Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-13T03:08:15.649Z Has data issue: false hasContentIssue false
  • English
  • Français

The association between early life stress and prefrontal cortex activation during implicit emotion regulation is moderated by sex in early adolescence

Published online by Cambridge University Press:  22 November 2017

Natalie L. Colich ,
Eileen S. Williams ,
Tiffany C. Ho ,
Lucy S. King ,
Kathryn L. Humphreys ,
Alexandria N. Price ,
Sarah J. Ordaz  and
Ian H. Gotlib
Natalie L. Colich*
Affiliation:
Stanford University
Eileen S. Williams
Affiliation:
Stanford University
Tiffany C. Ho
Affiliation:
Stanford University
Lucy S. King
Affiliation:
Stanford University
Kathryn L. Humphreys
Affiliation:
Stanford University
Alexandria N. Price
Affiliation:
Stanford University
Sarah J. Ordaz
Affiliation:
Stanford University
Ian H. Gotlib
Affiliation:
Stanford University
*
Address correspondence and reprint requests to: Natalie Colich, Department of Psychology, Stanford University, Stanford, CA 94305; E-mail: ncolich@stanford.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

Early life stress (ELS) is a significant risk factor for the emergence of internalizing problems in adolescence. Beginning in adolescence, females are twice as likely as males to experience internalizing disorders. The present study was designed to examine sex differences in the association between ELS and internalizing problems in early pubertal adolescents, and whether and how corticolimbic function and connectivity may underlie these associations. Fifty-nine early pubertal males and 78 early pubertal females, ages 9–13 years (all Tanner Stage 3 or below) underwent functional magnetic resonance imaging as they performed an emotion label task that robustly interrogates corticolimbic function. Participants were also interviewed about their experience of ELS. Females exhibited a positive association between ELS and internalizing problems, whereas males exhibited no such association. Whole-brain and amygdala region of interest analyses indicated that whereas females exhibited a positive association between ELS and the ventrolateral prefrontal cortex during implicit emotion regulation, males showed no such association. Activation in these regions was positively associated with internalizing problems in females but not males; however, activation in these regions did not mediate the association between ELS and internalizing problems. Finally, both boys and girls exhibited an association between ELS and increased negative connectivity between the right ventrolateral prefrontal cortex and bilateral amygdala. Using a carefully characterized sample of early pubertal adolescents, the current study highlights important sex differences in the development of corticolimbic circuitry during a critical period of brain development. These sex differences may play a significant role in subsequent risk for internalizing problems.

Type
Special Issue Articles
Information
Development and Psychopathology , Volume 29 , Special Issue 5: Biological and Behavioral Effects of Early Adversity on Multiple Levels of Development , December 2017 , pp. 1851 - 1864
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

We thank Holly Pham, Isabella Lazzareschi, Cat Camacho, Monica Ellwood-Lowe, Sophie Schouboe, Maddie Pollak, and Morgan Popolizio for their assistance in scheduling and running the participants. We also thank the adolescents and families who participated in our study. This work was supported by NIMH Grants R01MH101495 (to I.H.G.), K01MH106805 (to S.J.O.), and F32MH107129 (to K.L.H.N.); the Brain & Behavior Research Foundation Young Investigator Awards 23583 (to S.J.O.) 23819 (to K.L.H.); the Klingenstein Third Generation Foundation Fellowship Awards (to S.J.O. and K.L.H.); the National Science Foundation Graduate Fellowship Awards (to N.L.C. and L.S.K.); and the Stanford University Gerald J. Lieberman Graduate Fellowship (to N.L.C.).

