The maternal brain and its plasticity in humans

Hormones and Behavior

Volumn 77, Issue , 2016, Pages 113-123

  Kim, Pilyoung ^a   Strathearn, Lane ^b   Swain, James E ^c  

^a UNIVERSITY OF DENVER   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Attachment; Brain imaging; Caregiving; fMRI; Intervention; Maternal; Neural plasticity; Oxytocin; Parenting; Postpartum psychopathology

Indexed keywords

DOPAMINE; OXYTOCIN;

AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; CONNECTOME; CORPUS STRIATUM; EMOTIONALITY; EMPATHY; EXECUTIVE FUNCTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFERIOR FRONTAL GYRUS; INSULA; MIDDLE FRONTAL GYRUS; MOTHER CHILD RELATION; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PARENTAL BEHAVIOR; PARENTAL SENSITIVITY; POSTCENTRAL GYRUS; POSTTRAUMATIC STRESS DISORDER; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PUERPERAL DEPRESSION; PUERPERIUM; REWARD; RISK FACTOR; SENSORY STIMULATION; SUBSTANCE ABUSE; SUPERIOR TEMPORAL GYRUS; THALAMUS; VAGINAL DELIVERY; BRAIN; FEMALE; MATERNAL BEHAVIOR; PATHOPHYSIOLOGY; PHYSIOLOGY;

BRAIN; FEMALE; HUMANS; MATERNAL BEHAVIOR; MOTHER-CHILD RELATIONS; NEURONAL PLASTICITY; POSTPARTUM PERIOD;

EID: 84956593781     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.08.001     Document Type: Article

References (180)

1. Aharon I., Etcoff N., Ariely D., Chabris C.F., O'Connor E., Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 2001, 32:537-551.
2. American Psychiatric Association Diagnostic and statistical manual of mental disorders 2000, Washington, DC. 4th ed.
3. Anda R.F., Felitti V.J., Bremner J.D., Walker J.D., Whitfield C., Perry B.D., Dube S.R., Giles W.H. The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. Eur. Arch. Psychiatry Clin. Neurosci. 2006, 256:174-186.
4. Apter-Levy Y., Feldman M., Vakart A., Ebstein R.P., Feldman R. Impact of maternal depression across the first 6 years of life on the child's mental health, social engagement, and empathy: The moderating role of oxytocin. Am. J. Psychiatry 2013, 170:1161-1168.
5. Atkinson L., Leung E., Goldberg S., Benoit D., Poulton L., Myhal N., Blokland K., Kerr S. Attachment and selective attention: disorganization and emotional Stroop reaction time. Dev. Psychopathol. 2009, 21:99-126.
6. Atzil S., Hendler T., Feldman R. Specifying the neurobiological basis of human attachment: brain, hormones, and behavior in synchronous and intrusive mothers. Neuropsychopharmacology 2011, 36:2603-2615.
7. Atzil S., Hendler T., Zagoory-Sharon O., Winetraub Y., Feldman R. Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin. J. Am. Acad. Child Adolesc. Psychiatry 2012, 51:798-811.
8. Atzil S., Hendler T., Feldman R. The brain basis of social synchrony. Soc. Cogn. Affect. Neurosci. 2014, 9:1193-1202.
9. Bagner D.M., Pettit J.W., Lewinsohn P.M., Seeley J.R. Effect of maternal depression on child behavior: a sensitive period?. J. Am. Acad. Child Adolesc. Psychiatry 2010, 49:699-707.
10. Barrett J., Wonch K.E., Gonzalez A., Ali N., Steiner M., Hall G.B., Fleming A.S. Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Soc. Neurosci. 2012, 7:252-268.
11. Bos P.A., Hermans E.J., Montoya E.R., Ramsey N.F., van Honk J. Testosterone administration modulates neural responses to crying infants in young females. Psychoneuroendocrinology 2010, 35:114-121.
12. Bowlby J. Attachment 1969, Basic Books, New York. 2nd ed.
13. Britton J.R., Britton H.L., Gronwaldt V. Breastfeeding, sensitivity, and attachment. Pediatrics 2006, 118:e1436-e1443.
14. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
15. Bureau J.F., Easterbrooks M.A., Lyons-Ruth K. Maternal depressive symptoms in infancy: unique contribution to children's depressive symptoms in childhood and adolescence?. Dev. Psychopathol. 2009, 21:519-537.
16. Caldji C., Hellstrom I.C., Zhang T.-Y., Diorio J., Meaney M.J. Environmental regulation of the neural epigenome. FEBS Lett. 2011, 585:2049-2058.
