. (1990) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12578-0 · Cited by 77 · see citing works
Kow, L., Johnson, A. E., Ogawa, S., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000125948 · Cited by 73 · see citing works
Parental Care and its Relationship to Social Organization in the Montane Vole (Microtus montanus)
McGuire, B., & Novak, M. A. (1986) · Journal of Mammalogy · doi:10.2307/1380883 · Cited by 65 · see citing works
Oxytocin and rodent sociosexual responses: from behavior to gene expression
M.Witt, D. (1995) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00006-z · Cited by 64 · see citing works
Nesting Patterns of Adult Voles, Microtus montanus, in Field Populations
Jannett, F. J. (1982) · Journal of Mammalogy · doi:10.2307/1380450 · Cited by 64 · see citing works
Merendino, J. J., Spiegel, A. M., Crawford, J. D., O’Carroll, A., Brownstein, M., & Lolait, S. J. (1993) · New England Journal of Medicine · doi:10.1056/nejm199305273282106 · Cited by 64 · see citing works
Oxytocin Concentrations during the Neonatal Period
Leake, R. D., Weitzman, R. E., & Fisher, D. A. (2009) · Biology of the Neonate · doi:10.1159/000241417 · Cited by 58 · see citing works
Hudson, R. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90054-3 · Cited by 58 · see citing works
Raggenbass, M., Charpak, S., Dubois‐Dauphin, M., & Dreifuss, J.-J. (1988) · Journal of Receptor Research · doi:10.3109/10799898809048992 · Cited by 37 · see citing works
Classical conditioning of opioid activity in the fetal rat.
Smotherman, W. P., & Robinson, S. R. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.5.951 · Cited by 23 · see citing works
Mechanisms maintaining monogamy in monkeys.
Snowdon, C. T. (1990) · Sinauer Associates eBooks · doi:10.1037/11525-010 · Cited by 23 · see citing works
YOUNG, L. J., WAYMIRE, K. G., NILSEN, R., MACGREGOR, G. R., WANG, Z., & INSEL, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51955.x · Cited by 20 · see citing works
Robinson, S. R., Hoeltzel, T. C. M., & Smotherman, W. P. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00358-c · Cited by 16 · see citing works
Classical conditioning of opioid activity in the fetal rat.
Smotherman, W. P., & Robinson, S. R. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.5.951 · Cited by 16 · see citing works
Wang (1996) · doi:10.1002/(sici)1096-9861(19960318)366:4
Flagged first, then by citations
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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
Adolescence: A foundation for future health
Sawyer, S. M., Afifi, R. A., Bearinger, L. H., Blakemore, S.-J., Dick, B., Ezeh, A. C., & Patton, G. C. (2012) · The Lancet · doi:10.1016/s0140-6736(12)60072-5 · Cited by 2,635 · see citing works
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
Neuroendocrine perspectives on social attachment and love
Sue Carter, C. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00055-9 · Cited by 1,425 · see citing works
Psychobiology and molecular genetics of resilience
Feder, A., Nestler, E. J., & Charney, D. S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2649 · Cited by 1,272 · see citing works
Lending a Hand: Social Regulation of the Neural Response to Threat
Coan, J. A., Schaefer, H. S., & Davidson, R. J. (2006) · Psychological Science · doi:10.1111/j.1467-9280.2006.01832.x · Cited by 1,218 · see citing works
Russo, S. J., Murrough, J. W., Han, M.-H., Charney, D. S., & Nestler, E. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3234 · Cited by 1,206 · see citing works
NELSON, E. E., LEIBENLUFT, E., McCLURE, E. B., & PINE, D. S. (2005) · Psychological Medicine · doi:10.1017/s0033291704003915 · Cited by 1,075 · see citing works
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
Insel, T. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.005 · Cited by 1,044 · 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
Adolescent Onset of the Gender Difference in Lifetime Rates of Major Depression: A Theoretical Model
Cyranowski, J. M., Frank, E., Young, E., & Shear, M. K. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.1.21 · Cited by 1,276 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Promoting social behavior with oxytocin in high-functioning autism spectrum disorders.