References

Achenbach, T. M. (1991). Integrative Guide to the 1991 CBCL/4–18, YSR, and TRF profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families.Google Scholar
Achenbach, T. M., & Rescorla, L. A. (2001). Manual for the ASEBA school-age forms and profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families.Google Scholar
Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: Sage.Google Scholar
Andersen, S. L., & Teicher, M. H. (2008). Stress, sensitive periods and maturational events in adolescent depression. Trends in Neurosciences, 31, 183–191. doi:10.1016/j.tins.2008.01.004 Google Scholar
Andersen, S. L., Tomada, A., Vincow, E. S., Valente, E., Polcari, A., & Teicher, M. H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry, 20, 292–301. doi:10.1176/appi.neuropsych.20.3.292 CrossRefGoogle ScholarPubMed
Angold, A., Costello, E. J., & Worthman, C. M. (1998). Puberty and depression: The roles of age, pubertal status and pubertal timing. Psychological Medicine, 28, 51–61.CrossRefGoogle ScholarPubMed
Bangasser, D. A., & Valentino, R. J. (2014). Sex differences in stress-related psychiatric disorders: Neurobiological perspectives. Frontiers in Neuroendocrinology, 35, 303–319. doi:10.1016/j.yfrne.2014.03.008 Google Scholar
Barnett, D., Manly, J. T., & Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. In Cicchetti, D. & Toth, S. L. (Eds.), Child abuse, child development, and social policy (pp. 7–73). Norwood, NJ: Ablex.Google Scholar
Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003). General multilevel linear modeling for group analysis in FMRI. NeuroImage, 20, 1052–1063. doi:10.1016/S1053-8119(03)00435-X Google Scholar
Bourke, C. H., Harrell, C. S., & Neigh, G. N. (2012). Stress-induced sex differences: Adaptations mediated by the glucocorticoid receptor. Hormones and Behavior, 62, 210–218. doi:10.1016/j.yhbeh.2012.02.024 Google Scholar
Burghy, C. A., Stodola, D. E., Ruttle, P. L., Molloy, E. K., Armstrong, J. M., Oler, J. A., … Birn, R. M. (2012). Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nature Neuroscience, 15, 1–8. doi:10.1038/nn.3257 Google Scholar
Callaghan, B. L., & Tottenham, N. (2016). The stress acceleration hypothesis: Effects of early-life adversity on emotion circuits and behavior. Current Opinion in Behavioral Sciences, 7, 76–81. doi:10.1016/j.cobeha.2015.11.018 CrossRefGoogle ScholarPubMed
Casey, B. J., Jones, R. M., & Hare, T. A. (2008). The adolescent brain. Annals of the New York Academy of Sciences, 1124, 111–126. doi:10.1196/annals.1440.010 CrossRefGoogle ScholarPubMed
Cohen-Gilbert, J. E., & Thomas, K. M. (2013). Inhibitory control during emotional distraction across adolescence and early adulthood, 84, 1954–1966. doi:10.1111/cdev.12085 Google ScholarPubMed
Coleman, L., & Coleman, J. (2002). The measurement of puberty: A review. Journal of Adolescence, 25, 535–550. doi:10.1006/jado.2002.0494 Google Scholar
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., … Kugel, H. (2012). Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry, 71, 286–293. doi:10.1016/j.biopsych.2011.10.021 Google Scholar
Eiland, L., & Romeo, R. D. (2013). Stress and the developing adolescent brain. Neuroscience, 249, 162–171. doi:10.1016/j.neuroscience.2012.10.048 CrossRefGoogle ScholarPubMed
Fan, Y., Herrera-Melendez, A. L., Pestke, K., Feeser, M., Aust, S., Otte, C., … Grimm, S. (2014). Early life stress modulates amygdala-prefrontal functional connectivity: Implications for oxytocin effects. Human Brain Mapping, 35, 5328–5339. doi:10.1002/hbm.22553 Google Scholar
Forbes, E. E., Phillips, M. L., Silk, J. S., Ryan, N. D., & Dahl, R. E. (2011). Neural systems of threat processing in adolescents: Role of pubertal maturation and relation to measures of negative affect. Developmental Neuropsychology, 36, 429–452. doi:10.1080/87565641.2010.550178 CrossRefGoogle ScholarPubMed
