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The neurobiology of attachment

Nature Reviews Neuroscience volume 2, pages 129136 (2001) | Download Citation

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Abstract

It is difficult to think of any behavioural process that is more intrinsically important to us than attachment. Feeding, sleeping and locomotion are all necessary for survival, but humans are, as Baruch Spinoza famously noted, “a social animal” and it is our social attachments that we live for. Over the past decade, studies in a range of vertebrates, including humans, have begun to address the neural basis of attachment at a molecular, cellular and systems level. This review describes some of the important insights from this work.

Key points

Summary

  • Humans are a “social animal” and it is our social attachments that we live for. Recent studies have begun to reveal the common neural mechanisms that underlie specific social attachments.

  • Apart from pharmacological studies in maternal monkeys and recent imaging studies in humans, most studies have so far been done in non-primate mammals.

  • Infant–mother attachment. Studies in chick show that during imprinting — when a chick develops an enduring selectivity for following its mother — a long-term memory is formed, entailing changes in the postsynaptic structure of specific cortical regions of the brain. By contrast, rat pups develop maternal recognition through olfactory learning. At this time, no specific cortical region of the pup brain has been identified as important.

  • Maternal–infant attachment. In the rat, many of the same neuroendocrine factors — oestrogen and progesterone — that are associated with pregnancy and lactation are also critical for the onset of maternal behaviour. The neuropeptides prolactin and oxytocin also have a central role. The effects of oxtocin might be mediated through the ventral tegmental area and the medial preoptic area.

  • Olfactory learning. In sheep, selective maternal behaviour can be instigated by vaginocervical stimulation, which stimulates the release of oxytocin. Furthermore, injection of oxytocin into the paraventricular nucleus of the hypothalamus can induce maternal acceptance of the lamb. The maternal ewe's identification of her lamb is accompanied by a robust increase in extracellular concentrations of glutamate and GABA within the olfactory bulb and a reorganization of synapses.

  • Adult–adult pair bond formation. In monogamous prairie voles, oxytocin and vasopressin seem to be necessary and sufficient for pair-bond formation. Neither peptide has a notable effect in the non-monogamous montane vole. Differences in behaviour might be due to differences in the expression patterns of the receptors for these factors. Differences in the promoter regions of these receptor genes have been implictaed in these species differences in receptor distribution and behaviour.

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References

  1. 1.

    & The nature of love — Simplified . Amer. Psychol. 25, 161– 168 (1970).

  2. 2.

    & Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans . Cell 94, 679–689 (1998).

  3. 3.

    Attachment and Loss: Attachment 2nd edn Vol. 1 (Basic Books, New York, 1982).

  4. 4.

    in Contemporary Issues in Comparative Psychology (ed. Dewsbury, D.) 225–251 (Sinauer, Sunderland, Massachusetts, 1990).

  5. 5.

    & Contrasting responses to intruders and involuntary separation by monogamous and polygynous New World monkeys . Physiol. Behav. 38, 795– 801 (1986).

  6. 6.

    , , , & Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. Psychoneuroendocrinology 18, 307–321 ( 1993).

  7. 7.

    & The neural basis of romantic love. NeuroReport 11, 3829–3834 (2000).

  8. 8.

    et al. Feasibility of using fMRI to study mothers responding to infant cries. Depression and Anxiety 10, 99– 104 (1999).

  9. 9.

    & Imprinting, learning and development: from behaviour to brain and back. Trends Neurosci. 21, 306–311 (1998).

  10. 10.

    Visual imprinting and the neural mechanisms of recognition memory. Trends Neurosci. 21, 300–305 (1998).

  11. 11.

    , & Organization of the dorsalcaudal neostriatal complex: a retrograde and anterograde tracing study in the domestic chick with special emphasis on pathways relevant to imprinting. J. Comp. Neurol. 395, 380–404 (1998).

  12. 12.