Andari, E., Duhamel, J.-R., Zalla, T., Herbrecht, E., Leboyer, M., & Sirigu, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910249107 · Cited by 941 · see citing works
Pubertal transitions in health
Patton, G. C., & Viner, R. (2007) · The Lancet · doi:10.1016/s0140-6736(07)60366-3 · Cited by 877 · see citing works
Oxytocin increases generosity in humans
Zak, P. J., Stanton, A. A., & Ahmadi, S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001128 · Cited by 831 · 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 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
Genetics of austim: complex aetiology for a heterogeneous disorder
Folstein, S. E., & Rosen-Sheidley, B. (2001) · Nature Reviews Genetics · doi:10.1038/35103559 · Cited by 771 · 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
Oxytocin Increases Retention of Social Cognition in Autism
Hollander, E., Bartz, J., Chaplin, W., Phillips, A., Sumner, J., Soorya, L., Anagnostou, E., & Wasserman, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.030 · Cited by 693 · 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
Feldman, R., Eidelman, A. I., Sirota, L., & Weller, A. (2002) · PEDIATRICS · doi:10.1542/peds.110.1.16 · Cited by 634 · see citing works
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
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
The Peptide That Binds: A Systematic Review of Oxytocin and its Prosocial Effects in Humans
MacDonald, K., & MacDonald, T. M. (2010) · Harvard Review of Psychiatry · doi:10.3109/10673220903523615 · Cited by 585 · see citing works
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
HOW THE BRAIN PROCESSES SOCIAL INFORMATION: Searching for the Social Brain
Insel, T. R., & Fernald, R. D. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144148 · Cited by 556 · see citing works
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
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
The neuroendocrine basis of social recognition
Ferguson, J. N., Young, L. J., & Insel, T. R. (2002) · Frontiers in Neuroendocrinology · doi:10.1006/frne.2002.0229 · Cited by 494 · see citing works
Self-citationEmpathy 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
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
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
“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
Sbarra, D. A., & Hazan, C. (2008) · Personality and Social Psychology Review · doi:10.1177/1088868308315702 · Cited by 427 · see citing works
The parent–infant dyad and the construction of the subjective self
Fonagy, P., Gergely, G., & Target, M. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01727.x · Cited by 555 · see citing works
Neurochemistry in the pathophysiology of autism.
McDougle, C. J., Erickson, C. A., Stigler, K. A., & Posey, D. J. (2005) · PubMed · Cited by 408 · 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
The signal functions of early infant crying
Soltis, J. (2004) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0400010x · Cited by 387 · see citing works
Baskerville, T. A., & Douglas, A. J. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00154.x · Cited by 377 · see citing works
Oxytocin, motherhood and bonding
Kendrick, K. M. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00014.x · Cited by 378 · see citing works
Meloy, J. R. (1998) · Elsevier eBooks · doi:10.1016/b978-012490560-3/50020-7 · Cited by 372 · see citing works
The origins of altruism in offspring care.