Friston, K., Buechel, C., Fink, G., Morris, J., Rolls, E., & Dolan, R. (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage, 6, 218–229. doi:10.1006/nimg.1997.0291 CrossRefGoogle ScholarPubMed
Garrett, A. S., Carrion, V., Kletter, H., Karchemskiy, A., Weems, C. F., & Reiss, A. (2012). Brain activation to facial expressions in youth with PTSD symptoms. Depression and Anxiety, 29, 449–459. doi:10.1002/da.21892 Google Scholar
Ge, X., Conger, R. D., & Elder, G. H. J. (2001). Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms. Developmental Psychology, 37, 404–417. doi:10.1037/0012-1649.37.3.404 Google Scholar
Ge, X., Lorenz, F. O., Conger, R. D., Elder, G. H., & Simons, R. L. (1994). Trajectories of stressful life events and depressive symptoms during adolescence. Developmental Psychology, 30, 467–483.Google Scholar
Gee, D. G., & Casey, B. J. (2015). The impact of developmental timing for stress and recovery. Neurobiology of Stress, 1, 184–194. doi:10.1016/j.ynstr.2015.02.001 Google Scholar
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, 110, 15638–15643. doi:10.1073/pnas.1307893110 CrossRefGoogle ScholarPubMed
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., … Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience, 33, 4584–4593. doi:10.1523/jneurosci.3446-12.2013 CrossRefGoogle ScholarPubMed
Gee, D. G., Karlsgodt, K. H., van Erp, T. G. M., Bearden, C. E., Lieberman, M. D., Belger, A., … Cannon, T. D. (2012). Altered age-related trajectories of amygdala-prefrontal circuitry in adolescents at clinical high risk for psychosis: A preliminary study. Schizophrenia Research, 134, 1–9. doi:10.1016/j.schres.2011.10.005 CrossRefGoogle ScholarPubMed
Giedd, J. N. (2004). Structural magnetic resonance imaging of the adolescent brain. Annals of the New York Academy of Sciences, 1021, 77–85. doi:10.1196/annals.1308.009 Google Scholar
Green, J. G., Mclaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2010). Childhood adversities and adult psychiatric disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 67, 113–123. doi:10.1001/archgenpsychiatry.2009.187 CrossRefGoogle ScholarPubMed
Hankin, B. L., & Abramson, L. Y. (1999). Development of gender differences in depression: Description and possible explanations. Annals of Medicine, 31, 372–379. doi:10.3109/07853899908998794 Google Scholar
Hariri, A., Bookheimer, S. Y., & Mazziotta, J. C. (2000). Modulating emotional responses: Effects of a neocortical network on the limbic system. NeuroReport, 11, 43–48.CrossRefGoogle ScholarPubMed
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.Google Scholar
Hayward, C., Gotlib, I. H., Schraedley, P. K., & Litt, I. F. (1999). Ethnic differences in the association between pubertal status and symptoms of depression in adolescent girls. Journal of Adolescent Health, 25, 143–149.Google Scholar
Heim, C., & Binder, E. B. (2012). Current research trends in early life stress and depression: Review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Experimental Neurology, 233, 102–111. doi:10.1016/j.expneurol.2011.10.032 Google Scholar
Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023–1039. doi:10.1016/S0006-3223(01)01157-X CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Wagner, D., Wilcox, M. M., Miller, A. H., & Nemeroff, C. B. (2002). The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: A multiple regression analysis. Depression and Anxiety, 15, 117–125. doi:10.1002/da.10015 CrossRefGoogle ScholarPubMed
Herringa, R. J., Birn, R. M., Ruttle, P. L., Burghy, C. A., Stodola, D. E., Davidson, R. J., & Essex, M. J. (2013). Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceedings of the National Academy of Sciences, 110, 19119–19124. doi:10.1073/pnas.1310766110 Google Scholar
