A prospective longitudinal study of perceived infant outcomes at 18-24 months: Neural and psychological correlates of parental thoughts and actions assessed during the first month postpartum

Frontiers in Psychology

Volumn 6, Issue NOV, 2015, Pages

  Kim, Pilyoung ^a   Rigo, Paola ^b   Leckman, James F ^c   Mayes, Linda C ^c   Cole, Pamela M ^d   Feldman, Ruth ^e   Swain, James E ^c,f  

^a UNIVERSITY OF DENVER   (United States)

^b UNIVERSITY OF TRENTO   (Italy)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e BAR ILAN UNIVERSITY   (Israel)

^f UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Father; Infant; Mother; Neuroimaging; Parenting; Postpartum; Socioemotional development

Indexed keywords

EID: 84949684037     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2015.01772     Document Type: Article

References (75)

1. Abraham, E., Hendler, T., Shapira-Lichter, I., Kanat-Maymon, Y., Zagoory-Sharon, O., and Feldman, R. (2014). Father's brain is sensitive to childcare experiences. Proc. Natl. Acad. Sci. U.S.A. 111, 9792-9797. doi: 10.1073/pnas.1402569111.
2. Ainsworth, M. S. (1979). Infant-mother attachment. Am. Psychol. 34, 932-937. doi: 10.1037/0003-066X.34.10.932.
3. Atzil, S., Hendler, T., and Feldman, R. (2011). Specifying the neurobiological basis of human attachment: brain, hormones, and behavior in synchronous and intrusive mothers. Neuropsychopharmacology 36, 2603-2615. doi: 10.1038/npp.2011.172.
4. Atzil, S., Hendler, T., Zagoory-Sharon, O., Winetraub, Y., and Feldman, R. (2012). Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin. J. Am. Acad. Child Adolesc. Psychiatry 51, 798-811. doi: 10.1016/j.jaac.2012.06.008.
5. Barrett, J., and Fleming, A. S. (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. doi: 10.1111/j.1469-7610.2010.02306.x.
6. Barrett, J., Wonch, K. E., Gonzalez, A., Ali, N., Steiner, M., Hall, G. B., et al. (2012). Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Soc. Neurosci. 7, 252-268. doi: 10.1080/17470919.2011.609907.
7. Beck, A. T., Steer, R. A., and Garbin, M. G. (1988). Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clin. Psychol. Rev. 8, 77-100. doi: 10.1016/0272-7358(88)90050-5.
8. Bornstein, M. H. (2002). "Parenting infants," in Handbook of Parenting, ed. M. H. Bornstein (Mahwah, NJ: Erlbaum), 3-43.
9. Briggs-Gowan, M., and Carter, A. (2002). Brief Infant-Toddler Social and Emotional Assessment (BITSEA) Manual, Version 2.0. New Haven, CT: Yale University.
10. Briggs-Gowan, M. J., and Carter, A. S. (2006). BITSEA: Brief Infant-Toddler Social and Emotional Assessment. Examiner's Manual. San Antonio, TX: PsychCorp: Harcourt Assessment.
11. Briggs-Gowan, M. J., and Carter, A. S. (2008). Social-emotional screening status in early childhood predicts elementary school outcomes. Pediatrics 121, 957-962. doi: 10.1542/peds2007-1948.
12. Briggs-Gowan, M. J., Carter, A. S., Irwin, J. R., Wachtel, K., and Cicchetti, D. V. (2004). The brief infant-toddler social and emotional assessment: screening for social-emotional problems and delays in competence. J. Pediatr. Psychol. 29, 143-155. doi: 10.1093/jpepsy/jsh017.
13. Dedovic, K., Duchesne, A., Andrews, J., Engert, V., and Pruessner, J. C. (2009). The brain and the stress axis: the neural correlates of cortisol regulation in response to stress. Neuroimage 47, 864-871. doi: 10.1016/j.neuroimage.2009.05.074.