Preston, S. D. (2013) · Psychological Bulletin · doi:10.1037/a0031755 · Cited by 368 · see citing works
A potential role for thalamocingulate circuitry in human maternal behavior
Lorberbaum, J. P., Newman, J. D., Horwitz, A. R., Dubno, J. R., Lydiard, R. B., Hamner, M. B., Bohning, D. E., & George, M. S. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01284-7 · Cited by 359 · see citing works
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
Visions of CompassionWestern Scientists and Tibetan Buddhists Examine Human Nature
Davidson, R. J., & Harrington, A. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195130430.001.0001 · Cited by 346 · see citing works
A. Bartz, J., & Hollander, E. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.018 · Cited by 311 · see citing works
Social vocalizations can release oxytocin in humans
Seltzer, L. J., Ziegler, T. E., & Pollak, S. D. (2010) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.0567 · Cited by 298 · see citing works
Jakubiak, B. K., & Feeney, B. C. (2016) · Personality and Social Psychology Review · doi:10.1177/1088868316650307 · Cited by 302 · see citing works
Swain, J. E., Kim, P., Spicer, J., Ho, S. S., Dayton, C. J., Elmadih, A., & Abel, K. M. (2014) · Brain Research · doi:10.1016/j.brainres.2014.03.007 · Cited by 290 · see citing works
Liu, Y., Curtis, J. T., & Wang, Z. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.4.910 · Cited by 282 · see citing works
Oxytocin receptor polymorphisms and adult attachment style in patients with depression
Costa, B., Pini, S., Gabelloni, P., Abelli, M., Lari, L., Cardini, A., Muti, M., Gesi, C., Landi, S., Galderisi, S., et al. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.05.006 · Cited by 282 · see citing works
The Mentalization-Focused Approach to Self Pathology
Fonagy, P., & Target, M. (2006) · Journal of Personality Disorders · doi:10.1521/pedi.2006.20.6.544 · Cited by 273 · see citing works
González, A., Lovic, V., Ward, G. R., Wainwright, P. E., & Fleming, A. S. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2001)38:1 · Cited by 273 · see citing works
The Role of Oxytocin in Mother-Infant Relations: A Systematic Review of Human Studies
Galbally, M., Lewis, A. J., van IJzendoorn, M., & Permezel, M. (2011) · Harvard Review of Psychiatry · doi:10.3109/10673229.2011.549771 · Cited by 260 · see citing works
Brown, S. L., & Brown, R. M. (2006) · Psychological Inquiry · doi:10.1207/s15327965pli1701_01 · Cited by 247 · see citing works
DAWSON, G., WEBB, S. J., WIJSMAN, E., SCHELLENBERG, G., ESTES, A., MUNSON, J., & FAJA, S. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050327 · Cited by 247 · see citing works
Neurobiology of empathy and callousness: Implications for the development of antisocial behavior
Shirtcliff, E. A., Vitacco, M. J., Graf, A., Gostisha, A. J., Merz, J., & Zahn‐Waxler, C. (2009) · Behavioral Sciences & the Law · doi:10.1002/bsl.862 · Cited by 244 · see citing works
Feldman, R., Weller, A., Sirota, L., & Eidelman, A. I. (2003) · Journal of Family Psychology · doi:10.1037/0893-3200.17.1.94 · Cited by 245 · see citing works
Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin
Lee, P. R., Brady, D. L., Shapiro, R. A., Dorsa, D. M., & Koenig, J. I. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.042 · Cited by 270 · see citing works
BALB/c mice: Low sociability and other phenotypes that may be relevant to autism
Brodkin, E. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.06.025 · Cited by 223 · see citing works
Meyer‐Lindenberg, A., Kolachana, B. S., Gold, B., Olsh, A., Nicodemus, K. K., Mattay, V. S., Dean, M. C., & Weinberger, D. R. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.54 · Cited by 219 · see citing works
Evidence of dysregulated peripheral oxytocin release among depressed women
Cyranowski, J. M., Hofkens, T. L., Frank, E., Seltman, H., Cai, H.-M., & Amico, J. A. (2008) · Psychosomatic Medicine · doi:10.1097/psy.0b013e318188ade4 · Cited by 220 · see citing works
The association between oxytocin receptor gene polymorphism (OXTR) and trait empathy
