Early life stress is associated with default system integrity and emotionality during infancy

Journal of Child Psychology and Psychiatry and Allied Disciplines

Volumn 56, Issue 11, 2015, Pages 1212-1222

  Graham, Alice M ^a   Pfeifer, Jennifer H ^b   Fisher, Philip A ^b,c   Carpenter, Samuel ^a   Fair, Damien A ^a,d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF OREGON   (United States)

^c OREGON SOCIAL LEARNING CENTER   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

brain development; family functioning; Functional MRI; infancy; stress

Indexed keywords

ADULT; AMYGDALA; CINGULATE GYRUS; EMOTION; FAMILY CONFLICT; FEMALE; HUMAN; INFANT; MALE; MENTAL STRESS; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY;

ADULT; AMYGDALA; EMOTIONS; FAMILY CONFLICT; FEMALE; GYRUS CINGULI; HUMANS; INFANT; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PREFRONTAL CORTEX; STRESS, PSYCHOLOGICAL;

EID: 84944057416     PISSN: 00219630     EISSN: 14697610     Source Type: Journal    
DOI: 10.1111/jcpp.12409     Document Type: Article

References (83)

1. Andrews-Hanna, J.R., Reidler, J.S., Sepulcre, J., Poulin, R., &, Buckner, R.L., (2010). Functional-anatomic fractionation of the brain's default network. Neuron, 65, 550-562.
2. Beckmann, C.F., Jenkinson, M., Woolrich, M.W., Behrens, T.E.J., David, E., Devlin, J.T., &, Smith, S.M., (2006). Applying FSL to the FIAC Data: Model-based and model-free analysis of voice and sentence repetition priming. Human Brain Mapping, 27, 380-391.
3. Berman, M.G., Peltier, S., Nee, D.E., Kross, E., Deldin, P.J., &, Jonides, J., (2011). Depression, rumination and the default network. Social Cognitive and Affective Neuroscience, 6, 548-555.
4. Blasi, A., Mercure, E., Lloyd-Fox, S., Thomson, A., Brammer, M., Sauter, D.,... &, Murphy, D.G.M., (2011). Early specialization for voice and emotion processing in the infant brain. Current Biology, 21, 1-5.
5. Bluhm, R.L., Williamson, P.C., Osuch, E.A., Frewen, P.A., Stevens, T.K., Boksman, K.,... &, Lanius, R.A,. (2009). Alterations in default network connectivity in posttraumatic stress disorder related to early-life trauma. Journal of Psychiatry & Neuroscience, 34, 187-194.
6. Callaghan, B.L., &, Richardson, R., (2011). Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats. Behavioral Neuroscience, 125, 20-28.
7. Callaghan, B.L., &, Richardson, R., (2013). Early experiences and the development of emotional learning systems in rats. Biology of Mood & Anxiety Disorders, 3, 8.
8. Callaghan, B.L., Sullivan, R.M., Howell, B., &, Tottenham, N., (2014). The international society for developmental psychobiology sackler symposium: Early adversity and the maturation of emotion circuits-A cross-species analysis. Developmental Psychobiology, 56, 1635-1650.
9. Cox, M.J., &, Paley, B., (2003). Understanding families as systems. Current Directions in Psychological Science, 12, 193-196.
10. Cummings, E.M., &, Davies, P.T., (2002). Effects of marital conflict on children: Recent advances and emerging themes in process-oriented research. Journal of Child Psychology and Psychiatry, 43, 31-63.
11. Cummings, E.M., &, Davies, P.T., (2010). Marital Conflict and Children: An Emotional Security Perspective (p. 320). New York: The Guilford Press.
12. Daniels, J.K., Frewen, P., McKinnon, M.C., &, Lanius, R.A., (2011). Default mode alterations in posttraumatic stress disorder related to early-life trauma: A developmental perspective. Journal of Psychiatry & Neuroscience, 36, 56-59.
13. El-Sheikh, M., Cummings, E.M., Kouros, C.D., Elmore-Staton, L., &, Buckhalt, J.A., (2008). Marital psychological and physical aggression and children's mental and physical health: Direct, mediated, and moderated effects. Journal of Consulting and Clinical Psychology, 76, 138-148.
14. Fair, D.A., Cohen, A.L., Power, J.D., Dosenbach, N.U.F., Church, J.A., Miezin, F.M.,... &, Petersen, S. E., (2009). Functional brain networks develop from a "local to distributed" organization. PLoS Computational Biology, 5, e1000381.
15. Fair, D.A., Nigg, J.T., Iyer, S., Bathula, D., Mills, K.L., Dosenbach, N.U.F.,... &, Milham, M. P., (2012). Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Frontiers in Systems Neuroscience, 6, 80.