14. Essex, M. J., Klein, M. H., Cho, E., and Kalin, N. H. (2002). Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biol. Psychiatry 52, 776-784. doi: 10.1016/S0006-3223(02)01553-6.
15. Feldman, R. (2007a). Parent-infant synchrony and the construction of shared timing; Physiological precursors, developmental outcomes, and risk conditions. J. Child Psychol. Psychiatry 48, 329-354. doi: 10.1111/j.1469-7610.2006.01701.x.
16. Feldman, R. (2007b). Parent-infant synchrony: biological foundations and developmental outcomes. Curr. Dir. Psychol. Sci. 16, 340-345. doi: 10.1111/j.1467-8721.2007.00532.x.
17. Feldman, R. (2015). Sensitive periods in human social development: new insights from research on oxytocin, synchrony, and high-risk parenting. Dev. Psychopathol. 27, 369-395. doi: 10.1017/s0954579415000048.
18. Feldman, R., and Bamberger, E. (2011). Fathering matters: father-child relatedness from infancy to adolescence shapes children's social competence and dialogical skills. Paper Presented at the Biannial Meeting of the Society For Research in Child Development, Boston.
19. Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., and 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. doi: 10.1097/CHI.0b013e3181b21651.
20. Feldman, R., and Masalha, S. (2010). Parent-child and triadic antecedents of children's social competence: cultural specificity, shared process. Dev. Psychol. 46, 455-467. doi: 10.1037/a0017415.
21. Figee, M., Wielaard, I., Mazaheri, A., and Denys, D. (2013). Neurosurgical targets for compulsivity: what can we learn from acquired brain lesions? Neurosci. Biobehav. Rev. 37, 328-339. doi: 10.1016/j.neubiorev.2013.01.005.
22. Fleming, A. S., Kraemer, G. W., Gonzalez, A., Lovic, V., Rees, S., and Melo, A. (2002). Mothering begets mothering: the transmission of behavior and its neurobiology across generations. Pharmacol. Biochem. Behav. 73, 61-75. doi: 10.1016/S0091-3057(02)00793-1.
23. Gordon, I., Zagoory-Sharon, O., Leckman, J. F., and Feldman, R. (2010). Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood. Horm. Behav. 58, 513-518. doi: 10.1016/j.yhbeh.2010.04.007.
24. Grossmann, K., Grossmann, K. E., Fremmer-Bombik, E., Kindler, H., and Scheuerer-Englisch, H. (2002). The uniqueness of the child-father attachment relationship: fathers' sensitive and challenging play as a pivotal variable in a 16-year longitudinal study. Soc. Dev. 11, 301-337. doi: 10.1111/1467-9507.00202.
25. Grossmann, K., Grossmann, K. E., Kindler, H., and Zimmermann, P. (2008). "A wider view of attachment and exploration: the influence of mothers and fathers on the development of psychological security from infancy to young adulthood," in Handbook of Attachment: Theory, Research, and Clinical Applications, eds J. Cassidy and P. R. Shaver (New York, NY: Guilford Press), 857-879.
26. Haley, D. W., and Stansbury, K. (2003). Infant stress and parent responsiveness: regulation of physiology and behavior during still-face and reunion. Child Dev. 74, 1534-1546. doi: 10.1111/1467-8624.00621.
27. Hayes, A. F. (2013). Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach. New York, NY: The Guilford Press.
28. Ho, S. S., Konrath, S., Brown, S., and Swain, J. E. (2014). Empathy and stress related neural responses in maternal decision making. Front. Neurosci. 8:152. doi: 10.3389/fnins.2014.00152.