Herringa, R. J., Burghy, C. A., Stodola, D. E., Fox, M. E., Davidson, R. J., & Essex, M. J. (2016). Enhanced prefrontal-amygdala connectivity following childhood adversity as a protective mechanism against internalizing in adolescence. Biological Psychiatry, 1, 326–334. doi:10.1016/j.bpsc.2016.03.003 Google Scholar
Humphreys, K. L., & Zeanah, C. H. (2015). Deviations from the expectable environment in early childhood and emerging psychopathology. Neuropsychopharmacology, 40, 154–170. doi:10.1038/npp.2014.165 CrossRefGoogle ScholarPubMed
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841. doi:10.1006/nimg.2002.1132 Google Scholar
Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156. doi:10.1016/S1361-8415(01)00036-6 CrossRefGoogle ScholarPubMed
Kajantie, E., & Phillips, D. I. W. (2006). The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology, 31, 151–178. doi:10.1016/j.psyneuen.2005.07.002 Google Scholar
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 593. doi:10.1001/archpsyc.62.6.593 Google Scholar
Lee, F. S., Heimer, H., Giedd, J. N., Lein, E. S., Estan, N., Weinberger, D. R., & Casey, B. J. (2014). Adolescent mental health—Opportunity and obligation. Science, 346, 547–549. doi:10.1126/science.1260497 Google Scholar
Lieberman, M. D., Eisenberger, N. I., Crockett, M. J., Tom, S. M., Pfeifer, J. H., & Way, B. M. (2007). Putting feelings into words: Affect labeling disrupts amygdala activity in response to affective stimuli. Psychological Science, 18, 421–428. doi:10.1111/j.1467-9280.2007.01916.x Google Scholar
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445. doi:10.1038/nrn2639 Google Scholar
Malter Cohen, M., Tottenham, N., & Casey, B. J. (2013). Translational developmental studies of stress on brain and behavior: Implications for adolescent mental health and illness? Neuroscience, 249, 53–62. doi:10.1016/j.neuroscience.2013.01.023 CrossRefGoogle ScholarPubMed
Marshall, W., & Tanner, J. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291–303. doi:10.1136/adc.44.235.291 Google Scholar
Marshall, W., & Tanner, J. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 13–23.Google Scholar
Marusak, H. A., Martin, K. R., Etkin, A., & Thomason, M. E. (2014). Childhood trauma exposure disrupts the automatic regulation of emotional processing. Neuropsychopharmacology, 40, 1250–1258. doi:10.1038/npp.2014.311 Google Scholar
Maughan, A., & Cicchetti, D. (2002). Impact of child maltreatment and interadult violence on children's emotion regulation abilities and socioemotional adjustment. Child Development, 73, 1525–1542. doi:10.1111/1467-8624.00488 Google Scholar
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. British Journal of Psychiatry, 202, 269–276. doi:10.1192/bjp.bp.112.116624 CrossRefGoogle ScholarPubMed
McEwen, B., & Morrison, J. (2013). The brain on stress: Vulnerability and plasticity of the prefrontal cortex over the life course. Neuron, 79, 16–29. doi:10.1016/j.neuron.2013.06.028 CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Greif Green, J., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2012). Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. Archives of General Psychiatry, 69, 1151. doi:10.1001/archgenpsychiatry.2011.2277 Google Scholar
McLaughlin, K. A., Peverill, M., Gold, A. L., Alves, S., & Sheridan, M. A. (2015). Child maltreatment and neural systems underlying emotion regulation. Journal of the American Academy of Child & Adolescent Psychiatry, 54, 753–762. doi:10.1016/j.jaac.2015.06.010 Google Scholar
