Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T21:21:21.494Z Has data issue: false hasContentIssue false
  • English
  • Français

Working memory moderates the association between early institutional care and separation anxiety symptoms in late childhood and adolescence

Published online by Cambridge University Press:  30 April 2019

Laura Alicia Alba ,
Jessica Flannery ,
Mor Shapiro  and
Nim Tottenham
Laura Alicia Alba
Affiliation:
Department of School Psychology, University of California, Riverside, Riverside, CA, USA
Jessica Flannery
Affiliation:
Department of Psychology, University of Oregon, Eugene, OR, USA
Mor Shapiro
Affiliation:
Kaiser Permanente, Oakland, CA, USA
Nim Tottenham*
Affiliation:
Department of Psychology, Columbia University, New York, NY, USA
*
Author for correspondence: Nim Tottenham, Department of Psychology, Columbia University, 1190 Amsterdam Avenue MC5501, New York, NY 10027; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Adverse caregiving, for example, previous institutionalization (PI), is often associated with emotion dysregulation that increases anxiety risk. However, the concept of developmental multifinality predicts heterogeneity in anxiety outcomes. Despite this well-known heterogeneity, more work is needed to identify sources of this heterogeneity and how these sources interact with environmental risk to influence mental health. Here, working memory (WM) was examined during late childhood/adolescence as an intra-individual factor to mitigate the risk for separation anxiety, which is particularly susceptible to caregiving adversities. A modified “object-in-place” task was administered to 110 youths (10–17 years old), with or without a history of PI. The PI youths had elevated separation anxiety scores, which were anticorrelated with morning cortisol levels, yet there were no group differences in WM. PI youths showed significant heterogeneity in separation anxiety symptoms and morning cortisol levels, and WM moderated the link between caregiving and separation anxiety and mediated the association between separation anxiety and morning cortisol in PI youth. Findings suggest that (a) institutional care exerts divergent developmental consequences on separation anxiety versus WM, (b) WM interacts with adversity-related emotion dysregulation, and (c) WM may be a therapeutic target for separation anxiety following early caregiving adversity.

Keywords

cortisolearly caregiving adversityemotion dysregulationseparation anxietyworking memory
Type
Special Issue Articles
Information
Development and Psychopathology , Volume 31 , Special Issue 3: Emotion Dysregulation and Emerging Psychopathology , August 2019 , pp. 989 - 997
Copyright
Copyright © Cambridge University Press 2019 

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.)

