Specifying the neurobiological basis of human attachment: Brain, hormones, and behavior in synchronous and intrusive mothers

Neuropsychopharmacology

Volumn 36, Issue 13, 2011, Pages 2603-2615

  Atzil, Shir ^a,b   Hendler, Talma ^b,c   Feldman, Ruth ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

attachment; emotion regulation; imaging; maternal behavior; motivation; synchrony

Indexed keywords

NEUROPEPTIDE; OXYTOCIN;

ADULT; AMYGDALOID NUCLEUS; ANALYSIS; ANXIETY; ARTICLE; ASSOCIATION; EMOTION; EMPATHY; FEMALE; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFANT; INTRUSIVE MOTHER; MATERNAL BEHAVIOR; MOTHER; MOTHER CHILD RELATION; MOTIVATION; NUCLEUS ACCUMBENS; OXYTOCIN BLOOD LEVEL; PRIORITY JOURNAL; REWARD; SYNCHRONOUS MOTHER; THEORY OF MIND; VIDEORECORDING; VIGNETTE;

ADULT; BRAIN; FEMALE; HUMANS; INFANT; MALE; MATERNAL BEHAVIOR; MOTHER-CHILD RELATIONS; OXYTOCIN; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 80855137956     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.172     Document Type: Article

References (84)

