The human parental brain: In vivo neuroimaging

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 35, Issue 5, 2011, Pages 1242-1254

  Swain, James E ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Attachment; Brain imaging; FMRI; Parent child relationships; Parenting and caregiving

Indexed keywords

AFFECT; ARTICLE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CHILD BEHAVIOR; CHILD CARE; CHILD PARENT RELATION; CINGULATE GYRUS; COGNITION; EMOTIONAL ATTACHMENT; EMOTIONALITY; EMPATHY; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPOTHALAMUS; IN VIVO STUDY; LIMBIC CORTEX; LIMBIC SYSTEM; MENTAL HEALTH; MENTAL PERFORMANCE; MENTAL TASK; MESENCEPHALON; MOTIVATION; NEUROANATOMY; NEUROIMAGING; NEUROPHYSIOLOGY; NEUROPSYCHOLOGY; NONHUMAN; PARENTAL BEHAVIOR; SENSORY STIMULATION; SOCIAL BEHAVIOR; TRUST; VISUAL STIMULATION;

BRAIN; FEMALE; HUMANS; INFANT; INFANT BEHAVIOR; MAGNETIC RESONANCE IMAGING; MALE; NEUROIMAGING; PARENTS; PHOTIC STIMULATION;

EID: 79957860568     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2010.10.017     Document Type: Article

References (112)