17. Champagne F.A. Maternal imprints and the origins of variation. Horm. Behav. 2011, 60:4-11.
18. Champagne F., Meaney M.J. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog. Brain Res. 2001, 133:287-302.
19. Champagne F.A., Meaney M.J. Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav. Neurosci. 2007, 121:1353-1363.
20. Champagne F.A., Weaver I.C., Diorio J., Sharma S., Meaney M.J. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 2003, 144:4720-4724.
21. Champagne F.A., Chretien P., Stevenson C.W., Zhang T.Y., Gratton A., Meaney M.J. Variations in nucleus accumbens dopamine associated with individual differences in maternal behav. in the rat. J. Neurosci. 2004, 24:4113-4123.
22. Cohen L., Mizrahi A. Plasticity during motherhood: changes in excitatory and inhibitory layer 2/3 neurons in auditory cortex. J. Neurosci. 2015, 35:1806-1815.
23. Cornish A.M., McMahon C.A., Ungerer J.A., Barnett B., Kowalenko N., Tennant C. Postnatal depression and infant cognitive and motor development in the second postnatal year: the impact of depression chronicity and infant gender. Infant Behav. Dev. 2005, 28:407-417.
24. Cuthbert B.N. The RDoC framework: facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology. World Psychiatry 2014, 13:28-35.
25. Deal L.W., Holt V.L. Young maternal age and depressive symptoms: results from the 1988 National Maternal and Infant Health Survey. Am. J. Public Health 1998, 88:266-270.
26. Decety J. The neural pathways, development and functions of empathy. Curr. Opin. Behav. Sci. 2015, 3:1-6.
27. Delgado M.R., Nystrom L.E., Fissell C., Noll D.C., Fiez J.A. Tracking the hemodynamic responses to reward and punishment in the striatum. J. Neurophysiol. 2000, 84:3072-3077.
28. Dube S.R., Felitti V.J., Dong M., Chapman D.P., Giles W.H., Anda R.F. Childhood abuse, neglect, and household dysfunction and the risk of illicit drug use: the adverse childhood experiences study. Pediatrics 2003, 111:564-572.
29. Evans J., Heron J., Francomb H., Oke S., Golding J. Cohort study of depressed mood during pregnancy and after childbirth. BMJ 2001, 323:257-260.
30. Fan Y., Duncan N.W., de Greck M., Northoff G. Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci. Biobehav. Rev. 2011, 35:903-911.
31. Feldman R. Parent-infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. J. Child Psychol. Psychiatry 2007, 48:329-354.
32. Feldman R., Gordon I., Zagoory-Sharon O. The cross-generation transmission of oxytocin in humans. Horm. Behav. 2010, 58:669-676.
33. Feldman R., Weller A., Leckman J.F., Kuint J., Eidelman A.I. The nature of the mother's tie to her infant: maternal bonding under conditions of proximity, separation, and potential loss. J. Child Psychol. Psychiatry 1999, 40:929-939.
34. Feldman R., Granat A., Pariente C., Kanety H., Kuint J., Gilboa-Schechtman E. Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. J. Am. Acad. Child Adolesc. Psychiatry 2009, 48:919-927.
35. Feygin D.L., Swain J.E., Leckman J.F. The normalcy of neurosis: evolutionary origins of obsessive-compulsive disorder and related behaviors. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:854-864.
36. Field T., Healy B., Goldstein S., Perry S., Bendell D., Schanberg S., Zimmerman E.A., Kuhn C. Infants of depressed mothers show "depressed" behavior even with nondepressed adults. Child Dev. 1988, 59:1569-1579.
37. Fleming A.S., Kraemer G.W., Gonzalez A., Lovic V., Rees S., Melo A. Mothering begets mothering: the transmission of behavior and its neurobiology across generations. Pharmacol. Biochem. Behav. 2002, 73:61-75.
38. Frith U., Frith C.D. Development and neurophysiology of mentalizing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:459-473.
39. Frith C.D., Frith U. The neural basis of mentalizing. Neuron 2006, 50:531-534.
40. Ganzel B.L., Kim P., Glover G.H., Temple E. Resilience after 9/11: multimodal neuroimaging evidence for stress-related change in the healthy adult brain. NeuroImage 2008, 40:788-795.
41. Gavin N.I., Gaynes B.N., Lohr K.N., Meltzer-Brody S., Gartlehner G., Swinson T. Perinatal depression: a systematic review of prevalence and incidence. Obstet. Gynecol. 2005, 106:1071-1083.
42. Gaynes B.N., Gavin N., Meltzer-Brody S., Lohr K.N., Swinson T., Gartlehner G., Brody S., Miller W.C. Perinatal depression: prevalence, screening accuracy, and screening outcomes. Evid. Rep. Technol. Assess. (Summ.) 2005, 1-8.
43. Gee C.B., Rhodes J.E. Adolescent mothers' relationship with their children's biological fathers: social support, social strain, and relationship continuity. J. Fam. Psychol. 2003, 17:370-383.