1. ACOG (2006). ACOG Committee Opinion No. 343: psychosocial risk factors: perinatal screening and intervention. Obstet Gynecol 108: 469-477.
2. Adolphs R, Damasio H, Tranel D, Cooper G, Damasio AR (2000). A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J Neurosci 20: 2683-2690. (Pubitemid 30220356)
3. Andersson L, Sundstrom-Poromaa I, Wulff M, Astrom M, Bixo M (2006). Depression and anxiety during pregnancy and six months postpartum: a follow-up study. Acta Obstet Gynecol Scand 85: 937-944. (Pubitemid 44114952)
4. Aron A, Fisher H, Mashek DJ, Strong G, Li H, Brown LL (2005). Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol 94: 327-337. (Pubitemid 40923250)
5. Assaf M, Kahn I, Pearlson GD, Johnson MR, Yeshurun Y, Calhoun VD et al (2009). Brain activity dissociates mentalization from motivation during an interpersonal competitive game. Brain Imag Behav 3: 24-37.
6. Barrett J, Fleming AS (2011). Annual Research Review: all mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. J Child Psychol Psychiatry 52: 368-397.
7. Bartels A, Zeki S (2004). The neural correlates of maternal and romantic love. NeuroImage 21: 1155-1166. (Pubitemid 38314977)
8. Beck AT (1978). Beck Depression Inventory. Harcourt Brace Jovanovich. Psychological Corporation: San Antonio, TX.
9. Bowlby J (1958). The nature of the child's tie to his mother. Int J Psychoanal 39: 350-373.
10. Bowlby J (1969). Attachment and Loss. Basic Books: New York, NY.
11. Bryant RA, Kemp AH, Felmingham KL, Liddell B, Olivieri G, Peduto A et al (2008). Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: an fMRI study. Hum Brain Mapp 29: 517-523. (Pubitemid 351706800)
12. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26: 321-352. (Pubitemid 34555410)
13. Carter CS (2007). Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res 176: 170-186. (Pubitemid 44879628)
14. Carter CS, Ahnert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW et al (2005). Attachment and Bonding: A New Synthesis. The MIT Press: Boston, MA.
15. Champagne FA (2008). Epigenetic mechanisms and the transgenera-tional effects of maternal care. Front Neuroendocrinol 29: 386-397.
16. Champagne FA, Chretien P, Stevenson CW, Zhang TY, Gratton A, Meaney MJ (2004). Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci 24: 4113-4123. (Pubitemid 38620786)
17. Dayan E, Casile A, Levit-Binnun N, Giese MA, Hendler T, Flash T (2007). Neural representations of kinematic laws of motion: evidence for action-perception coupling. Proc Natl Acad Sci USA 104: 20582-20587.
18. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC (2007). Oxytocin improves 'mind-reading' in humans. Biol Psychiatry 61: 731-733.
19. Douglas AJ (2010). Baby love? Oxytocin-dopamine interactions in mother-infant bonding. Endocrinology 151: 1978-1980.
20. Feldman R (2007). Parent-infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. J Child Psychol Psychiatry 48: 329-354. (Pubitemid 46372122)
21. Feldman R (2010). The relational basis of adolescent adjustment: trajectories of mother-child interactive behaviors from infancy to adolescence shape adolescents' adaptation. Attach Hum Dev 12: 173-192.
22. Feldman R, Eidelman AI (2004). Parent-infant synchrony and the social-emotional development of triplets. Dev Psychol 40: 1133-1147. (Pubitemid 39454162)
23. Feldman R, Eidelman AI (2007). Maternal postpartum behavior and the emergence of infant-mother and infant-father synchrony in preterm and full-term infants: the role of neonatal vagal tone. Dev Psychobiol 49: 290-302. (Pubitemid 46640390)
24. Feldman R, Gordon I, Schneiderman I, Weisman O, Zagoory-Sharon O (2010a). Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35: 1133-1141.
25. Feldman R, Gordon I, Zagoory-Sharon O (2010b). The cross-generation transmission of oxytocin in humans. Horm Behav 58: 669-676.
26. Feldman R, Gordon I, Zagoory-Sharon O (2011). Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: considering stress and affiliation components of human bonding. Dev Sci 14: 752-761.
27. Feldman R, Granat A, Pariente C, Kanety H, Kuint J, Gilboa-Schechtman E (2009). Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. J Am Acad Child Adolesc Psychiatry 48: 919-927.
28. Feldman R, Singer M, Zagoory O (2010c). Touch attenuates infants' physiological reactivity to stress. Dev Sci 13: 271-278.
29. Feldman R, Weller A, Zagoory-Sharon O, Levine A (2007b). Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol Sci 18: 965-970.