29. Hostinar, C. E., Sullivan, R. M., and Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development. Psychol. Bull. 140, 256-282. doi: 10.1037/a0032671.
30. Huyser, C., Veltman, D. J., De Haan, E., and Boer, F. (2009). Paediatric obsessive-compulsive disorder, a neurodevelopmental disorder? Evidence from neuroimaging. Neurosci. Biobehav. Rev. 33, 818-830. doi: 10.1016/j.neubiorev.2009.01.003.
31. Karabekiroglu, K., Briggs-Gowan, M. J., Carter, A. S., Rodopman-Arman, A., and Akbas, S. (2010). The clinical validity and reliability of the Brief Infant-Toddler Social and Emotional Assessment (BITSEA). Infant Behav. Dev. 33, 503-509. doi: 10.1016/j.infbeh.2010.07.001.
32. Kim, P., Feldman, R., Mayes, L. C., Eicher, V., Thompson, N., Leckman, J. F., et al. (2011). Breastfeeding, brain activation to own infant cry, and maternal sensitivity. J. Child Psychol. Psychiatry 52, 907-915. doi: 10.1111/j.1469-7610.2011.02406.x.
33. Kim, P., Leckman, J. F., Mayes, L. C., Feldman, R., Wang, X., and Swain, J. E. (2010a). The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period. Behav. Neurosci. 124, 695-700. doi: 10.1037/a0020884.
34. Kim, P., Leckman, J. F., Mayes, L. C., Newman, M.-A., Feldman, R., and Swain, J. E. (2010b). Perceived quality of maternal care in childhood and structure and function of mothers' brain. Dev. Sci. 13, 662-673. doi: 10.1111/j.1467-7687.2009.00923.x.
35. Kim, P., Mayes, L., Feldman, R., Leckman, J. F., and Swain, J. E. (2013). Early postpartum parental preoccupation and positive parenting thoughts: relationship with parentinfant interaction. Infant Ment. Health J. 34, 104-116. doi: 10.1002/Imhj.21359.
36. Kim, P., Rigo, P., Mayes, L. C., Feldman, R., Leckman, J. F., and Swain, J. E. (2014). Neural plasticity in fathers of human infants. Soc. Neurosci. 9, 522-535. doi: 10.1080/17470919.2014.933713.
37. Kim, P., Strathearn, L., and Swain, J. E. (2015). The maternal brain and its plasticity in humans. Horm. Behav. doi: 10.1016/j.yhbeh.2015.08.001 [Epub ahead of print].
38. Kuo, P. X., Carp, J., Light, K. C., and Grewen, K. M. (2012). Neural responses to infants linked with behavioral interactions and testosterone in fathers. Biol. Psychol. 91, 302-306. doi: 10.1016/j.biopsycho.2012.08.002.
39. Lamb, M. E., and Lewis, C. (2013). "Father-child relationships," in Handbook of Father Involvement, 2nd Edn, eds N. Cabrera and C. TamisLeMonda (New York, NY: Routledge), 119-134.
40. Landers, M. S., and Sullivan, R. M. (2012). The development and neurobiology of infant attachment and fear. Dev. Neurosci. 34, 101-114. doi: 10.1159/000336732.
41. Landi, N., Montoya, J., Kober, H., Rutherford, H. J., Mencl, W. E., Worhunsky, P. D., et al. (2011). Maternal neural responses to infant cries and faces: relationships with substance use. Front. Psychiatry 2:32. doi: 10.3389/fpsyt.2011.00032.
42. Laurent, H. K., and Ablow, J. C. (2011). A cry in the dark: depressed mothers show reduced neural activation to their own infant's cry. Soc. Cogn. Affect. Neurosci. 7, 125-134. doi: 10.1093/scan/nsq091.
43. Leckman, J. F., Feldman, R., Swain, J. E., Eicher, V., Thompson, N., and Mayes, L. C. (2004). Primary parental preoccupation: circuits, genes, and the crucial role of the environment. J. Neural. Transm. 111, 753-771. doi: 10.1007/s00702-003-0067-x.
44. Leckman, J. F., Mayes, L. C., Feldman, R., Evans, D. W., King, R. A., and Cohen, D. J. (1999). Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive-compulsive disorder. Acta Psychiatr. Scand. Suppl. 396, 1-26. doi: 10.1111/j.1600-0447.1999.tb10951.x.