44. Gill K.E., Beveridge T.J.R., Smith H.R., Porrino L.J. The effects of rearing environment and chronic methylphenidate administration on behavior and dopamine receptors in adolescent rats. Brain Res. 2013, 1527:67-78.
45. Glynn L.M. Giving birth to a new brain: hormone exposures of pregnancy influence human memory. Psychoneuroendocrinology 2010, 35:1148-1155.
46. Gonzalez A., Jenkins J.M., Steiner M., Fleming A.S. Maternal early life experiences and parenting: the mediating role of cortisol and executive function. J. Am. Acad. Child Adolesc. Psychiatry 2012, 51:673-682.
47. Gotlib I.H., Whiffen V.E., Mount J.H., Milne K., Cordy N.I. Prevalence rates and demographic characteristics associated with depression in pregnancy and the postpartum. J. Consult. Clin. Psychol. 1989, 57:269-274.
48. Gotlib I.H., Whiffen V.E., Wallace P.M., Mount J.H. Prospective investigation of postpartum depression: factors involved in onset and recovery. J. Abnorm. Psychol. 1991, 100:122-132.
49. Grace S.L., Evindar A., Stewart D.E. The effect of postpartum depression on child cognitive development and behavior: a review and critical analysis of the literature. Arch. Womens Ment. Health 2003, 6:263-274.
50. Groenewold N.A., Opmeer E.M., de Jonge P., Aleman A., Costafreda S.G. Emotional valence modulates brain functional abnormalities in depression: evidence from a meta-analysis of fMRI studies. Neurosci. Biobehav. Rev. 2012, 37:152-163.
51. Hall F.S., Wilkinson L.S., Humby T., Inglis W., Kendall D.A., Marsden C.A., Robbins T.W. Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol. Biochem. Behav. 1998, 59:859-872.
52. Halligan S.L., Murray L., Martins C., Cooper P.J. Maternal depression and psychiatric outcomes in adolescent offspring: a 13-year longitudinal study. J. Affect. Disord. 2007, 97:145-154.
53. Hamzei F., Glauche V., Schwarzwald R., May A. Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction. NeuroImage 2012, 59:3364-3372.
54. Harmer A.L.M., Sanderson J., Mertin P. Influence of negative childhood experiences on psychological functioning, support, and parenting for mothers recovering from addiction. Child Abuse Negl. 1999, 23:421-433.
55. Hay D.F., Pawlby S., Waters C.S., Sharp D. Antepartum and postpartum exposure to maternal depression: different effects on different adolescent outcomes. J. Child Psychol. Psychiatry 2008, 49:1079-1088.
56. Heim C., Young L.J., Newport D.J., Mletzko T., Miller A.H., Nemeroff C.B. Lower CSF oxytocin concentrations in women with a history of childhood abuse. Mol. Psychiatry 2009, 14:954-958.
57. Hein G., Singer T. I feel how you feel but not always: the empathic brain and its modulation. Curr. Opin. Neurobiol. 2008, 18:153-158.
58. Hipwell A.E., Kumar R. Maternal psychopathology and prediction of outcome based on mother-infant interaction ratings (BMIS). Br. J. Psychiatry 1996, 169:655-661.
59. Hipwell A.E., Murray L., Ducournau P., Stein A. The effects of maternal depression and parental conflict on children's peer play. Child Care Health Dev. 2005, 31:11-23.
60. Ho S.S., Konrath S., Brown S., Swain J.E. Empathy and stress related neural responses in maternal decision making. Front. Neurosci. 2014, 8:152.
61. Hoffman K.T., Marvin R.S., Cooper G., Powell B. Changing toddlers' and preschoolers' attachment classifications: the Circle of Security intervention. J. Consult. Clin. Psychol. 2006, 74:1017-1026.
62. Hopper J.W., Frewen P.A., van der Kolk B.A., Lanius R.A. Neural correlates of reexperiencing, avoidance, and dissociation in PTSD: symptom dimensions and emotion dysregulation in responses to script-driven trauma imagery. J. Trauma. Stress. 2007, 20:713-725.
63. Iyengar U., Kim S., Martinez S., Fonagy P., Strathearn L. Unresolved trauma in mothers: intergenerational effects and the role of reorganization. Front. Psychol. 2014, 5:966.
64. Joosen K.J., Mesman J., Bakermans-Kranenburg M.J., van IJzendoorn M.H. Maternal sensitivity to infants in various settings predicts harsh discipline in toddlerhood. Attach Hum. Dev. 2012, 14:101-117.
65. Keller H., Lohaus A., Völker S., Elben C., Ball J. Warmth and contingency and their relationship to maternal attitudes toward parenting. J. Genet. Psychol. 2003, 164:275-292.