30. Fleming AS, Korsmit M (1996). Plasticity in the maternal circuit: effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. Behav Neurosci 110: 567-582. (Pubitemid 26227103)
31. Friston KJ, Frith CD, Liddle PF, Frackowiak RS (1993). Functional connectivity: the principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab 13: 5-14. (Pubitemid 23016598)
32. Gallagher HL, Frith CD (2003). Functional imaging of 'theory of mind'. Trends Cogn Sci 7: 77-83.
33. Gilboa A, Shalev AY, Laor L, Lester H, Louzoun Y, Chisin R et al (2004). Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder. Biol Psychiatry 55: 263-272. (Pubitemid 38117162)
34. Goebel R, Esposito F, Formisano E (2006). Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp 27: 392-401. (Pubitemid 43787637)
35. Gordon I, Zagoory-Sharon O, Leckman JF, Feldman R (2010a). Oxytocin and the development of parenting in humans. Biol Psychiatry 68: 377-382.
36. Gordon I, Zagoory-Sharon O, Leckman JF, Feldman R (2010b). Oxytocin, cortisol, and triadic family interactions. Physiol Behav 101: 679-684.
37. Gordon I, Zagoory-Sharon O, Schneiderman I, Leckman JF, Weller A, Feldman R (2008). Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress. Psychophysiology 45: 349-352. (Pubitemid 351502505)
38. Greicius MD, Krasnow B, Reiss AL, Menon V (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100: 253-258. (Pubitemid 36078061)
39. Hansen S (1994). Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit. Physiol Behav 55: 615-620. (Pubitemid 24104385)
40. Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K (1991). The effects of 6-OHDA-induced dopamine depletions in the ventral or dorsal striatum on maternal and sexual behavior in the female rat. Pharmacol Biochem Behav 39: 71-77.
41. Hurlemann R, Patin A, Onur OA, Cohen MX, Baumgartner T, Metzler S et al (2010). Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J Neurosci 30: 4999-5007.
42. Iacoboni M, Dapretto M (2006). The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7: 942-951.
43. Insel TR, Young L, Wang Z (1997). Central oxytocin and reproductive behaviours. Rev Reprod 2: 28-37. (Pubitemid 27165964)
44. Insel TR, Young LJ (2001). The neurobiology of attachment. Nat Rev Neurosci 2: 129-136. (Pubitemid 33673367)
45. Isabella RA, Belsky J (1991). Interactional synchrony and the origins of infant-mother attachment: a replication study. Child Dev 62: 373-384.
46. Kaitz M, Maytal H (2005). Interactions between anxious mothers and their infants:an integration of theory and research findings. Infant Ment Health J 26: 570-597.
47. Keer SE, Stern JM (1999). Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 67: 659-669.
48. Keysers C, Fadiga L (2008). The mirror neuron system: new frontiers. Soc Neurosci 3: 193-198.
49. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005). Oxytocin increases trust in humans. Nature 435: 673-676. (Pubitemid 40825511)
50. Leckman JF, Feldman R, Swain JE, Eicher V, Thompson N, Mayes LC (2004). Primary parental preoccupation: circuits, genes, and the crucial role of the environment. J Neural Transm 111: 753-771. (Pubitemid 38916274)
51. Leckman JF, Herman AE (2002). Maternal behavior and developmental psychopathology. Biol Psychiatry 51: 27-43. (Pubitemid 34093792)
52. Leckman JF, Mayes LC (1999). Preoccupations and behaviors associated with romantic and parental love. Perspectives on the origin of obsessive-compulsive disorder. Child Adolesc Psychiatr Clin N Am 8: 635-665. (Pubitemid 29360212)
53. Leckman JF, Mayes LC, Feldman R, Evans DW, King RA, Cohen DJ (1999). Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive-compulsive disorder. Acta Psychiatr Scand Suppl 396: 1-26. (Pubitemid 29374413)
54. Lee A, Clancy S, Fleming AS (2000). Mother rats bar-press for pups: effects of lesions of the mpoa and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav Brain Res 108: 215-231. (Pubitemid 30084838)
55. Levine A, Zagoory-Sharon O, Feldman R, Weller A (2007). Oxytocin during pregnancy and early postpartum: individual patterns and maternal-fetal attachment. Peptides 28: 1162-1169. (Pubitemid 46843394)
56. Li M, Fleming AS (2003). Differential involvement of nucleus accumbens shell and core subregions in maternal memory in postpartum female rats. Behav Neurosci 117: 426-445. (Pubitemid 36686961)
57. Liddell BJ, Brown KJ, Kemp AH, Barton MJ, Das P, Peduto A et al (2005). A direct brainstem-amygdala-cortical 'alarm' system for subliminal signals of fear. NeuroImage 24: 235-243. (Pubitemid 39611044)