Wu, N., Li, Z., & Su, Y. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2012.01.009 · Cited by 221 · see citing works
The Neural Basis of Moral Cognition
Moll, J., de Oliveira‐Souza, R., & Zahn, R. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.005 · Cited by 216 · see citing works
Evolutionary Approaches to Psychopathology: The Role of Natural Defences
Gilbert, P. (2001) · Australian & New Zealand Journal of Psychiatry · doi:10.1046/j.1440-1614.2001.00856.x · Cited by 218 · see citing works
Cognitive Accuracy and Intelligent Executive Function in the Brain and in Business
Bailey, C. E. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1412.011 · Cited by 217 · see citing works
Feldman, R., & Eidelman, A. I. (2003) · Developmental Psychobiology · doi:10.1002/dev.10126 · Cited by 210 · see citing works
An Empirical Review of the Neural Underpinnings of Receiving and Giving Social Support
Eisenberger, N. I. (2013) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31829de2e7 · Cited by 213 · see citing works
Bigelow, A. E., Power, M., MacLellan‐Peters, J., Alex, M. R., & McDonald, C. (2012) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1111/j.1552-6909.2012.01350.x · Cited by 206 · see citing works
Fleming, A. S., Kraemer, G. W., Gonzalez, A., Lovic, V., Rees, S., & Melo, A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00793-1 · Cited by 203 · see citing works
Representing Sex in the Brain, One Module at a Time
Yang, C. F., & Shah, N. M. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.029 · Cited by 197 · see citing works
Neural circuits underlying crying and cry responding in mammals
Newman, J. D. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.011 · Cited by 198 · see citing works
Attachment disorders: Assessment strategies and treatment approaches
O’Connor, T. G., & Zeanah, C. H. (2003) · Attachment & Human Development · doi:10.1080/14616730310001593974 · Cited by 195 · see citing works
Acute stress reactions in adults
Shalev, A. Y. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01335-5 · Cited by 194 · see citing works
Feldman, R., Weller, A., Leckman, J. F., Kuint, J., & Eidelman, A. I. (1999) · Journal of Child Psychology and Psychiatry · doi:10.1017/s0021963099004308 · Cited by 317 · see citing works
Parent-infant synchrony and the social emotional development of triplets
Feldman, R., & Eidelman, A. I. (2004) · Developmental Psychology · doi:10.1037/0012-1649.40.6.1133 · Cited by 180 · see citing works
Riedl, R., & Javor, A. (2011) · Journal of Neuroscience Psychology and Economics · doi:10.1037/a0026318 · Cited by 180 · see citing works
Rosenfeld, A. J., Lieberman, J. A., & Jarskog, L. F. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq015 · Cited by 178 · see citing works
Jansen, L. M. C., Gispen-de Wied, C. C., Wiegant, V. M., Westenberg, H. G. M., Lahuis, B. E., & van Engeland, H. (2006) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-006-0124-z · Cited by 177 · see citing works
The Mentalization‐Focused Approach to Social Development
Fonagy, P. (2006) · Wiley eBooks · doi:10.1002/9780470712986.ch3 · Cited by 175 · see citing works
Genes Controlling Affiliative Behavior as Candidate Genes for Autism
Yrigollen, C. M., Han, S. S., Kochetkova, A., Babitz, T., Chang, J. T., Volkmar, F. R., Leckman, J. F., & Grigorenko, E. L. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.11.015 · Cited by 172 · see citing works
Implications of breaking mother-young social bonds
Newberry, R. C., & Swanson, J. C. (2008) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2007.03.021 · Cited by 206 · see citing works
Doron, G., & Kyrios, M. (2005) · Clinical Psychology Review · doi:10.1016/j.cpr.2005.02.002 · Cited by 168 · see citing works
The sociophysiology of caring in the doctor-patient relationship
Adler, H. M. (2002) · Journal of General Internal Medicine · doi:10.1046/j.1525-1497.2002.10640.x · Cited by 162 · see citing works
If music is the food of love, what about survival and reproductive success?