66. Keren M., Feldman R., Eidelman A.I., Sirota L., Lester B. Clinical interview for high-risk parents of premature infants (CLIP): relations to mother-infant interaction. Infant Ment. Health J. 2003, 24:93-110.
67. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 2005, 62:593-602.
68. Kim P., Bianco H. How motherhood and poverty change the brain. Zero Three 2014, 34:29-36.
69. Kim P., Leckman J.F., Mayes L.C., Feldman R., Wang X., Swain J.E. The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period. Behav. Neurosci. 2010, 124:695-700.
70. Kim P., Leckman J.F., Mayes L.C., Newman M.-A., Feldman R., Swain J.E. Perceived quality of maternal care in childhood and structure and function of mothers' brain. Dev. Sci. 2010, 13:662-673.
71. Kim P., Feldman R., Mayes L.C., Eicher V., Thompson N., Leckman J.F., Swain J.E. Breastfeeding, brain activation to own infant cry, and maternal sensitivity. J. Child Psychol. Psychiatry 2011, 52:907-915.
72. Kim P., Mayes L., Feldman R., Leckman J.F., Swain J.E. Early postpartum parental preoccupation and positive parenting thoughts: relationship with parent-infant interaction. Infant Ment. Health J. 2013, 34:104-116.
73. Kim S., Fonagy P., Allen J., Martinez S.R., Iyengar U., Strathearn L. Mothers who are securely attached during pregnancy show more attuned infant mirroring at 7 months postpartum. Infant Behav. Dev. 2014, 37:491-504.
74. Kim S., Fonagy P., Allen J., Strathearn L. Mothers' unresolved trauma blunts amygdala response to infant distress. Soc. Neurosci. 2014, 9:352-363.
75. Kim S., Iyengar U., Mayes L., Potenza M.N., Rutherford H.J., Strathearn L. Mothers with addictions show reduced reward response to infant cues: can oxytocin reverse this pattern?. Society for Neuroscience 2014, Society for Neuroscience, Washington DC, (p. Poster#: 56.05/X59).
76. Kinsley C.H., Meyer E.A. The construction of the maternal brain: theoretical comment on Kim et al. (2010). Behav. Neurosci. 2010, 124:710-714.
77. Kober H., Barrett L.F., Joseph J., Bliss-Moreau E., Lindquist K., Wager T.D. Functional grouping and cortical-subcortical interactions in emotion: a meta-analysis of neuroimaging studies. NeuroImage 2008, 42:998-1031.
78. Kufahl P.R., Li Z., Risinger R.C., Rainey C.J., Wu G., Bloom A.S., Li S.J. Neural responses to acute cocaine administration in the human brain detected by fMRI. NeuroImage 2005, 28:904-914.
79. Lahey B.B., Michalska K.J., Liu C., Chen Q., Hipwell A.E., Chronis-Tuscano A., Waldman I.D., Decety J. Preliminary genetic imaging study of the association between estrogen receptor-alpha gene polymorphisms and harsh human maternal parenting. Neurosci. Lett. 2012, 525:17-22.
80. Lanius R.A., Frewen P.A., Girotti M., Neufeld R.W.J., Stevens T.K., Densmore M. Neural correlates of trauma script-imagery in posttraumatic stress disorder with and without comorbid major depression: a functional MRI investigation. Psychiatry Res. 2007, 155:45-56.
81. Laurent H.K., Ablow J.C. A cry in the dark: depressed mothers show reduced neural activation to their own infant's cry. Soc. Cogn. Affect. Neurosci. 2012, 7:125-134.
82. Laurent H.K., Stevens A., Ablow J.C. Neural correlates of hypothalamic-pituitary-adrenal regulation of mothers with their infants. Biol. Psychiatry 2011, 70:826-832.
83. Leckman J.F., Mayes L.C. Preoccupations and behaviors associated with romantic and parental love. Perspectives on the origin of obsessive-compulsive disorder. Child Adolesc. Psychiatr. Clin. N. Am. 1999, 8:635-665.
84. Leckman J.F., Feldman R., Swain J.E., Eicher V., Thompson N., Mayes L.C. Primary parental preoccupation: circuits, genes, and the crucial role of the environment. J. Neural Transm. 2004, 111:753-771.
85. Leerkes E.M. Maternal sensitivity during distressing tasks: a unique predictor of attachment security. Infant Behav. Dev. 2011, 34:443-446.
86. Leerkes E.M., Nayena Blankson A., O'Brien M. Differential effects of maternal sensitivity to infant distress and nondistress on social-emotional functioning. Child Dev. 2009, 80:762-775.
87. Leibenluft E., Gobbini M.I., Harrison T., Haxby J.V. Mothers' neural activation in response to pictures of their children and other children. Biol. Psychiatry 2004, 56:225-232.