References

Avishai-Eliner, S., Yi, S. J., & Baram, T. Z. (1996). Developmental profile of messenger RNA for the corticotropin-releasing hormone receptor in the rat limbic system. Developmental Brain Research, 91, 159–163. doi:0165380695001581Google Scholar
Bachevalier, J., & Nemanic, S. (2008). Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus, 18, 64–80. doi:10.1002/hipo.20369Google Scholar
Baddeley, A. (1992). Working memory. Science, 255, 556–559.Google Scholar
Baram, T. Z., Hirsch, E., Snead, O. C. III, & Schultz, L. (1992). Corticotropin-releasing hormone-induced seizures in infant rats originate in the amygdala. Annals of Neurology, 31, 488–494. doi:10.1002/ana.410310505Google Scholar
Barker, G. R., & Warburton, E. C. (2015). Object-in-place associative recognition memory depends on glutamate receptor neurotransmission within two defined hippocampal-cortical circuits: A critical role for AMPA and NMDA receptors in the hippocampus, perirhinal, and prefrontal cortices. Cerebral Cortex, 25, 472–481. doi:10.1093/cercor/bht245Google Scholar
Beauchaine, T. P. (2015). Future directions in emotion dysregulation and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 44, 875–896. doi:10.1080/15374416.2015.1038827Google Scholar
Beauchaine, T. P., & Thayer, J. F. (2015). Heart rate variability as a transdiagnostic biomarker of psychopathology. International Journal of Psychophysiology, 98(2, Pt. 2), 338–350. doi:10.1016/j.ijpsycho.2015.08.004Google Scholar
Beauchaine, T. P., & Zisner, A. (2017). Motivation, emotion regulation, and the latent structure of psychopathology: An integrative and convergent historical perspective. International Journal of Psychophysiology, 119, 108–118. doi:10.1016/j.ijpsycho.2016.12.014Google Scholar
Bick, J., Zeanah, C. H., Fox, N. A., & Nelson, C. A. (2018). Memory and executive functioning in 12-year-old children with a history of institutional rearing. Child Development, 89, 495–508. doi:10.1111/cdev.12952Google Scholar
Birmaher, B. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 545.Google Scholar
Birmaher, B., Brent, D. A., Chiappetta, L., Bridge, J., Monga, S., & Baugher, M. (1999). Psychometric properties of the Screen for Child Anxiety Related Emotional Disorders (SCARED): A replication study. Journal of the American Academy of Child & Adolescent Psychiatry, 38, 1230–1236.Google Scholar
Blair, C., & Raver, C. C. (2016). Poverty, stress, and brain development: New directions for prevention and intervention. Academic Pediatrics, 16(3, Suppl.), S30–S36. doi:10.1016/j.acap.2016.01.010Google Scholar
Buchanan, T. W., Tranel, D., & Adolphs, R. (2006). Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learning and Memory, 13, 382–387. doi:10.1101/lm.206306Google Scholar
Castle, J., Groothues, C., Bredenkamp, D., Beckett, C., O'Connor, T., & Rutter, M. (1999). Effects of qualities of early institutional care on cognitive attainment. E.R.A. Study Team. English and Romanian Adoptees. American Journal of Orthopsychiatry, 69, 424–437.Google Scholar
Church, J. A., Petersen, S. E., & Schlaggar, B. L. (2010). The “Task B problem” and other considerations in developmental functional neuroimaging. Human Brain Mapping, 31, 852–862 doi:10.1002/hbm.21036Google Scholar
Cicchetti, D., & Rogosch, F. A. (1997). The role of self-organization in the promotion of resilience in maltreated children. Development and Psychopathology, 9, 797–815.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2007). Personality, adrenal steroid hormones, and resilience in maltreated children: A multilevel perspective. Development and Psychopathology, 19, 787–809. doi:10.1017/S0954579407000399Google Scholar
Cole, P. M., Hall, S. E., & Hajal, N. J. (2013). Emotion dysregulation as a risk factor for psychopathology. In Beauchaine, T. P. & Hinshaw, S. P. (Eds.), Child and adolescent psychopathology (2nd ed.). Hoboken, NJ: Wiley.Google Scholar
Curtis, W. J., & Cicchetti, D. (2007). Emotion and resilience: A multilevel investigation of hemispheric electroencephalogram asymmetry and emotion regulation in maltreated and nonmaltreated children. Development and Psychopathology, 19, 811–840. doi:10.1017/S0954579407000405Google Scholar
Dabbs, J. M. Jr. (1991). Salivary testosterone measurements: Collecting, storing, and mailing saliva samples. Physiology and Behavior, 49, 815–817.Google Scholar
Doom, J. R., & Cicchetti, D. (2018). The developmental psychopathology of stress exposure in childhood. In Harkness, K. & Hayden, E. P. (Eds.), The Oxford handbook of stress and mental health. New York: Oxford University Press.Google Scholar
Drury, S. S., Gleason, M. M., Theall, K. P., Smyke, A. T., Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2012). Genetic sensitivity to the caregiving context: The influence of 5httlpr and BDNF val66met on indiscriminate social behavior. Physiology and Behavior, 106, 728–735. doi:10.1016/j.physbeh.2011.11.014Google Scholar
Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1, 41–50. doi:10.1038/35036213Google Scholar