16. Fair, D.A., Posner, J., Nagel, B.J., Bathula, D., Dias, T.G.C., Mills, K.L.,... &, Nigg, J.T., (2010). Atypical default network connectivity in youth with attention-deficit/hyperactivity disorder. Biological Psychiatry, 68, 1084-1091.
17. Fonov, V.S., Evans, A.C., Botteron, K., Almli, C.R., McKinstry, R.C., &, Collins, D.L., (2011). Unbiased average age-appropriate atlases for pediatric studies. NeuroImage, 54, 313-327.
18. Fonov, V.S., Evans, A.C., Mckinstry, R.C., Almli, C.R., &, Collins, D.L., (2009). Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. NeuroImage, 47 (Supplement 1), S102.
19. Fonzo, G.A., Simmons, A.N., Thorp, S.R., Norman, S.B., Paulus, M.P., &, Stein, M.B,. (2010). Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biological Psychiatry, 68, 433-441.
20. Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., &, Noll, D.C., (1995). Improved assessment of significant activation in Functional Magnetic Resonance Imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33, 636-647.
21. Fox, M.D., &, Greicius, M.D., (2010). Clinical applications of resting state functional connectivity. Frontiers in Systems Neuroscience, 4, 1-13.
22. Fox, M.D., &, Raichle, M.E., (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8, 700-711.
23. Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., &, Raichle, M.E., (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102, 9673-9678.
24. Fransson, P., Skiöld, B., Engström, M., Hallberg, B., Mosskin, M., Aden, U.,... &, Blennow, M., (2009). Spontaneous brain activity in the newborn brain during natural sleep-an fMRI study in infants born at full term. Pediatric Research, 66, 301-305.
25. Gaffrey, M.S., Luby, J.L., Botteron, K., Repovš, G., &, Barch, D.M., (2012). Default mode network connectivity in children with a history of preschool onset depression. Journal of Child Psychology and Psychiatry, 53, 964-972.
26. Gao, W., Alcauter, S., Elton, A., Hernandez-Castillo, C.R., Smith, J.K., Ramirez, J., &, Lin, W., (2015). Functional network development during the first year: Relative sequence and socioeconomic correlations. Cerebral Cortex, 1-10, 25, 2919-1928.
27. Gao, W., Alcauter, S., Smith, J.K., Gilmore, J.H., &, Lin, W., (2015). Development of human brain cortical network architecture during infancy. Brain Structure and Function, 220, 1173-1186.
28. Gao, W., Elton, A., Zhu, H., Alcauter, S., Smith, J.K., Gilmore, J.H., &, Lin, W., (2014). Intersubject variability of and genetic effects on the brain's functional connectivity during infancy. The Journal of Neuroscience, 34, 11288-11296.
29. Gao, W., Gilmore, J.H., Giovanello, K.S., Smith, J.K., Shen, D., Zhu, H., &, Lin, W., (2011). Temporal and spatial evolution of brain network topology during the first two years of life. PLoS One, 6, e25278.
30. Gao, W., Gilmore, J.H., Shen, D., Smith, J.K., Zhu, H., &, Lin, W., (2013). The synchronization within and interaction between the default and dorsal attention networks in early infancy. Cerebral Cortex, 23, 594-603.
31. Gao, W., Zhu, H., Giovanello, K.S., Smith, J.K., Shen, D., Gilmore, J. H., &, Lin, W,. (2009). Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects. Proceedings of the National Academy of Sciences of the United States of America, 106, 6790-6795.
32. Gartstein, M.A., Putnam, S., &, Rothbart, M.K., (2012). Etiology of preschool behavior problems: Contributions of temperament attributes in early childhood. Infant Mental Health Journal, 33, 197-211.
33. Gartstein, M.A., &, Rothbart, M.K., (2003). Studying infant temperament via the Revised Infant Behavior Questionnaire. Infant Behavior and Development, 26, 64-86.
34. Gee, D.G., Gabard-Durnam, L.J., Flannery, J., Goff, B., Humphreys, K.L., Telzer, E.H.,... &, Tottenham, N., (2013). Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proceedings of the National Academy of Sciences of the United States of America, 110, 15638-15643.
35. Gluckman, P.D., &, Hanson, M.A., (2004). Living with the past: evolution, development, and patterns of disease. Science, 305, 1733-1736.
36. Graham, A.M., Fisher, P.A., &, Pfeifer, J.H., (2013). What sleeping babies hear: A functional MRI study of interparental conflict and infants' emotion processing. Psychological Science, 24, 782-789.