    & Changes of neuronal responsiveness in the mediorostral neostriatum/hyperstriatum after auditory filial imprinting in the domestic chick. Neuroscience 76, 355–365 (1997).

  13. 13.

    & Stimulus evoked increase of glutamate in the mediorostral neostriatum/hyperstriatum ventrale of domestic chicks after filial imprinting: an in vivo microdialysis study. J. Neurochem. 66, 1167–1173 (1996).

  14. 14.

    & The infant rat separation paradigm: A novel test for novel anxiolytics. Trends Pharmacol. Sci. 12, 402–404 (1991).

  15. 15.

    & The locus ceruleus, norepinephrine, and memory in newborns. Br. Res. Bull. 35, 467–472 (1994).

  16. 16.

    & Spatial distribution of [14C]2-deoxyglucose uptake in the glomerular layer of the rat olfactory bulb following early odor preference learning. J. Comp. Neurol. 376, 557–566 (1996).

  17. 17.

    & Oxytocin and infant-mother bonding in rats. Behav. Neurosci. 110, 583– 592 (1996).

  18. 18.

    , & Neural consequences of environmental enrichment. Nature Rev. Neurosci. 1, 191–198 (2000).

  19. 19.

    & in Parental Care in Mammals (eds Gubernick, D. J. & Klopfer, P. H.) 1– 76 (Plenum, New York, 1981).

  20. 20.

    in The Physiology of Reproduction (eds Knobil, E. & Neill, J.) 221–302 (Raven, New York, 1994).

  21. 21.

    A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114, 930– 940 (1984).

  22. 22.

    , & The habenular complex mediates hormonal stimulation of maternal behavior in rats. Behav. Neurosci. 106, 853–865 (1992).

  23. 23.

    & Neuroanatomical circuitry for mammalian maternal behavior. Ann. NY Acad. Sci. 807 , 101–125 (1997).

  24. 24.

    , , , & Axon-sparing lesions of the preoptic area and substantia innominata disrupt maternal behavior in rats. Behav. Neurosci. 102, 381–395 (1988).

  25. 25.

    & Prolactin (PRL) regulation of maternal behavior in rats: Bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology 126, 837–848 (1990).

  26. 26.

    , , , & Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 139, 4102–4107 (1998).

  27. 27.

    , , & Oxytocin induces maternal behaviour in virgin female rats. Science 216, 648– 649 (1982).

  28. 28.

    in Mammalian Parenting, Biochemical, Neurobiological, and Behavioral Determinants (eds Krasnegor, N. & Bridges, R.) 260–280 (Oxford Univ. Press, New York, 1990).

  29. 29.

    , , , & Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 108, 1163– 1171 (1994).

  30. 30.

    , , , & The olfactory bulb: A critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience 72, 1083–1088 ( 1996).

  31. 31.

    & Olfactory regulation of maternal behavior in rats: II. Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins . J. Comp. Physiol. Psychol. 86, 233– 246 (1974).

  32. 32.

    , , & Push-pull perfusion and microdialysis studies of central oxytocin and vasopressin release in freely moving rats during pregnancy, parturition, and lactation. NY Acad. Sci. 652, 326–339 ( 1992).

  33. 33.

    et al. The action of oxytocin originating in the hypothalamic paraventricular nucleus on the mitral and granule cells in the rat main olfactory bulb. Neuroscience 72, 1073–1082 (1996).

  34. 34.

    , , , & in Advances in Study of Behavior (eds Rosenblatt, J. & Snowdon, C.) 385–422 (Academic, San Diego, 1996).

  35. 35.

    , , & Vaginal stimulation: An important determinant of maternal bonding in sheep. Science 219, 81–83 ( 1983).

  36. 36.

    , & Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes. Physiol. Behav. 50, 595–600 (1991).

  37. 37.

    , , & Microdialysis measurement of oxytocin, aspartate, GABA and glutamate release from the olfactory bulb of sheep during vaginocervical stimulation. Brain Res. 442, 171–177 (1988).

  38. 38.

    , & Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 46, 56–61 (1987).

  39. 39.

    & Oxytocin facilitation of maternal behavior in sheep. Ann. NY Acad. Sci. 652, 83–101 (1992).

  40. 40.

    , , , & Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behav. Neurosci. 106, 427– 432 (1992).

  41. 41.

    , , & Changes in oxytocin immunoreactivity and mRNA expression in the sheep brain during pregnancy, parturition and lactation and in response to oestrogen and progesterone. J. Neuroendocrinol. 5, 435 –444 (1993).

  42. 42.

    et al. Previous maternal experience potentiates the effect of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus. Eur. J. Neurosci. 11, 3725–3737 (1999).

  43. 43.

    et al. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 44, 383– 395 (1997).

  44. 44.

    , , , & The role of oxytocin release in the paraventricular nucleus in the control of maternal behaviour in the sheep. J. Neuroendocrinol. 8, 163– 177 (1996).

  45. 45.

    , , , & Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: changes with maternal experience and effects on acetylcholine, γ-aminobutyric acid, glutamate and noradrenaline release. Brain Res. 669 , 197–206 (1995).

  46. 46.

    A cortical–hippocampal system for declarative memory. Nature Rev. Neurosci. 1, 41–50 (2000).

  47. 47.

    , & Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256, 833–836 (1992).

  48. 48.

    et al. Formation of olfactory memories mediated by nitric oxide. Nature 388, 670–674 ( 1997).

  49. 49.

    , , , & Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure. Neuroscience 87, 583–590 (1998).

  50. 50.

    , , & Release of classical neurotransmitters and nitric oxide in the rat olfactory bulb, evoked by vaginocervical stimulation and potassium, varies with the oestrus cycle. Eur. J. Neurosci. 12, 80– 88 (2000).

  51. 51.

    Monogamy in mammals. Q. Rev. Biol. 52, 39 –69 (1977).

  52. 52.

    in American Zoology Nebraska Symposium on Motivation (ed. Leger, D. W.) 1–50 (Nebraska Univ. Press, Lincoln, Nebraska, 1988).

  53. 53.

    , & Physiological substrates of mammalian monogamy: The prairie vole model. Neurosci. Biobehav. Rev. 19, 303–314 (1995).

  54. 54.

    Oxytocin and rodent sociosexual responses: from behavior to gene expression . Neurosci. Biobehav. Rev. 19, 315– 324 (1995).

  55. 55.

    , , & Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J. Neuroendocrinol. 6, 247–250 (1994).

  56. 56.

    , , , & A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545–548 (1993).

  57. 57.

    & A gender specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles . Behav. Neurosci. 109, 782– 789 (1995).

  58. 58.

    , , & Oxytocin and complex social behaviors: species comparisons. Psychopharmacol. Bull. 29, 409–414 ( 1993).

  59. 59.

    , , & Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: Behavioral consequences. Behav. Neurosci. 111 , 599–605 (1997).

  60. 60.

    , , & Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: A quantitative comparative study. J. Comp. Neurol. 366, 726–737 (1996).

  61. 61.

    & Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl Acad. Sci. USA 89, 5981– 5985 (1992).

  62. 62.

    , & Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14, 5381–5392 ( 1994).

  63. 63.

    , , , & Species differences in central oxytocin receptor gene expression: Comparative analysis of promoter sequences. J. Neuroendocrinol. 8, 777–783 ( 1996).

  64. 64.

    , & Molecular and cellular mechanisms of monogamy. Horm. Behav. (in the press).

  65. 65.

    et al. Manipulation of vasopressin receptor expression in adult brain using an AAV viral vector. Soc. Neurosci. Annu. Meeting 30, 373.11 (2000).

  66. 66.

    Oxytocin and vasopressin receptors and species-typical social behaviors. Horm. Behav. 36, 212–221 (1999).

  67. 67.

    et al. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles: A mechanism for pair bonding. Behav. Neurosci. 113, 602–611 ( 1999).