Ellis, B. H., Fisher, P. A., & Zaharie, S. (2004). Predictors of disruptive behavior, developmental delays, anxiety, and affective symptomatology among institutionally reared Romanian children. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 1283–1292. doi:10.1097/01.chi.0000136562.24085.160Google Scholar
Erickson, K., Drevets, W., & Schulkin, J. (2003). Glucocorticoid regulation of diverse cognitive functions in normal and pathological emotional states. Neuroscience and Biobehavioral Reviews, 27, 233–246.Google Scholar
Etkin, A., Prater, K. E., Hoeft, F., Menon, V., & Schatzberg, A. F. (2010). Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. American Journal of Psychiatry, 167, 545–554. doi:10.1176/appi.ajp.2009.09070931Google Scholar
Etkin, A., & Schatzberg, A. F. (2011). Common abnormalities and disorder-specific compensation during implicit regulation of emotional processing in generalized anxiety and major depressive disorders. American Journal of Psychiatry, 168, 968–978. doi:10.1176/appi.ajp.2011.10091290Google Scholar
Fenoglio, K. A., Brunson, K. L., Avishai-Eliner, S., Chen, Y., & Baram, T. Z. (2004). Region-specific onset of handling-induced changes in corticotropin-releasing factor and glucocorticoid receptor expression. Endocrinology, 145, 2702–2706. doi:10.1210/en.2004-0111Google Scholar
Flannery, J. E., Gabard-Durnam, L. J., Shapiro, M., Goff, B., Caldera, C., Louie, J., … Tottenham, N. (2017). Diurnal cortisol after early institutional care—Age matters. Developmental Cognitive Neuroscience. Advance online publication. doi:10.1016/j.dcn.2017.03.006Google Scholar
Fox, N. A., Almas, A. N., Degnan, K. A., Nelson, C. A., & Zeanah, C. H. (2011). The effects of severe psychosocial deprivation and foster care intervention on cognitive development at 8 years of age: Findings from the Bucharest Early Intervention Project. Journal of Child Psychology and Psychiatry, 52, 919–928. doi:10.1111/j.1469-7610.2010.02355.xGoogle 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. Procedings of the National Academy of Sciences of the USA, 110, 15638–15643. doi:10.1073/pnas.1307893110Google Scholar
Gilmore, J. H., Shi, F., Woolson, S. L., Knickmeyer, R. C., Short, S. J., Lin, W., … Shen, D. (2012). Longitudinal development of cortical and subcortical gray matter from birth to 2 years. Cerebral Cortex, 22, 2478–2485. doi:10.1093/cercor/bhr327Google Scholar
Green, S. A., Goff, B., Gee, D. G., Gabard-Durnam, L., Flannery, J., Telzer, E. H., … Tottenham, N. (2016). Discrimination of amygdala response predicts future separation anxiety in youth with early deprivation. Journal of Child Psychology and Psychiatry, 57, 1135–1144. doi:10.1111/jcpp.12578Google Scholar
Gunnar, M. R., Bruce, J., & Grotevant, H. D. (2000). International adoption of institutionally reared children: Research and policy. Development and Psychopathology, 12, 677–693.Google Scholar
Gunnar, M. R., Frenn, K., Wewerka, S. S., & Van Ryzin, M. J. (2009). Moderate versus severe early life stress: Associations with stress reactivity and regulation in 10-12-year-old children. Psychoneuroendocrinology, 34, 62–75. doi:10.1016/j.psyneuen.2008.08.013Google Scholar
Gunnar, M. R., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Reviews of Psychology, 58, 145–173. doi:10.1146/annurev.psych.58.110405.085605Google Scholar
Hadwin, J. A., & Richards, H. J. (2016). Working memory training and CBT reduces anxiety symptoms and attentional biases to threat: A preliminary study. Frontiers in Psychology, 7, 47. doi:10.3389/fpsyg.2016.00047Google Scholar
Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., … Davidson, R. J. (2015). Behavioral problems after early life stress: Contributions of the hippocampus and amygdala. Biological Psychiatry, 77, 314–323. doi:10.1016/j.biopsych.2014.04.020Google Scholar
Hayes, A. F. (2018). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach (2nd ed.). New York: Guilford Press.Google Scholar
Hostinar, C. E., Stellern, S. A., Schaefer, C., Carlson, S. M., & Gunnar, M. R. (2012). Associations between early life adversity and executive function in children adopted internationally from orphanages. Procedings of the National Academy of Sciences of the USA, 109, 17208–17212. doi:1121246109Google Scholar
Humphrey, T. (1968). The development of the human amygdala during early embryonic life. Journal of Comparative Neurology, 132, 135–165.Google Scholar
Humphreys, K. L., Gabard-Durnam, L., Goff, B., Telzer, E. H., Flannery, J., Gee, D. G., … Tottenham, N. (in press). Friendship and social functioning following early institutional rearing: The role of ADHD symptoms. Development and Psychopathology. doi:10.1017/S0954579418001050Google Scholar
Humphreys, K. L., Gleason, M. M., Drury, S. S., Miron, D., Nelson, C. A. III, Fox, N. A., & Zeanah, C. H. (2015). Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: Follow-up of an open, randomised controlled trial. Lancet Psychiatry, 2, 625–634. doi:10.1016/S2215-0366(15)00095-4Google Scholar