1. Aron A., Fisher H., Mashek D.J., Strong G., Li H., Brown L.L. Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol 2005, 94:327-337.
2. Baron-Cohen S., Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J AutismDevDisord 2004, 34:163-175.
3. Barrett J., Hall G., Wonch K., Ali N., Gonzalez A., Steiner M., et al. Quality of early parental care reported by mothers is related to anterior cingulate response to own infant stimuli: preliminary findings. Neuroimage 2009, 47:S181-S.
4. Bartels A., Zeki S. The neural basis of romantic love. NeuroReport 2000, 11:3829-3834.
5. Bartels A., Zeki S. Functional brain mapping during free viewing of natural scenes. Hum Brain Mapp 2004, 21:75-85.
6. Bartels A., Zeki S. The neural correlates of maternal and romantic love. Neuroimage 2004, 21:1155-1166.
7. Bartels A., Zeki S. Brain dynamics during natural viewing conditions-a new guide for mapping connectivity in vivo. Neuroimage 2005, 24:339-349.
8. Baxter L.R. Basal ganglia systems in ritualistic social displays: reptiles and humans; function and illness. Physiol Behav 2003, 79:451-460.
9. Bodini B., Iacoboni M., Lenzi G.L. Acute stroke effects on emotions: an interpretation through the mirror system. Curr Opin Neurol 2004, 17:55-60.
10. Britton J.C., Phan K.L., Taylor S.F., Welsh R.C., Berridge K.C., Liberzon I. Neural correlates of social and nonsocial emotions: an fMRI study. Neuroimage 2006.
11. Brown G.W., Bifulco A., Harris T.O. Life events, vulnerability and onset of depression: some refinements. Br J Psychiatry 1987, 150:30-42.
12. Buchheim A., Erk S., George C., Kachele H., Kircher T., Martius P., et al. Neural correlates of attachment trauma in borderline personality disorder: a functional magnetic resonance imaging study. Psychiatry Res 2008, 163:223-235.
13. Buchheim A., Erk S., George C., Kachele H., Ruchsow M., Spitzer M., et al. Measuring attachment representation in an fMRI environment: a pilot study. Psychopathology 2006, 39:144-152.
14. Caplan H.L., Cogill S.R., Alexandra H., Robson K.M., Katz R., Kumar R. Maternal depression and the emotional development of the child. Br J Psychiatry 1989, 154:818-822.
15. Carr L., Iacoboni M., Dubeau M.C., Mazziotta J.C., Lenzi G.L. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci USA 2003, 100:5497-5502.
16. Cassidy J., Ziv Y., Stupica B., Sherman L.J., Butler H., Karfgin A., et al. Enhancing attachment security in the infants of women in a jail-diversion program. Attach HumDev 2010, 12:333-353.
17. Champagne F.A. Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 2010, 52:299-311.
18. Critchley H.D. Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int J Psychophysiol 2009, 73:88-94.
19. Crowley M.J., Wu J., Molfese P.J., Mayes L.C. Social exclusion in middle childhood: Rejection events, slow-wave neural activity, and ostracism distress. Soc Neurosci 2010, 12:1-13.
20. Dapretto M., Davies M.S., Pfeifer J.H., Scott A.A., Sigman M., Bookheimer S.Y., et al. Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 2006, 9:28-30.
21. Decety J., Grezes J. The power of simulation: imagining one's own and other's behavior. Brain Res 2006, 1079:4-14.
22. Draganski B., Gaser C., Busch V., Schuierer G., Bogdahn U., May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004, 427:311-312.
23. Draganski B., Gaser C., Kempermann G., Kuhn H.G., Winkler J., Buchel C., et al. Temporal and spatial dynamics of brain structure changes during extensive learning. J Neurosci 2006, 26:6314-6317.
24. Drevets W.C., Savitz J., Trimble M. The subgenual anterior cingulate cortex in mood disorders. CNS Spectr 2008, 13:663-681.
25. Eisenberger N.I., Lieberman M.D., Williams K.D. Does rejection hurt? An FMRI study of social exclusion. Science 2003, 302:290-292.
26. Feldman R., Gordon I., Schneiderman I., Weisman O., Zagoory-Sharon O. Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 2010, 35:1133-1141.
27. Feldman R., Gordon I., Zagoory-Sharon O. The cross-generation transmission of oxytocin in humans. Horm Behav. 2010, 58:669-676.
28. 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.
29. Fisher H., Aron A., Brown L.L. Romantic love: an fMRI study of a neural mechanism for mate choice. J Comp Neurol 2005, 493:58-62.
30. Fisher H., Aron A., Mashek D., Li H., Strong G., Brown L.L. The neural mechanisms of mate choice: a hypothesis. Neuro Endocrinol Lett 2002, 23(Suppl 4):92-97.
31. Fisher H.E., Aron A., Mashek D., Li H., Brown L.L. Defining the brain systems of lust, romantic attraction, and attachment. Arch Sex Behav 2002, 31:413-419.
32. Fleming A.S., Corter C., Stallings J., Steiner M. Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Horm Behav 2002, 42:399-413.
33. Frith U., Frith C.D. Development and neurophysiology of mentalizing. Philos Trans R Soc Lond B Biol Sci 2003, 358:459-473.
34. Frodi A.M., Lamb M.E. Child abusers' responses to infant smiles and cries. ChildDev 1980, 51:238-241.
35. Gallese V., Keysers C., Rizzolatti G. Aunifying view of the basis of social cognition. Trends Cogn Sci 2004, 8:396-403.
36. Glocker M.L., Langleben D.D., Ruparel K., Loughead J.W., Valdez J.N., Griffin M.D., et al. Baby schema modulates the brain reward system in nulliparous women. Proc Natl Acad Sci USA 2009, 106:9115-9119.
37. Gray J.R. Emotional modulation of cognitive control: approach-withdrawal states double-dissociate spatial from verbal two-back task performance. J Exp Psychol Gen 2001, 130:436-452.
38. Gutman D.A., Holtzheimer P.E., Behrens T.E., Johansen-Berg H., Mayberg H.S. A tractography analysis of two deep brain stimulation white matter targets for depression. Biol Psychiatry 2009, 65:276-282.