McLaughlin, K. A., & Sheridan, M. A. (2016). Beyond cumulative risk: A dimensional approach to childhood adversity. Current Directions in Psychological Science, 25, 239–245. doi:10.1177/0963721416655883 CrossRefGoogle Scholar
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience and Biobehavioral Reviews, 47, 578–591. doi:10.1016/j.neubiorev.2014.10.012 Google Scholar
McRae, K., Gross, J. J., Weber, J., Robertson, E. R., Sokol-Hessner, P., Ray, R. D., … Ochsner, K. N. (2012). The development of emotion regulation: An fMRI study of cognitive reappraisal in children, adolescents and young adults. Social Cognitive and Affective Neuroscience, 7, 11–22. doi:10.1093/scan/nsr093 Google Scholar
Mueller, S. C., Maheu, F. S., Dozier, M., Peloso, E., Mandell, D., Leibenluft, E., … Ernst, M. (2010). Early-life stress is associated with impairment in cognitive control in adolescence: An fMRI study. Neuropsychologia, 48, 3037–3044. doi:10.1016/j.neuropsychologia.2010.06.013 CrossRefGoogle ScholarPubMed
Negriff, S., & Susman, E. J. (2011). Pubertal timing, depression, and externalizing problems: A framework, review, and examination of gender differences. Journal of Research on Adolescence, 21, 717–746. doi:10.1111/j.1532-7795.2010.00708.x Google Scholar
Nemeroff, C. B. (2004). Neurobiological consequences of childhood trauma. Journal of Clinical Psychiatry, 65(Suppl. 1), 18–28.Google ScholarPubMed
Novais, A., Monteiro, S., Roque, S., Correia-Neves, M., & Sousa, N. (2016). How age, sex and genotype shape the stress response. Neurobiology of Stress. Advance online publication. doi:10.1016/j.ynstr.2016.11.004 Google ScholarPubMed
Ochsner, K. N., Silvers, J. A., & Buhle, J. T. (2012). Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences, 1251, E1–E24. doi:10.1111/j.1749-6632.2012.06751.x CrossRefGoogle ScholarPubMed
Oldehinkel, A. J., Verhulst, F. C., & Ormel, J. (2011). Mental health problems during puberty: Tanner stage-related differences in specific symptoms. The TRAILS study. Journal of Adolescence, 34, 73–85. doi:10.1016/j.adolescence.2010.01.010 CrossRefGoogle ScholarPubMed
Ordaz, S., & Luna, B. (2012). Sex differences in physiological reactivity to acute psychosocial stress in adolescence. Psychoneuroendocrinology, 37, 1135–1157. doi:10.1016/j.psyneuen.2012.01.002 Google Scholar
O'Reilly, J. X., Woolrich, M. W., Behrens, T. E. J., Smith, S. M., & Johansen-Berg, H. (2012). Tools of the trade: Psychophysiological interactions and functional connectivity. Social Cognitive and Affective Neuroscience, 7, 604–609. doi:10.1093/scan/nss055 Google Scholar
Pechtel, P., Lyons-Ruth, K., Anderson, C. M., & Teicher, M. H. (2014). Sensitive periods of amygdala development: The role of maltreatment in preadolescence. NeuroImage, 97, 236–244. doi:10.1016/j.neuroimage.2014.04.025 Google Scholar
Pechtel, P., & Pizzagalli, D. A. (2011). Effects of early life stress on cognitive and affective function: An integrated review of human literature. Psychopharmacology, 214, 55–70. doi:10.1007/s00213-010-2009-2 Google Scholar
Pessoa, L. (2010). Emotion and cognition and the amygdala: From “what is it?” to “what's to be done?” Neuropsychologia, 48, 3416–3429. doi:10.1016/j.neuropsychologia.2010.06.038 Google Scholar
Pessoa, L., Kastner, S., & Ungerleider, L. G. (2002). Attentional control of the processing of neutral and emotional stimuli. Cognitive Brain Research, 15, 31–45. doi:10.1016/S0926-6410(02)00214-8 CrossRefGoogle Scholar
Peters, S., Jolles, D. J., Duijvenvoorde, A. C. K., Crone, E. A., & Peper, J. S. (2015). The link between testosterone and amygdala–orbitofrontal cortex connectivity in adolescent alcohol use. Psychoneuroendocrinology, 53, 117–126. doi:10.1016/j.psyneuen.2015.01.004 Google Scholar