88. Leuner B., Glasper E.R., Gould E. Parenting and plasticity. Trends Neurosci. 2010, 33:465-473.
89. Logsdon M.C., Birkimer J.C., Simpson T., Looney S. Postpartum depression and social support in adolescents. J. Obstet. Gynecol. Neonatal. Nurs. 2005, 34:46-54.
90. Lorberbaum J.P., Newman J.D., Horwitz A.R., Dubno J.R., Lydiard R.B., Hammer M.B., Bohning D.E., George M.S. A potential role for thalamocingulate circuitry in human maternal behavior. Biol. Psychiatry 2002, 51:431-445.
91. Lovic V., Fleming A.S. Propagation of maternal behavior across generations is associated with changes is non-maternal cognitive and behavioral processes. Behav. Process. 2015, (in press).
92. Lovic V., Keen D., Fletcher P.J., Fleming A.S. Early-life maternal separation and social isolation produce an increase in impulsive action but not impulsive choice. Behav. Neurosci. 2011, 125:481-491.
93. Madigan S., Wade M., Plamondon A., Jenkins J. Maternal abuse history, postpartum depression, and parenting: links with preschoolers' internalizing problems. Infant Ment. Health J. 2015, 36:146-155.
94. Magnuson K.A., Duncan G.J. Parents in poverty. Handbook of Parenting 2002, 95-121. Erlbaum, Mahwah, NJ. 2nd ed. M.H. Bronstein (Ed.).
95. Marcus S., Lopez J.F., McDonough S., Mackenzie M.J., Flynn H., Neal C.R., Gahagan S., Volling B., Kaciroti N., Vazquez D.M. Depressive symptoms during pregnancy: impact on neuroendocrine and neonatal outcomes. Infant Behav. Dev. 2011, 34:26-34.
96. Mayes L.C., Feldman R., Granger R. The effects of polydrug use with and without cocaine on mother infant interaction at 3 and 6 months. Infant Behav. Dev. 1997, 20:489-502.
97. McElwain N.L., Booth-Laforce C. Maternal sensitivity to infant distress and nondistress as predictors of infant-mother attachment security. J. Fam. Psychol. 2006, 20:247-255.
98. McEwen B.S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann. N. Y. Acad. Sci. 2001, 933:265-277.
99. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12:342-348.
100. McLearn K.T., Minkovitz C.S., Strobino D.M., Marks E., Hou W. Maternal depressive symptoms at 2 to 4 months post partum and early parenting practices. Arch. Pediatr. Adolesc. Med. 2006, 160:279-284.
101. Meaney M.J., Brake W., Gratton A. Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse?. Psychoneuroendocrinology 2002, 27:127-138.
102. Melis M.R., Argiolas A. Dopamine and sexual behavior. Neurosci. Biobehav. Rev. 1995, 19:19-38.
103. Michalska K.J., Decety J., Liu C., Chen Q., Martz M.E., Jacob S., Hipwell A.E., Lee S.S., Chronis-Tuscano A., Waldman I.D., Lahey B.B. Genetic imaging of the association of oxytocin receptor gene (OXTR) polymorphisms with positive maternal parenting. Front. Behav. Neurosci. 2014, 8:21.
104. Minnes S., Singer L.T., Humphrey-Wall R., Satayathum S. Psychosocial and behavioral factors related to the post-partum placements of infants born to cocaine-using women. Child Abuse Negl. 2008, 32:353-366.
105. Mitchell J.P. Inferences about mental states. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:1309-1316.
106. Mitchell D.G., Rhodes R.A., Pine D.S., Blair R.J. The contribution of ventrolateral and dorsolateral prefrontal cortex to response reversal. Behav. Brain Res. 2008, 187:80-87.
107. Morgan H.D., Fleming A.S., Stern J.M. Somatosensory control of the onset and retention of maternal responsiveness in primiparous Sprague-Dawley rats. Physiol. Behav. 1992, 51:549-555.
108. Morgan H.D., Watchus J.A., Milgram N.W., Fleming A.S. The long lasting effects of electrical simulation of the medial preoptic area and medial amygdala on maternal behavior in female rats. Behav. Brain Res. 1999, 99:61-73.
109. Moser D.A., Aue T., Wang Z., Rusconi Serpa S., Favez N., Peterson B.S., Schechter D.S. Limbic brain responses in mothers with post-traumatic stress disorder and comorbid dissociation to video clips of their children. Stress 2013, 16:493-502.
110. Moses-Kolko E.L., Perlman S.B., Wisner K.L., James J., Saul A.T., Phillips M.L. Abnormally reduced dorsomedial prefrontal cortical activity and effective connectivity with amygdala in response to negative emotional faces in postpartum depression. Am. J. Psychiatry 2010, 167:1373-1380.
111. Moses-Kolko E.L., Horner M.S., Phillips M.L., Hipwell A.E., Swain J.E. In search of neural endophenotypes of postpartum psychopathology and disrupted maternal caregiving. J. Neuroendocrinol. 2014, 26:665-684.