39. Hasson U., Nir Y., Levy I., Fuhrmann G., Malach R. Intersubject synchronization of cortical activity during natural vision. Science 2004, 303:1634-1640.
40. Heim C., Owens M.J., Plotsky P.M., Nemeroff C.B. The role of early adverse life events in the etiology of depression and posttraumatic stress disorder. Focus on corticotropin releasing factor. Ann NY Acad Sci 1997, 821:194-207.
41. 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.
42. Iacoboni M. Neurobiology of imitation. Curr Opin Neurobiol 2009, 19:661-665.
43. Johansen-Berg H., Gutman D.A., Behrens T.E., Matthews P.M., Rushworth M.F., Katz E., et al. Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cereb Cortex 2008, 18:1374-1383.
44. Kaffman A., Meaney M.J. Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. J Child Psychol Psychiatry 2007, 48:224-244.
45. Kendler K.S., Kessler R.C., Neale M.C., Heath A.C., Eaves L.J. The prediction of major depression in women: toward an integrated etiologic model. Am J Psychiatry 1993, 150:1139-1148.
46. Keverne E.B., Curley J.P. Vasopressin, oxytocin and social behaviour. Curr Opin Neurobiol 2004, 14:777-783.
47. Kim-Cohen J., Moffitt T.E., Taylor A., Pawlby S.J., Caspi A. Maternal depression and children's antisocial behavior: nature and nurture effects. Arch Gen Psychiatry 2005, 62:173-181.
48. Kim P., Feldman R., Leckman J.F., Mayes L.C., Swain J.E. Breastfeeding, brain activation to own infant cry, and maternal sensitivity. J Child Psychol Psychiatry 2010, in submission.
49. Kim P., Leckman J.F., Mayes L.C., Feldman R., Xin W., Swain J.E. The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period. Behavioral Neuroscience 2010, 124(5):695-700.
50. 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.
51. Kringelbach M.L., Lehtonen A., Squire S., Harvey A.G., Craske M.G., Holliday I.E., et al. A specific and rapid neural signature for parental instinct. PLoS ONE 2008, 3:e1664.
52. 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.
53. Leckman J.F., Mayes L.C., Feldman R., Evans D.W., King R.A., Cohen D.J. Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive-compulsive disorder. Acta Psychiatr Scand Suppl 1999, 396:1-26.
54. LeDoux J. The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 2003, 23:727-738.
55. Lee H.J., Macbeth A.H., Pagani J.H., Young W.S. Oxytocin: the great facilitator of life. Prog Neurobiol 2009, 88:127-151.
56. 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.
57. Lenzi D., Trentini C., Pantano P., Macaluso E., Iacoboni M., Lenzi G.L., et al. Neural basis of maternal communication and emotional expression processing during infant preverbal stage. Cereb Cortex 2008, 19:1124-1133.
58. Lorberbaum J.P., Newman J.D., Dubno J.R., Horwitz A.R., Nahas Z., Teneback C.C., et al. Feasibility ofusing fMRI to study mothers responding to infant cries. Depress Anxiety 1999, 10:99-104.
59. Lorberbaum J.P., Newman J.D., Horwitz A.R., Dubno J.R., Lydiard R.B., Hamner M.B., et al. A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 2002, 51:431-445.
60. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009, 10:434-445.
61. MacLean P.D. The triune brain in evolution: role in paleocerebral functions 1990, Plenum Press, New York.
62. Masten C.L., Eisenberger N.I., Borofsky L.A., Pfeifer J.H., McNealy K., Mazziotta J.C., et al. Neural correlates of social exclusion during adolescence:understanding the distress of peer rejection. Soc Cogn Affect Neurosci 2009, 4:143-157.
63. Mayberg H.S., Lozano A.M., Voon V., McNeely H.E., Seminowicz D., Hamani C., et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005, 45:651-660.
64. Mayes L.C., Swain J.E., Leckman J.F. Parental attachment systems: neural circuits, genes, and experiential contributions to parental engagement. Clin Neurosci Res 2005, 4:301-313.
65. McEwen B.S. Understanding the potency of stressful early life experiences on brain and body function. Metabolism 2008, 57(Suppl2):S11-S15.
66. Morris J.P., Pelphrey K.A., McCarthy G. Regional brain activation evoked when approaching a virtual human on a virtual walk. J Cogn Neurosci 2005, 17:1744-1752.
67. Murray L., Cooper P.J. The impact of postpartum depression on child development. Aetiological mechanisms in developmental psychopathology 2003, Oxford University Press, Oxford. I. Goodyer (Ed.).
68. Najib A., Lorberbaum J.P., Kose S., Bohning D.E., George M.S. Regional brain activity in women grieving a romantic relationship breakup. Am J Psychiatry 2004, 161:2245-2256.
69. Nitschke J.B., Nelson E.E., Rusch B.D., Fox A.S., Oakes T.R., Davidson R.J. Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. Neuroimage 2004, 21:583-592.
70. 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.
71. Numan M., Insel T.R. The neurobiology of parental behavior 2003, Springer-Verlag, New York.
72. Olausson H., Lamarre Y., Backlund H., Morin C., Wallin B.G., Starck G., et al. Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 2002, 5:900-904.
73. Olds D.L., Kitzman H., Cole R., Robinson J., Sidora K., Luckey D.W., et al. Effects of nurse home-visiting on maternal life course and child development: age 6 follow-up results of a randomized trial. Pediatrics 2004, 114:1550-1559.
74. Olds D.L., Sadler L., Kitzman H. Programs for parents of infants and toddlers: recent evidence from randomized trials. J Child Psychol Psychiatry 2007, 48:355-391.
75. Panksepp J. Emotional endophenotypes in evolutionary psychiatry. Prog Neuropsychopharmacol Biol Psychiatry 2006, 30:774-784.
76. Pelphrey K.A., Morris J.P., McCarthy G. Grasping the intentions of others: the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. J Cogn Neurosci 2004, 16:1706-1716.