58. Lorberbaum JP, Newman JD, Horwitz AR, Dubno JR, Lydiard RB, Hamner MB et al (2002). A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 51: 431-445. (Pubitemid 34260963)
59. MacLean MR, Raizada MK, Sumners C (1990). The influence of angiotensin II on catecholamine synthesis in neuronal cultures from rat brain. Biochem Biophys Res Commun 167: 492-497. (Pubitemid 20113206)
60. MacLean PD, Newman JD (1988). Role of midline frontolimbic cortex in production of the isolation call of squirrel monkeys. Brain Res 450: 111-123.
61. Meaney MJ (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24: 1161-1192. (Pubitemid 32695257)
62. Murphy MR, MacLean PD, Hamilton SC (1981). Species-typical behavior of hamsters deprived from birth of the neocortex. Science 213: 459-461. (Pubitemid 11023970)
63. Noriuchi M, Kikuchi Y, Senoo A (2008). The functional neuroanatomy of maternal love: mother's response to infant's attachment behaviors. Biol Psychiatry 63: 415-423. (Pubitemid 351146649)
64. Oxley G, Fleming AS (2000). The effects of medial preoptic area and amygdala lesions on maternal behavior in the juvenile rat. Dev Psychobiol 37: 253-265.
65. Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA (1994). Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108: 1163-1171.
66. Pessoa L, Kastner S, Ungerleider LG (2002). Attentional control of the processing of neural and emotional stimuli. Brain Res Cogn Brain Res 15: 31-45. (Pubitemid 35335790)
67. Rizzolatti GCL (2005). Mirror neuron: a neurological approach to empathy. In: Changeux ARDJ-P, Singer W, Christen Y (eds). Neurobiology of Human Values. Springer-Verlag: Berlin, Heidelberg. pp 107-123.
68. Shahrokh DK, Zhang TY, Diorio J, Gratton A, Meaney MJ (2010). Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151: 2276-2286.
69. Silverman ME, Loudon H, Safier M, Protopopescu X, Leiter G, Liu X et al (2007). Neural dysfunction in postpartum depression: an FMRI pilot study. CNS Spectr 12: 853-862. (Pubitemid 350247190)
70. Slotnick BM (1967). Disturbances of maternal behavior in the rat following lesions of the cingulate cortex. Behaviour 29: 204-236.
71. Spielberger CDGR, Lushene SHRE. (1970). Manual for the State-Trait Anxiety Inventory. Palo Alto Consulting Psychologist Press: Palo Alto, CA.
72. Sroufe LA (2005). Attachment and development: a prospective, longitudinal study from birth to adulthood. Attach Hum Dev 7: 349-367. (Pubitemid 43123700)
73. Stamm JS (1955). The function of the median cerebral cortex in maternal behavior of rats. J Comp Physiol Psychol 48: 347-356.
74. Strathearn L, Fonagy P, Amico J, Montague PR (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 34: 2655-2666.
75. Swain JE, Lorberbaum JP, Kose S, Strathearn L (2007). Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry 48: 262-287. (Pubitemid 46372121)
76. Toscano JE, Bauman MD, Mason WA, Amaral DG (2009). Interest in infants by female rhesus monkeys with neonatal lesions of the amygdala or hippocampus. Neuroscience 162: 881-891.
77. Tronick EZ (1989). Emotions and emotional communication in infants. Am Psychol 44: 112-119.
78. Tsafrir D, Tsafrir I, Ein-Dor L, Zuk O, Notterman DA, Domany E (2005). Sorting points into neighborhoods (SPIN): data analysis and visualization by ordering distance matrices. Bioinformatics 21: 2301-2308. (Pubitemid 40731583)
79. Vernotica EM, Rosenblatt JS, Morrell JI (1999). Microinfusion of cocaine into the medial preoptic area or nucleus accumbens transiently impairs maternal behavior in the rat. Behav Neurosci 113: 377-390. (Pubitemid 29230946)
80. Vesga-Lopez O, Blanco C, Keyes K, Olfson M, Grant BF, Hasin DS (2008). Psychiatric disorders in pregnant and postpartum women in the United States. Arch Gen Psychiatry 65: 805-815. (Pubitemid 351957706)
81. Vollm BA, Taylor AN, Richardson P, Corcoran R, Stirling J, McKie S et al (2006). Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage 29: 90-98. (Pubitemid 41828033)
82. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al (2004). Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854. (Pubitemid 38989508)
83. Weisman O, Zagoory-Sharon O, Feldman R (2011). Intranasal Oxytocin Improves the Autonomic, Hormonal and Social basis of Fatherhood. Poster Presentation at the 10th World Congress of Biological Psychiatry. Prague, Czech Republic.
84. Zaretsky M, Mendelsohn A, Mintz M, Hendler T (2010). In the eye of the beholder: internally driven uncertainty of danger recruits the amygdala and dorsomedial prefrontal cortex. J Cogn Neurosci 22: 2263-2275.