112. Murray L., Cooper P. Effects of postnatal depression on infant development. Arch. Dis. Child. 1997, 77:99-101.
113. Murray L., Cooper P.J. Postpartum Depression and Child Development 1997, Guilford Press, New York.
114. Musser E.D., Kaiser-Laurent H., Ablow J.C. The neural correlates of maternal sensitivity: an fMRI study. Dev. Cogn. Neurosci. 2012, 2:428-436.
115. Muzik M., Rosenblum K.L., Alfafara E.A., Schuster M.M., Miller N.M., Waddell R.M., Kohler E.S. Mom Power: preliminary outcomes of a group intervention to improve mental health and parenting among high-risk mothers. Arch. Womens Ment. Health 2015, 18:507-521.
116. Noriuchi M., Kikuchi Y., Senoo A. The functional neuroanatomy of maternal love: mother's response to infant's attachment behaviors. Biol. Psychiatry 2008, 63:415-423.
117. Numan M. Motivational systems and the neural circuitry of maternal behavior in the rat. Dev. Psychobiol. 2007, 49:12-21.
118. Numan M. Neurobiology of Social Behavior: Toward an Understanding of the Prosocial and Antisocial Brain 2014, Academic Press. 1st ed.
119. Numan M., Woodside B. Maternity: neural mechanisms, motivational processes, and physiological adaptations. Behav. Neurosci. 2010, 124:715-741.
120. Ochsner K.N., Silvers J.A., Buhle J.T. Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann. N. Y. Acad. Sci. 2012, 1251:E1-E24.
121. Orru G., Pettersson-Yeo W., Marquand A.F., Sartori G., Mechelli A. Using Support Vector Machine to identify imaging biomarkers of neurological and psychiatric disease: a critical review. Neurosci. Biobehav. Rev. 2012, 36:1140-1152.
122. Ouchi H., Ono K., Murakami Y., Matsumoto K. Social isolation induces deficit of latent learning performance in mice: a putative animal model of attention deficit/hyperactivity disorder. Behav. Brain Res. 2013, 238:146-153.
123. Oxley G., Fleming A.S. The effects of medial preoptic area and amygdala lesions on maternal behavior in the juvenile rat. Dev. Psychobiol. 2000, 37:253-265.
124. Pearson R.M., Cooper R.M., Penton-Voak I.S., Lightman S.L., Evans J. Depressive symptoms in early pregnancy disrupt attentional processing of infant emotion. Psychol. Med. 2010, 40:621-631.
125. Pearson R.M., Lightman S.L., Evans J. The impact of breastfeeding on mothers' attentional sensitivity towards infant distress. Infant Behav. Dev. 2011, 34:200-205.
126. Powell B., Cooper G., Hoffman K., Marvin B. The Circle of Security Intervention: Enhancing Attachment in Early Parent-Child Relationships 2014, Guilford Press.
127. Preston S.D. The origins of altruism in offspring care. Psychol. Bull. 2013, 139:1305-1341.
128. Pruessner J.C., Champagne F., Meaney M.J., Dagher A. Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J. Neurosci. 2004, 24:2825-2831.
129. Riem M.M., Bakermans-Kranenburg M.J., Pieper S., Tops M., Boksem M.A., Vermeiren R.R., van Ijzendoorn M.H., Rombouts S.A. Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol. Psychiatry 2011, 70:291-297.
130. Riem M.M., van I.M.H., Tops M., Boksem M.A., Rombouts S.A., Bakermans-Kranenburg M.J. Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal. Eur. Neuropsychopharmacol. 2013, 23:1288-1295.
131. Righetti-Veltema M., Bousquet A., Manzano J. Impact of postpartum depressive symptoms on mother and her 18-month-old infant. Eur. Child Adolesc. Psychiatry 2003, 12:75-83.
132. Rupp H.A., James T.W., Ketterson E.D., Sengelaub D.R., Ditzen B., Heiman J.R. Amygdala response to negative images in postpartum vs nulliparous women and intranasal oxytocin. Soc. Cogn. Affect. Neurosci. 2014, 9:48-54.
133. Rutherford H., Williams S., Moy S., Mayes L., Johns J. Disruption of maternal parenting circuitry by addictive process: rewiring of reward and stress systems. Front. Psychiatr. 2011, 2.
134. Sanders M.R., Kirby J.N., Tellegen C.L., Day J.J. The Triple P-Positive Parenting Program: a systematic review and meta-analysis of a multi-level system of parenting support. Clin. Psychol. Rev. 2014, 34:337-357.