37. Graham, A.M., Kim, H.K., &, Fisher, P.A., (2012). Partner aggression in high-risk families from birth to age 3 years: Associations with harsh parenting and child maladjustment. Journal of Family Psychology, 26, 105-114.
38. Graham, A.M., Pfeifer, J.H., Fisher, P.A., Lin, W., Gao, W., &, Fair, D.A., (2015). The potential of infant fMRI research and the study of early life stress as a promising exemplar. Developmental Cognitive Neuroscience, 12, 12-39.
39. Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C.J., Wedeen, V.J., &, Sporns, O., (2008). Mapping the structural core of human cerebral cortex. PLoS Biology, 6, e159.
40. Hallquist, M.N., Hwang, K., &, Luna, B., (2013). The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage, 82, 208-225.
41. IBM Corp. (2012). IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.
42. Lancaster, J.L., Glass, T.G., Lankipalli, B.R., Downs, H., Mayberg, H., &, Fox, P.T., (1995). A modality-independent approach to spatial normalization of tomographic images of the human brain. Human Brain Mapping, 3, 209-223.
43. Lanius, R.A., Bluhm, R.L., Coupland, N.J., Hegadoren, K.M., Rowe, B., Théberge, J.,... &, Brimson, M., (2010). Default mode network connectivity as a predictor of post-traumatic stress disorder symptom severity in acutely traumatized subjects. Acta Psychiatrica Scandinavica, 121, 33-40.
44. Liston, C., Miller, M.M., Goldwater, D.S., Radley, J.J., Rocher, A.B., Hof, P.R.,... &, McEwen, B.S., (2006). Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26, 7870-7874.
45. Loman, M.M., &, Gunnar, M.R., (2010). Early experience and the development of stress reactivity and regulation in children. Neuroscience and Biobehavioral Reviews, 34, 867-876.
46. Love, O.P., &, Williams, T.D., (2008). Plasticity in the adrenocortical response of a free-living vertebrate: The role of pre- and post-natal developmental stress. Hormones and Behavior, 54, 496-505.
47. McCrory, E.J., De Brito, S.A., Kelly, P.A., Bird, G., Sebastian, C.L., Mechelli, A.,... &, Viding, E,. (2013). Amygdala activation in maltreated children during pre-attentive emotional processing. The British Journal of Psychiatry, 202, 269-276.
48. Meyer-Lindenberg, A., &, Tost, H., (2012). Neural mechanisms of social risk for psychiatric disorders. Nature Neuroscience, 15, 663-668.
49. Michelon, P., Snyder, A.Z., Buckner, R.L., McAvoy, M., &, Zacks, J.M., (2003). Neural correlates of incongruous visual information An event-related fMRI study. NeuroImage, 19, 1612-1626.
50. Moriceau, S., Roth, T.L., &, Sullivan, R.M., (2010). Rodent model of infant attachment learning and stress. Developmental Psychobiology, 52, 651-660.
51. Parade, S.H., &, Leerkes, E.M., (2008). The reliability and validity of the Infant Behavior Questionnaire-Revised. Infant Behavior & Development, 31, 637-646.
52. Philip, N.S., Sweet, L.H., Tyrka, A.R., Price, L.H., Bloom, R.F., &, Carpenter, L.L., (2013). Decreased default network connectivity is associated with early life stress in medication-free healthy adults. European Neuropsychopharmacology, 23, 24-32.
53. Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L., &, Petersen, S.E., (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59, 2142-2154.
54. Preacher, K.J., &, Hayes, A.F., (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40, 879-891.
55. Propper, C., &, Moore, G.A., (2006). The influence of parenting on infant emotionality: A multi-level psychobiological perspective. Developmental Review, 26, 427-460.
56. Raichle, M.E., (2010). Two views of brain function. Trends in Cognitive Sciences, 14, 180-190.
57. Raichle, M.E., Macleod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., &, Shulman, G.L., (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98, 676-682.
58. Sánchez, M.M., Ladd, C.O.C.O., &, Plotsky, P.M., (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology, 13, 419-449.
59. Sandor, S., &, Leahy, R., (1997). Surface-based labeling of cortical anatomy using a deformable atlas. IEEE Transactions on Medical Imaging, 16, 41-54.
60. Shattuck, D.W., Sandor-Leahy, S.R., Schaper, K.A., Rottenberg, D.A., &, Leahy, R.M., (2001). Magnetic resonance image tissue classification using a partial volume model. NeuroImage, 13, 856-876.
61. Shaw, P., Greenstein, D., Lerch, J., Clasen, L., Lenroot, R., Gogtay, N.,... &, Giedd, J., (2006). Intellectual ability and cortical development in children and adolescents. Nature, 440, 676-679.