45. Lieberman, M. D., and Cunningham, W. A. (2009). Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc. Cogn. Affect. Neurosci. 4, 423-428. doi: 10.1093/scan/nsp052.
46. Lorberbaum, J. P., Newman, J. D., Horwitz, A. R., Dubno, J. R., Lydiard, R. B., Hamner, M. B., et al. (2002). A potential role for thalamocingulate circuitry in human maternal behavior. Biolol. Psychiatry 51, 431-445. doi: 10.1016/S0006-3223(01)01284-7.
47. Lupien, S. J., Mcewen, B. S., Gunnar, M. R., and Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 10, 434-445. doi: 10.1038/nrn2639.
48. Mascaro, J. S., Hackett, P. D., Gouzoules, H., Lori, A., and Rilling, J. K. (2014). Behavioral and genetic correlates of the neural response to infant crying among human fathers. Soc. Cogn. Affect. Neurosci. 9, 1704-1712. doi: 10.1093/scan/nst166.
49. Mascaro, J. S., Hackett, P. D., and Rilling, J. K. (2013). Testicular volume is inversely correlated with nurturing-related brain activity in human fathers. Proc. Natl. Acad. Sci. U.S.A. 110, 15746-15751. doi: 10.1073/pnas.1305579110.
50. Meaney, M. J. (2010). Epigenetics and the biological definition of gene x environment interactions. Child Dev. 81, 41-79. doi: 10.1111/j.1467-8624.2009.01381.x.
51. Montoya, J. L., Landi, N., Kober, H., Worhunsky, P. D., Rutherford, H. J. V., Mencl, W. E., et al. (2012). Regional brain responses in nulliparous women to emotional infant stimuli. PLoS ONE 7:e36270. doi: 10.1371/journal.pone.0036270.
52. Moses-Kolko, E. L., Horner, M. S., Phillips, M. L., Hipwell, A. E., and Swain, J. E. (2014). In search of neural endophenotypes of postpartum psychopathology and disrupted maternal caregiving. J. Neuroendocrinol. 26, 665-684. doi: 10.1111/jne.12183.
53. Musser, E. D., Kaiser-Laurent, H., and Ablow, J. C. (2012). The neural correlates of maternal sensitivity: an fMRI study. Dev. Cogn. Neurosci. 2, 428-436. doi: 10.1016/j.dcn.2012.04.003.
54. Nitschke, J. B., Nelson, E. E., Rusch, B. D., Fox, A. S., Oakes, T. R., and Davidson, R. J. (2004). Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. Neuroimage 21, 583-592. doi: 10.1016/j.neuroimage.2003.10.005.
55. Noriuchi, M., Kikuchi, Y., and Senoo, A. (2008). The functional neuroanatomy of maternal love: mother's response to infant's attachment behaviors. Biol. Psychiatry 63, 415-423. doi: 10.1016/j.biopsych.2007.05.018.
56. Numan, M., and Insel, T. R. (2003). The Neurobiology of Parental Behavior. New York, NY: Springer.
57. Panter-Brick, C., Burgess, A., Eggerman, M., Mcallister, F., Pruett, K., and Leckman, J. F. (2014). Engaging fathers: recommendations for a game change in parenting interventions; based on a systematic review of the global evidence. J. Child Psychol. Psychiatry 55, 1187-1212. doi: 10.1111/jcpp.12280.
58. Pereira, M., and Ferreira, A. (2015). Neuroanatomical and neurochemical basis of parenting: dynamic coordination of motivational, affective and cognitive processes. Horm. Behav. doi: 10.1016/j.yhbeh.2015.08.005 [Epub ahead of print].
59. Porter, C. L., and Hsu, H.-C. (2003). First-time mothers' perceptions of efficacy during the transition to motherhood: links to infant temperament. J. Fam. Psychol. 17, 54-64. doi: 10.1037/0893-3200.17.1.54.
60. Preacher, K. J., and Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav. Res. Methods 40, 879-891. doi: 10.3758/BRM.40.3.879.