135. Saxe R. Why and how to study Theory of Mind with fMRI. Brain Res. 2006, 1079:57-65.
136. Schechter D.S., Willheim E., Hinojosa C., Scholfield-Kleinman K., Turner J.B., McCaw J., Zeanah C.H., Myers M.M. Subjective and objective measures of parent-child relationship dysfunction, child separation distress, and joint attention. Psychiatry 2010, 73:130-144.
137. Schechter D.S., Moser D.A., Wang Z., Marsh R., Hao X., Duan Y., Yu S., Gunter B., Murphy D., McCaw J., Kangarlu A., Willheim E., Myers M.M., Hofer M.A., Peterson B.S. An fMRI study of the brain responses of traumatized mothers to viewing their toddlers during separation and play. Soc. Cogn. Affect. Neurosci. 2012, 7:969-979.
138. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
139. Seifritz E., Esposito F., Neuhoff J.G., Luthi A., Mustovic H., Dammann G., von Bardeleben U., Radue E.W., Cirillo S., Tedeschi G., Di Salle F. Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents. Biol. Psychiatry 2003, 54:1367-1375.
140. Sexton M.B., Flynn H.A., Lancaster C., Marcus S.M., McDonough S.C., Volling B.L., Lopez J.F., Kaciroti N., Vazquez D.M. Predictors of recovery from prenatal depressive symptoms from pregnancy through postpartum. J. Womens Health (Larchmt) 2011, 21:43-49.
141. Shah P.E., Fonagy P., Strathearn L. Is attachment transmitted across generations? The plot thickens. Clin. Child Psychol. Psychiatry 2010, 15:329-346.
142. Silverman M.E., Loudon H., Safier M., Protopopescu X., Leiter G., Liu X., Goldstein M. Neural dysfunction in postpartum depression: an fMRI pilot study. CNS Spectr. 2007, 12:853-862.
143. Sng J., Meaney M.J. Environmental regulation of the neural epigenome. Epigenomics 2009, 1:131-151.
144. Sohr-Preston S.L., Scaramella L.V. Implications of timing of maternal depressive symptoms for early cognitive and language development. Clin. Child. Fam. Psychol. Rev. 2006, 9:65-83.
145. Sripada C., Angstadt M., Kessler D., Phan K.L., Liberzon I., Evans G.W., Welsh R.C., Kim P., Swain J.E. Volitional regulation of emotions produces distributed alterations in connectivity between visual, attention control, and default networks. NeuroImage 2014, 89:110-121.
146. Stanley C., Murray L., Stein A. The effect of postnatal depression on mother-infant interaction, infant response to the Still-face perturbation, and performance on an instrumental learning task. Dev. Psychopathol. 2004, 16:1-18.
147. Stoeckel L.E., Weller R.E., Cook E.W., Twieg D.B., Knowlton R.C., Cox J.E. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage 2008, 41:636-647.
148. Stowe Z.N., Nemeroff C.B. Women at risk for postpartum-onset major depression. Am. J. Obstet. Gynecol. 1995, 173:639-645.
149. Stowe Z.N., Hostetter A.L., Newport D.J. The onset of postpartum depression: Implications for clinical screening in obstetrical and primary care. Am. J. Obstet. Gynecol. 2005, 192:522-526.
150. Strathearn L. Maternal neglect: oxytocin, dopamine and the neurobiology of attachment. J. Neuroendocrinol. 2011, 23:1054-1065.
151. Strathearn L., Kim S. Mothers' amygdala response to positive or negative infant affect is modulated by personal relevance. Front. Neurosci. 2013, 7:1-10.
152. Strathearn L., Mayes L.C. Cocaine addiction in mothers: potential effects on maternal care and infant development. Ann. N.Y. Acad. Sci. 2010, 1187:1-183.
153. Strathearn L., Li J., Fonagy P., Montague P.R. What's in a smile? Maternal brain responses to infant facial cues. Pediatrics 2008, 122:40-51.
154. Strathearn L., Fonagy P., Amico J., Montague P.R. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 2009, 34:2655-2666.
155. Strathearn L., Mamun A.A., Najman J.M., O'Callaghan M.J. Does breastfeeding protect against substantiated child abuse and neglect? A 15-year cohort study. Pediatrics 2009, 123:483-493.
156. Sturge-Apple M.L., Davies P.T., Cummings E.M. Impact of hostility and withdrawal in interparental conflict on parental emotional unavailability and children's adjustment difficulties. Child Dev. 2006, 77:1623-1641.
157. Swain J.E. Brain imaging of human parent-infant relationships. Arch. Womens Ment. Health 2011, 14:s93-s94.
158. Swain J.E., Lorberbaum J.P. Imaging the human parental brain. Neurobiol. Parent. Brain 2008, 83-100.
159. Swain J.E., Mayes L.C., Leckman J.F. The development of parent-infant attachment through dynamic and interactive signaling loops of care and cry. Behav. Brain Res. 2004, 27:472-473.