Pfeifer, J. H., & Blakemore, S.-J. (2012). Adolescent social cognitive and affective neuroscience: Past, present, and future. Social Cognitive and Affective Neuroscience, 7, 1–10. doi:10.1093/scan/nsr099 Google Scholar
Phan, K. L., Fitzgerald, D. A., Nathan, P. J., Moore, G. J., Uhde, T. W., & Tancer, M. E. (2005). Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study. Biological Psychiatry, 57, 210–219. doi:10.1016/j.biopsych.2004.10.030 Google Scholar
Raffaelli, B., Strache, N., Parchetka, C., Artiges, E., Banaschewski, T., Bokde, A., … Gallinat, J. (2016). Sex-related differences in frequency and perception of stressful life events during adolescence. Journal of Public Health, 24, 365–374. doi:10.1007/s10389-016-0731-x Google Scholar
Ribbe, D. (1996). Psychometric review of Traumatic Events Screening Inventory for Children (TESI-C). In Stamm, B. (Ed.), Measurement of stress, trauma, and adaptation (pp. 386–387). Lutherville, MD: Sidran.Google Scholar
Rudolph, K. D., & Flynn, M. (2007). Childhood adversity and youth depression: Influence of gender and pubertal status. Development and Psychopathology, 19, 497–521. doi:10.1017/S0954579407070241 Google Scholar
Rudolph, K. D., & Hammen, C. (1999). Age and gender as determinants of stress exposure, generation, and reactions in youngsters: A transactional perspective. Child Development, 70, 660–677. doi:10.1111/1467-8624.00048 CrossRefGoogle ScholarPubMed
Rudolph, K. D., Hammen, C., Burge, D., Lindberg, N., Herzberg, D., & Daley, S. E. (2000). Toward an interpersonal life-stress model of depression: The developmental context of stress generation. Development and Psychopathology, 12, 215–234. doi:10.1017/S0954579400002066 Google Scholar
Sanchez, M. M., Young, L. J., Plotsky, P. M., & Insel, T. R. (2000). Distribution of corticosteroid receptors in the rhesus brain: Relative absence of glucocorticoid receptors in the hippocampal formation. Journal of Neuroscience, 20, 4657–4668. doi:20/12/4657 Google Scholar
Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009). Pubertal development: Correspondence between hormonal and physical development. Child Development, 80, 327–337. doi:10.1111/j.1467-8624.2009.01263.x Google Scholar
Silvers, J. A., Insel, C., Powers, A., Franz, P., Helion, C., Martin, R. E., … Ochsner, K. N. (2016). vlPFC–vmPFC–amygdala interactions underlie age-related differences in cognitive regulation of emotion. Cerebral Cortex. Advance online publication. doi:10.1093/cercor/bhw073 Google Scholar
Slora, E. J., Bocian, A. B., Herman-Giddens, M. E., Harris, D. L., Pedlow, S. E., Dowshen, S. A., & Wasserman, R. C. (2009). Assessing inter-rater reliability (IRR) of Tanner staging and orchidometer use with boys: A study from PROS. Journal of Pediatric Endocrinology and Metabolism, 22, 291–299.Google Scholar
Somerville, L., Hare, T., & Casey, B. (2011). Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents. Journal of Cognitive Neuroscience, 23, 2123–2134. doi:10.1162/jocn.2010.21572 Google Scholar
Spielberg, J. M., Forbes, E. E., Ladouceur, C. D., Worthman, C. M., Olino, T. M., Ryan, N. D., & Dahl, R. E. (2014). Pubertal testosterone influences threat-related amygdala-orbitofrontal coupling. Social Cognitive and Affective Neuroscience. Advance online publication. doi:10.1093/scan/nsu062 Google Scholar
Spielberg, J. M., Olino, T. M., Forbes, E. E., & Dahl, R. E. (2014). Exciting fear in adolescence: Does pubertal development alter threat processing? Developmental Cognitive Neuroscience, 8, 86–95. doi:10.1016/j.dcn.2014.01.004 Google Scholar
Stevens, J. S., & Hamann, S. (2012). Sex differences in brain activation to emotional stimuli: A meta-analysis of neuroimaging studies. Neuropsychologia, 50, 1578–1593. doi:10.1016/j.neuropsychologia.2012.03.011 CrossRefGoogle ScholarPubMed