77. Pelphrey K.A., Morris J.P., Michelich C.R., Allison T., McCarthy G. Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. Cereb Cortex 2005, 15:1866-1876.
78. Perlman S.B., Pelphrey K.A. Regulatory brain development: balancing emotion and cognition. Soc Neurosci 2010, 5:533-542.
79. Purhonen M., Kilpelainen-Lees R., Paakkonen A., Ypparila H., Lehtonen J., Karhu J. Effects of maternity on auditory event-related potentials to human sound. NeuroReport 2001, 12:2975-2979.
80. Purhonen M., Paakkonen A., Ypparila H., Lehtonen J., Karhu J. Dynamic behavior of the auditory N100 elicited by a baby's cry. Int J Psychophysiol 2001, 41:271-278.
81. Ranote S., Elliott R., Abel K.M., Mitchell R., Deakin J.F., Appleby L. The neural basis of maternal responsiveness to infants: an fMRI study. NeuroReport 2004, 15:1825-1829.
82. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 2009, 30:534-547.
83. Sander D., Grandjean D., Pourtois G., Schwartz S., Seghier M.L., Scherer K.R., et al. Emotion and attention interactions in social cognition: brain regions involved in processing anger prosody. Neuroimage 2005, 28:848-858.
84. Sander K., Brechmann A., Scheich H. Audition of laughing and crying leads to right amygdala activation in a low-noise fMRI setting. Brain Res Brain Res Protoc 2003, 11:81-91.
85. Sander K., Frome Y., Scheich H. FMRI activations of amygdala, cingulate cortex, and auditory cortex by infant laughing and crying. Hum Brain Mapp. 2007.
86. Saxe R. Uniquely human social cognition. Curr Opin Neurobiol 2006, 16:235-239.
87. Saxe R. Why and how to study theory of mind with fMRI. Brain Res 2006, 1079:57-65.
88. Schultz R.T. Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int JDev Neurosci 2005, 23:125-141.
89. Seifritz E., Esposito F., Neuhoff J.G., Luthi A., Mustovic H., Dammann G., et al. Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents. Biol Psychiatry 2003, 54:1367-1375.
90. Singer T., Seymour B., O'Doherty J., Kaube H., Dolan R.J., Frith C.D. Empathy for pain involves the affective but not sensory components of pain. Science 2004, 303:1157-1162.
91. Soltis J. The signal functions of early infant crying. Behav Brain Sci 2004, 27:459-490. 443-58; discussion.
92. Squire S., Stein A. Functional MRI and parental responsiveness: a new avenue into parental psychopathology and early parent-child interactions?. Br J Psychiatry 2003, 183:481-483.
93. Sroufe L.A., Carlson E.A., Levy A.K., Egeland B. Implications of attachment theory for developmental psychopathology. Dev Psychopathol 1999, 11:1-13.
94. Stowe Z.N., Nemeroff C.B. Women at risk for postpartum-onset major depression. Am J Obstet Gynecol 1995, 173:639-645.
95. 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.
96. 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.
97. Strathearn L., Li J., Montague P.R. An fMRI study of maternal mentalization: having the baby's mind in mind. Neuroimage 2005, 26:S25.
98. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Constable R.T., Schultz R.T. The neural circuitry of parent-infant attachment in the early postpartum 2003, American College of Neuropsychopharmacology, Puerto Rico.
99. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Constable R.T., Schultz R.T. Brain circuitry and psychology of human parent-infant attachment in the postpartum. International Academy of Child and Adolescent Psychiatry and Allied Professions,16th World Congress 2004, 365.
100. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Constable R.T., Schultz R.T. Neural substrates and psychology of human parent-infant attachment in the postpartum. Biol Psychiatry 2004, 55:153S.
101. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Schultz R.T. Early human parent-infant bond development: fMRI, thoughts and behaviors. Biol Psychiatry 2005, 57:112S.
102. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Schultz R.T. Own baby pictures induce parental brain activations according to psychology, experience and postpartum timing. Biol Psychiatry 2006, 59:126S.
103. Swain JE, Leckman JF, Mayes LCRF, Constable RT, Schultz RT. First-time mothers and fathers show differential activation of the right orbital frontal and insular cortices in response to listening to their own infant's cries. Biological Psychiatry. submitted for publication.
104. Swain JE, Leckman JF, Mayes LCRF, Hoyt E, Kang K, Kim P, David D, Nguyen S, Constable R T, Schultz RT. Functional brain activations of parents listening to their own baby-cry change over the early postpartum. Developmental Psychobiology. In press.
105. Swain J.E., Lorberbaum J.P., Kose S., Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry 2007, 48:262-287.
106. 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 Sci 2004, 27:472-473.
107. 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.
108. Tzourio N., Massioui F.E., Crivello F., Joliot M., Renault B., Mazoyer B. Functional anatomy of human auditory attention studied with PET. Neuroimage 1997, 5:63-77.
109. Uddin L.Q., Iacoboni M., Lange C., Keenan J.P. The self and social cognition: the role of cortical midline structures and mirror neurons. Trends Cogn Sci 2007, 11:153-157.
110. Veenema A.H. Early life stress development aggression neuroendocrine neurobiological correlates what can we learn animal models?. Front Neuroendocrinol 2009, 30:497-518.
111. Weissman M.M., Pilowsky D.J., Wickramaratne P.J., Talati A., Wisniewski S.R., Fava M., et al. Remissions in maternal depression and child psychopathology: a STAR*D-child report. Jama 2006, 295:1389-1398.
112. Werner E.E. Journeys from childhood to midlife: risk, resilience, and recovery. Pediatrics 2004, 114:492.