61. Ramchandani, P. G., Domoney, J., Sethna, V., Psychogiou, L., Vlachos, H., and Murray, L. (2013). Do early father-infant interactions predict the onset of externalising behaviours in young children? Findings from a longitudinal cohort study. J. Child Psychol. Psychiatry 54, 56-64. doi: 10.1111/j.1469-7610.2012.02583.x.
62. Riem, M. M., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A., Vermeiren, R. R., et al. (2011). Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol. Psychiatry 70, 291-297. doi: 10.1016/j.biopsych.2011.02.006.
63. Rilling, J. K., and Young, L. J. (2014). The biology of mammalian parenting and its effect on offspring social development. Science 345, 771-776. doi: 10.1126/science.1252723.
64. Schechter, D. S., Moser, D. A., Wang, Z. S., Marsh, R., Hao, X. J., Duan, Y. S., et al. (2012). An fMRI study of the brain responses of traumatized mothers to viewing their toddlers during separation and play. Soc. Cogn. Affect. Neurosci. 7, 969-979. doi: 10.1093/scan/nsr069.
65. Spielberger, C. D., and Vagg, P. R. (1984). Psychometric properties of the STAI: a reply to Ramanaiah, Franzen, and Schill. J. Pers. Assess. 48, 95-97. doi: 10.1207/s15327752jpa4801_16.
66. Storey, A. E., and Walsh, C. J. (2013). "Biological basis of mammalian paternal behavior," in Handbook of Father Involvement: Multidisciplinary Perspectives, Vol. 2, eds N. J. Cabrera and C. S. Tamis-LeMonda (London: Routledge), 3-22.
67. Strathearn, L., Li, J., Fonagy, P., and Montague, P. R. (2008). What's in a smile? Maternal brain responses to infant facial cues. Pediatrics 122, 40-51. doi: 10.1542/peds2007-1566.
68. Swain, J. E., Dayton, C. J., Kim, P., Tolman, R. M., and Volling, B. L. (2014a). Progress on the paternal brain: theory, animal models, human brain research, and mental health implications. Infant Ment. Health J. 35, 394-408. doi: 10.1002/imhj.21471.
69. Swain, J. E., Kim, P., Spicer, J., Ho, S. S., Dayton, C. J., Elmadih, A., et al. (2014b). Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain Res. 1508, 78-101. doi: 10.1016/j.brainres.2014.03.007.
70. Swain, J. E., Konrath, S., Brown, S. L., Finegood, E. D., Akce, L. B., Dayton, C. J., et al. (2012). Parenting and beyond: common neurocircuits underlying parental and altruistic caregiving. Parent. Sci. Pract. 12, 115-123. doi: 10.1080/15295192.2012.680409.
71. Swain, J. E., and Lorberbaum, J. P. (2008). "Imaging the human parental brain," in Neurobiology of the Parental Brain, ed. R. Bridges (Waltham, MA: Acadamic Press), 83-100.
72. Swain, J. E., Mayes, L. C., and Leckman, J. F. (2004). The development of parent-infant attachment through dynamic and interactive signaling loops of care and cry. Behav. Brain Sci. 27, 472-473. doi: 10.1017/S0140525X0437010X.
73. Volling, B. L., Mcelwain, N. L., Notaro, P. C., and Herrera, C. (2002). Parents' emotional availability and infant emotional competence: predictors of parent-infant attachment and emerging self-regulation. J. Fam. Psychol. 16, 447-465. doi: 10.1037/0893-3200.16.4.447.
74. Wan, M. W., Downey, D., Strachan, H., Elliott, R., Williams, S. R., and Abel, K. M. (2014). The neural basis of maternal bonding. PLoS ONE 9:e88436. doi: 10.1371/journal.pone.0088436.
75. Winnicott, D. W. (1956). "Primary maternal preoccupation," in Through Paediatrics to Psycho-Analysis, ed. D. W. Winnicott (London: Hogarth).