Dissanayake, E. (2008) · Musicae Scientiae · doi:10.1177/1029864908012001081 · Cited by 161 · see citing works
Brief report: theatre as therapy for children with autism spectrum disorder
Corbett, B. A., Gunther, J. R., Comins, D., Price, J., Ryan, N., Simon, D., Schupp, C. W., & Rios, T. (2011) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-1064-1 · Cited by 160 · see citing works
Buchheim, A., Erk, S., George, C., Kächele, H., Kircher, T., Martius, P., Pokorny, D., Ruchsow, M., Spitzer, M., & Walter, H. (2008) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.07.001 · Cited by 160 · see citing works
Feldman, R. (2000) · Infant Mental Health Journal · doi:10.1002/1097-0355(200007)21:3 · Cited by 155 · see citing works
Boyatzis, R. E., Rochford, K. C., & Taylor, S. N. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00670 · Cited by 164 · see citing works
Light, K. C., Smith, T. E., Johns, J. M., Brownley, K. A., Hofheimer, J. A., & Amico, J. A. (2000) · Health Psychology · doi:10.1037//0278-6133.19.6.560 · Cited by 154 · see citing works
Social approach–avoidance behavior of inbred mouse strains towards DBA/2 mice
Brodkin, E. S., Hagemann, A., Nemetski, S. M., & Silver, L. M. (2004) · Brain Research · doi:10.1016/j.brainres.2003.12.013 · Cited by 170 · see citing works
Effects of intranasal oxytocin on 'compassion focused imagery'
Rockliff, H., Karl, A., McEwan, K., Gilbert, J., Matos, M., & Gilbert, P. (2011) · Emotion · doi:10.1037/a0023861 · Cited by 147 · see citing works
Mother-to-Infant Emotional Involvement at Birth
Figueiredo, B., Costa, R., Pacheco, A., & Pais, Á. (2009) · Maternal and Child Health Journal · doi:10.1007/s10995-008-0312-x · Cited by 145 · see citing works
Low CSF oxytocin reflects high intent in suicide attempters
Jokinen, J., Chatzittofis, A., Hellström, C., Nordström, P., Uvnäs-Moberg, K., & Åsberg, M. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.016 · Cited by 143 · see citing works
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
The functional neuroanatomy of the evolving parent–infant relationship
Parsons, C. E., Young, K. S., Murray, L., Stein, A. L., & Kringelbach, M. L. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.03.001 · Cited by 141 · see citing works
Highly heritable and functionally relevant breed differences in dog behaviour
MacLean, E. L., Snyder-Mackler, N., vonHoldt, B. M., & Serpell, J. A. (2019) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2019.0716 · Cited by 144 · see citing works
Communicating affection: interpersonal behavior and social context
(2007) · Choice Reviews Online · doi:10.5860/choice.44-3351 · Cited by 142 · see citing works
- Authors
- Insel, T. R.
- Affiliations
- Emory University (US)
- Corresponding author
- Thomas R. Insel
- ORCID
- Thomas R. Insel
- Venue
- American Journal of Psychiatry
- Published
- 1997-06-01
- Volume
- 154
- Issue
- 6
- Pages
- 726-735
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- OpenAlex
- W1717145785
- Cited by
- 553
- References
- 82
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 20 · 2023: 19 · 2022: 7 · 2021: 21 · 2020: 8 · 2019: 12 · 2018: 12 · 2017: 10 · 2016: 10 · 2015: 18 · 2014: 20 · 2013: 21 · 2012: 30
- FWCI
- 4.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Psychiatry (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
- social attachment, neurobiology of attachment, oxytocin, vasopressin, pair bonding, parental behavior, social separation, autism spectrum disorder, neuropeptides
- MeSH terms
- Animals, Arginine Vasopressin, Behavior, Animal, Arvicolinae, Female, Humans, Male, Maternal Behavior, Oxytocin, Pair Bond, Sexual Behavior, Animal, Social Behavior, Vasopressins, Receptors, Vasopressin, Receptors, Oxytocin
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