160. Swain J.E., Tasgin E., Mayes L.C., Feldman R., Constable R.T., Leckman J.F. Maternal brain response to own baby-cry is affected by cesarean section delivery. J. Child Psychol. Psychiatry 2008, 49:1042-1052.
161. Swain J.E., Konrath S., Brown S.L., Finegood E.D., Akce L.B., Dayton C.J., Ho S.S. Parenting and beyond: common neurocircuits underlying parental and altruistic caregiving. Parent Sci. Pract. 2012, 12:115-123.
162. Swain J.E., Ho S.S., Dayton C.J., Rosenblum K.L., Muzik M. Brain activity in empathy and approach-motivation domains for high-risk parents is increased by intervention and inversely related to parenting stress. Neuropsychopharmacology 2014, 39:S523-S524.
163. Swain J.E., Kim P., Spicer J., Ho S.S., Dayton C.J., Elmadih A., Abel K.M. Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain Res. 2014, 1580:78-101.
164. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Hoyt E., Kang H., Kim P., David D., Nguyen S., Constable R.T., Schultz R.T. Functional brain activations of parents listening to their own baby-cry change over the early postpartum. Dev. Psychobiol. 2015, (under review).
165. Tottenham N., Sheridan M.A. A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front. Hum. Neurosci. 2009, 3:68.
166. van Hasselt F.N., Cornelisse S., Yuan Zhang T., Meaney M.J., Velzing E.H., Krugers H.J., Joëls M. Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus 2012, 22:255-266.
167. Van Zeijl J., Mesman J., Van IJzendoorn M.H., Bakermans-Kranenburg M.J., Juffer F., Stolk M.N., Koot H.M., Alink L.R.A. Attachment-based intervention for enhancing sensitive discipline in mothers of 1-to 3-year-old children at risk for externalizing behavior problems: a randomized controlled trial. J. Consult. Clin. Psychol. 2006, 74:994-1005.
168. Vasterling J.J., Duke L.M., Brailey K., Constans J.I., Allain A.N., Sutker P.B. Attention, learning, and memory performances and intellectual resources in Vietnam veterans: PTSD and no disorder comparisons. Neuropsychology 2002, 16:5-14.
169. Vazquez D.M., McDonough S., Marcus S., Flynn H., Neal C.R., Volling B., Kaciroti N., Lopez J.F. Women at risk for depression: prenatal depressive symptoms and afternoon ACTH levels predict post-partum depression. Arch. Gen. Psychiatry 2015, (in submission).
170. Vink M., Kahn R.S., Raemaekers M., van den Heuvel M., Boersma M., Ramsey N.F. Function of striatum beyond inhibition and execution of motor responses. Hum. Brain Mapp. 2005, 25:336-344.
171. Viviani D., Charlet A., van den Burg E., Robinet C., Hurni N., Abatis M., Magara F., Stoop R. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 2011, 333:104-107.
172. Wan M.W., Downey D., Strachan H., Elliott R., Williams S.R., Abel K.M. The neural basis of maternal bonding. PLoS One 2014, 9. e88436.
173. Warner R., Appleby L., Whitton A., Faragher B. Demographic and obstetric risk factors for postnatal psychiatric morbidity. Br. J. Psychiatry 1996, 168:607-611.
174. Weaver I.C.G., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
175. Weisman O., Granat A., Gilboa-Schechtman E., Singer M., Gordon I., Azulay H., Kuint J., Feldman R. The experience of labor, maternal perception of the infant, and the mother's postpartum mood in a low-risk community cohort. Arch. Womens Ment. Health 2010, 13:505-513.
176. Weissman M.M., Feder A., Pilowsky D.J., Olfson M., Fuentes M., Blanco C., Lantigua R., Gameroff M.J., Shea S. Depressed mothers coming to primary care: maternal reports of problems with their children. J. Affect. Disord. 2004, 78:93-100.
177. Winnicott D.W. Primary maternal preoccupation. Through Paediatrics to Psycho-analysis 1956, Hogarth, London. D.W. Winnicott (Ed.).
178. Winslow J.T., Noble P.L., Lyons C.K., Sterk S.M., Insel T.R. Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology 2003, 28:910-918.
179. Wittchen H.U., Jacobi F., Rehm J., Gustavsson A., Svensson M., Jonsson B., Olesen J., Allgulander C., Alonso J., Faravelli C., Fratiglioni L., Jennum P., Lieb R., Maercker A., van Os J., Preisig M., Salvador-Carulla L., Simon R., Steinhausen H.C. The size and burden of mental disorders and other disorders of the brain in Europe 2010. Eur. Neuropsychopharmacol. 2011, 21:655-679.
180. Zaki J., Ochsner K.N. The neuroscience of empathy: progress, pitfalls and promise. Nat. Neurosci. 2012, 15:675-680.