  68. 68.

    , , , & Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles. Behav. Neurosci. 114, 173–183 ( 2000).

  69. 69.

    et al. Associative process in addiction and reward. Ann. NY Acad Sci. 877, 412–438 (1999).

  70. 70.

    , , , & Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400, 766–768 (1999).

  71. 71.

    , , , & in Parental Care: Evolution, Mechanisms, and Adaptive Significance (eds Rosenblatt, J. S. & Snowdon, C. T.) 385–416 (Academic, San Diego, 1996 ).

  72. 72.

    , , , & Male stimuli are necessary for female sexual behavior and uterine growth in prairie voles (Microtus ochrogaster ). Horm. Behav. 21, 74– 82 (1987).

  73. 73.

    & in Oxytocin: Clinical and Laboratory Studies (eds Amico, J. & Robinson, A. G.) 359– 371 (Elsevier, New York, 1985).

  74. 74.

    , , , & Social amnesia in mice lacking the oxytocin gene. Nature Genet. 25, 284–288 (2000).

  75. 75.

    , , , & Neural activation in the socially amnestic mouse . Soc. Neurosci. Annu. Meeting 30, 373.8 (2000).

  76. 76.

    & Effects of morphine and naloxone on separation distress and approach attachment: Evidence for opiate mediation of social affect. Pharmacol. Biochem. Behav. 9, 213–220 (1978).

  77. 77.

    , , & Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. Dev. Psychobiol. 28, 71–84 (1995).

  78. 78.

    Oxytocin: a neuropeptide for affiliation — evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 17, 3–33 (1992 ).

  79. 79.

    & in Motherhood in Human and Non-Human Primates (eds Pryce, C. R. & Martin, R. D.) 87– 93 (Karger, Basel, 1994).

  80. 80.

    Regional changes in brain oxytocin receptor post-partum: Time-course and relationship to maternal behavior. J. Neuroendocrinol. 2, 539–545 (1990).

  81. 81.

    et al. Learning of olfactory cues is not necessary for early lamb recognition by the mother. Phys. Behav. 69, 405–412 (2000).

  82. 82.

    Oxytocin, motherhood, and bonding. Exp. Physiol. 85 , 111S–124S (2000).

  83. 83.

    , & B-endorphin concentrations in CSF of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14, 155–161 (1989).

  84. 84.

    & Endogenous opiates regulate oxytocin but not vasopressin secretion from the neurohypophysis. Nature 298, 161–162 ( 1982).

  85. 85.

    , , , & Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic area. Behav. Neurosci. 108, 1163– 1171 (1994).

  86. 86.

    , & Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats. Physiol. Behav. 48, 211–214 ( 1990).

  87. 87.

    , , , & Mesotelencephalic dopamine system and and reproductive behavior in the female rat: Effects of ventral tegmental 6-OHDA lesions on maternal and sexual responsiveness. Behav. Neurosci. 105, 588–598 (1991).

  88. 88.

    & Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol. Behav. 67, 659–669 (1999).

  89. 89.

    Affective Neuroscience (Oxford Univ. Press, New York, 1998).

  90. 90.

    , , & Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res. 555, 220–232 (1991).

  91. 91.

    et al. Vasopressin in the forebrain of common marmosets (Callithrix jacchus): Studies with in situ hybridization, immunocytochemistry and receptor autoradiography. Brain Res. 768, 147–156 (1997).

  92. 92.

    et al. Acute effects of cocaine on human brain activity and emotion . Neuron 19, 591–611 (1997).

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Acknowledgements

The authors are supported by NSF and NIMH. The authors thank M. Davis for his comments on an early draft of the manuscript and Z. Wang for his contributions to many of the ideas and results described.

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  1. Center for Behavioral Neuroscience, 954 Gatewood Road Northeast, Emory University, Atlanta , Georgia 30329, USA.

    • Thomas R. Insel
    •  & Larry J. Young

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https://doi.org/10.1038/35053579

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