Suzuki, H., Luby, J. L., Botteron, K. N., Dietrich, R., McAvoy, M. P., & Barch, D. M. (2014). Early life stress and trauma and enhanced limbic activation to emotionally valenced faces in depressed and healthy children. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 800–813. doi:10.1016/j.jaac.2014.04.013 CrossRefGoogle ScholarPubMed
Taylor, S. E., Eisenberger, N. I., Saxbe, D., Lehman, B. J., & Lieberman, M. D. (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry, 60, 296–301. doi:10.1016/j.biopsych.2005.09.027 Google Scholar
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience & Biobehavioral Reviews, 27, 33–44. doi:10.1016/S0149-7634(03)00007-1 CrossRefGoogle ScholarPubMed
Teicher, M. H., & Samson, J. A. (2016). Annual Research Review: Enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry, 57, 241–266. doi:10.1111/jcpp.12507 CrossRefGoogle ScholarPubMed
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience, 17, 652–666. doi:10.1038/nrn.2016.111 Google Scholar
Tottenham, N., & Galván, A. (2016). Stress and the adolescent brain. Neuroscience Biobehavioral Reviews, 70, 217–227. doi:10.1016/j.neubiorev.2016.07.030 Google Scholar
Tottenham, N., Hare, T. A., & Casey, B. J. (2011). Behavioral assessment of emotion discrimination, emotion regulation, and cognitive control in childhood, adolescence, and adulthood. Frontiers in Psychology, 2, 1–9. doi:10.3389/fpsyg.2011.00039 CrossRefGoogle ScholarPubMed
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. doi:10.1111/j.1467-7687.2010.00971.x Google Scholar
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., … Casey, B. J. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13, 46–61. doi:10.1111/j.1467-7687.2009.00852.x CrossRefGoogle ScholarPubMed
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., … Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242–249. doi:10.1016/j.psychres.2008.05.006 Google Scholar
van Harmelen, A.-L., van Tol, M.-J., Dalgleish, T., van der Wee, N. J. A., Veltman, D. J., Aleman, A., … Elzinga, B. M. (2014). Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience, 9, 2026–2033. doi:10.1093/scan/nsu008 Google Scholar
van Harmelen, A.-L., van Tol, M.-J., Demenescu, L. R., van der Wee, N. J. A., Veltman, D. J., Aleman, A., … Elzinga, B. M. (2013). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience, 8, 362–369. doi:10.1093/scan/nss007 Google Scholar
Weiss, E., Longhurt, J., & Mazure, C. (1999). Childhood sexual abuse as a risk factor for depression in women: Psychosocial and neurobiological correlates. American Journal of Psychiatry, 156, 816–828.Google Scholar
Wolf, R. C., & Herringa, R. J. (2016). Prefrontal–amygdala dysregulation to threat in pediatric posttraumatic stress disorder. Neuropsychopharmacology, 41, 822–831. doi:10.1038/npp.2015.209 Google Scholar
Woolrich, M. (2008). Robust group analysis using outlier inference. NeuroImage, 41, 286–301. doi:10.1016/j.neuroimage.2008.02.042 Google Scholar
Woolrich, M. W., Behrens, T. E. J., Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2004). Multilevel linear modelling for FMRI group analysis using Bayesian inference. NeuroImage, 21, 1732–1747. doi:10.1016/j.neuroimage.2003.12.023 Google Scholar
Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage, 14, 1370–1386. doi:10.1006/nimg.2001.0931 Google Scholar
Worsley, K. J. (2001). Statistical analysis of activation images. In Jezzard, P., Matthews, P. M., & Smith, S. M. (Eds.), Functional MRI: An introduction to methods (pp. 251–270). New York: Oxford University Press.Google Scholar
Yurgelun-Todd, D. A., & Killgore, W. D. S. (2006). Fear-related activity in the prefrontal cortex increases with age during adolescence: A preliminary fMRI study. Neuroscience Letters, 406, 194–199. doi:10.1016/j.neulet.2006.07.046 Google Scholar