62. Sheline, Y.I., Price, J.L., Yan, Z., &, Mintun, M.A., (2010). Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proceedings of the National Academy of Sciences of the United States of America, 107, 11020-11025.
63. Shortt, J.W., Capaldi, D.M., Kim, H.K., &, Owen, L.D., (2006). Relationship separation for young, at-risk couples: Prediction from dyadic aggression. Journal of Family Psychology, 20, 624-631.
64. Smith, S.M., (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143-155.
65. Smith, S.M., Bannister, P., Beckmann, C., &, Brady, M,. (2001). FSL: New tools for functional and structural brain image analysis. NeuroImage, 6, S249.
66. Smith, G.C., Gutovich, J., Smyser, C.D., Pineda, R., Newnham, C., Tjoeng, T.H.,... &, Inder, T., (2011). Neonatal intensive care unit stress is associated with brain development in preterm infants. Annals of Neurology, 70, 541-549.
67. Smith Slep, A.M., &, O'Leary, S.G., (2005). Parent and partner violence in families with young children: Rates, patterns, and connections. Journal of Consulting and Clinical Psychology, 73, 435-444.
68. Smyser, C.D., Inder, T.E., Shimony, J.S., Hill, J.E., Degnan, A.J., Snyder, A.Z., &, Neil, J.J., (2010). Longitudinal analysis of neural network development in preterm infants. Cerebral Cortex, 20, 2852-2862.
69. Snyder, D.K., (1997). Marital satisfaction inventory-Revised. CA: Western Psychological Services.
70. Sripada, R.K., Swain, J.E., Evans, G.W., Welsh, R.C., &, Liberzon, I., (2014). Childhood poverty and stress reactivity are associated with aberrant functional connectivity in default mode network. Neuropsychopharmacology, 39, 2244-2251.
71. Stein, J.L., Wiedholz, L.M., Bassett, D.S., Weinberger, D.R., Zink, C.F., Mattay, V.S., &, Meyer-Lindenberg, A., (2007). A validated network of effective amygdala connectivity. NeuroImage, 36, 736-745.
72. Straus, M.A., Hamby, S.L., Boney-McCoy, S., &, Sugarman, D.B., (1996). The Revised Conflict Tactics Scales (CTS2). Journal of Family Issues, 17, 283-316.
73. Sylvester, C.M., Corbetta, M., Raichle, M.E., Rodebaugh, T.L., Schlaggar, B.L., Sheline, Y.I.,... &, Lenze, E.J., (2012). Functional network dysfunction in anxiety and anxiety disorders. Trends in Neurosciences, 35, 527-535.
74. Talairach, P., &, Tournoux, J., (1988). Co-planar stereotaxic altas of the human brain. Stuttgart, Germany: Georg Thieme Verlag.
75. Thesen, S., Heid, O., Mueller, E., &, Schad, L.R,. (2000). Prospective acquisition correction for head motion with image-based tracking for real-time fMRI. Magnetic Resonance in Medicine, 44, 457-465.
76. Tottenham, N,. (2012). Human amygdala development in the absence of species expected caregiving. Developmental Psychobiology, 54, 598-611.
77. Tottenham, N,. (2014). The Importance of Early Experiences for Neuro-Affective Development. In, D.S. Pine, &, S.L. Andersen, (Eds.), Current topics in behavioral neuroscience, volume 16: The neurobiology of childhood. Berlin: Springer-Verlag.
78. Tottenham, N., Hare, T.A., Millner, A., Gilhooly, T., Zevin, J.D., &, Casey, B.J., (2011). Elevated amygdala response to faces following early deprivation. Developmental Science, 14, 190-204.
79. Tottenham, N., &, Sheridan, M.A., (2010). A review of adversity, the amygdala and the hippocampus: A consideration of developmental timing. Frontiers in Human Neuroscience, 3, 1-18.
80. Uchida, S., Hara, K., Kobayashi, A., Funato, H., Hobara, T., Otsuki, K.,... &, Watanabe, Y., (2010). Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. The Journal of Neuroscience, 30, 15007-15018.
81. Veer, I.M., Oei, N.Y.L., Spinhoven, P., van Buchem, M.A., Elzinga, B.M., &, Rombouts, S.A.R.B,. (2011). Beyond acute social stress: Increased functional connectivity between amygdala and cortical midline structures. NeuroImage, 57, 1534-1541.
82. Whitfield-Gabrieli, S., &, Ford, J.M., (2012). Default mode network activity and connectivity in psychopathology. Annual Review of Clinical Psychology, 8, 49-76.
83. Zhou, Y., Wang, Z., Qin, L., Wan, J., Sun, Y., Su, S.,... &, Xu, J., (2012). Early altered resting-state functional connectivity predicts the severity of post-traumatic stress disorder symptoms in acutely traumatized subjects. PLoS One, 7, e46833.