Jay, T. M., Rocher, C., Hotte, M., Naudon, L., Gurden, H., & Spedding, M. (2004). Plasticity at hippocampal to prefrontal cortex synapses is impaired by loss of dopamine and stress: Importance for psychiatric diseases. Neurotoxicity Research, 6, 233–244.Google Scholar
Kim, J., Delcasso, S., & Lee, I. (2011). Neural correlates of object-in-place learning in hippocampus and prefrontal cortex. Journal of Neuroscience, 31, 16991–17006. doi:10.1523/JNEUROSCI.2859-11.2011Google Scholar
Kirschbaum, C., & Hellhammer, D. H. (2000). Salivary cortisol. Encyclopedia of Stress, 3, 379–383.Google Scholar
Koss, K. J., Hostinar, C. E., Donzella, B., & Gunnar, M. R. (2014). Social deprivation and the HPA axis in early development. Psychoneuroendocrinology, 50, 1–13. doi:10.1016/j.psyneuen.2014.07.028Google Scholar
Koss, K. J., Mliner, S. B., Donzella, B., & Gunnar, M. R. (2016). Early adversity, hypocortisolism, and behavior problems at school entry: A study of internationally adopted children. Psychoneuroendocrinology, 66, 31–38. doi:10.1016/j.psyneuen.2015.12.018Google Scholar
Kwon, H., Reiss, A. L., & Menon, V. (2002). Neural basis of protracted developmental changes in visuo-spatial working memory. Procedings of the National Academy of Sciences of the USA, 99, 13336–13341. doi:10.1073/pnas.162486399Google 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.xGoogle Scholar
Loman, M. M., Wiik, K. L., Frenn, K. A., Pollak, S. D., & Gunnar, M. R. (2009). Postinstitutionalized children's development: Growth, cognitive, and language outcomes. Journal of Developmental and Behavioral Pediatrics, 30, 426–434. doi:10.1097/DBP.0b013e3181b1fd08Google Scholar
Lupien, S. J., & Lepage, M. (2001). Stress, memory, and the hippocampus: Can't live with it, can't live without it. Behavioral Brain Research, 127, 137–158.Google Scholar
Maheu, F. S., Dozier, M., Guyer, A. E., Mandell, D., Peloso, E., Poeth, K., … Ernst, M. (2010). A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cognitive, Affective, & Behavioral Neuroscience, 10, 34–49. doi:10.3758/CABN.10.1.34Google Scholar
Maldonado, E. F., Fernandez, F. J., Trianes, M. V., Wesnes, K., Petrini, O., Zangara, A., … Ambrosetti, L. (2008). Cognitive performance and morning levels of salivary cortisol and alpha-amylase in children reporting high vs. low daily stress perception. Spanish Journal of Psychology, 11, 3–15.Google Scholar
Martel, M. M., Nigg, J. T., Wong, M. M., Fitzgerald, H. E., Jester, J. M., Puttler, L. I., … Zucker, R. A. (2007). Childhood and adolescent resiliency, regulation, and executive functioning in relation to adolescent problems and competence in a high-risk sample. Development and Psychopathology, 19, 541–563. doi:10.1017/S0954579407070265Google Scholar
Masten, A. S., & Barnes, A. J. (2018). Resilience in children: Developmental perspectives. Children, 5, 98. doi:10.3390/children5070098Google Scholar
Masten, A. S., Best, K. M., & Garmezy, N. (1990). Resilience and development: Contributions from the study of children who overcome adversity. Development and Psychopathology, 2, 425–444.Google Scholar
Masten, A. S., & Tellegen, A. (2012). Resilience in developmental psychopathology: Contributions of the Project Competence Longitudinal Study. Development and Psychopathology, 24, 345–361. doi:10.1017/S095457941200003XGoogle Scholar
McLaughlin, K. A., Sheridan, M. A., & Nelson, C. A. (2017). Neglect as a violation of species-expectant experience: Neurodevelopmental consequences. Biological Psychiatry, 82, 462–471. doi:10.1016/j.biopsych.2017.02.1096Google Scholar
McLaughlin, K. A., Sheridan, M. A., Tibu, F., Fox, N. A., Zeanah, C. H., & Nelson, C. A. III. (2015). Causal effects of the early caregiving environment on development of stress response systems in children. Procedings of the National Academy of Sciences of the USA, 112, 5637–5642. doi:10.1073/pnas.1423363112Google Scholar
Mehta, M. A., Golembo, N. I., Nosarti, C., Colvert, E., Mota, A., Williams, S. C., … Sonuga-Barke, E. J. (2009). Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian Adoptees study pilot. Journal of Child Psychology & Psychiatry, 50, 943–951. doi:10.1111/j.1469-7610.2009.02084.xGoogle Scholar
Merz, E. C., & McCall, R. B. (2010). Behavior problems in children adopted from psychosocially depriving institutions. Journal of Abnormal Child Psychology, 38, 459–470. doi:10.1007/s10802-009-9383-4Google Scholar
Merz, E. C., McCal, R. B., Wright, A. J., & Luna, B. (2013). Inhibitory control and working memory in post-institutionalized children. Journal of abnormal child psychology, 41(6), 879–890.Google Scholar
Mitchell, D. G. V., Nakic, M., Fridberg, D., Kamel, N., Pine, D. S., & Blair, R. J. R. (2007). The impact of processing load on emotion. NeuroImage, 34, 1299–1309. doi:10.1016/j.neuroimage.2006.10.012Google Scholar
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. E. (2002). Rethinking feelings: An FMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 1215–1229. doi:10.1162/089892902760807212Google Scholar
O'Connor, T. G., Rutter, M., Beckett, C., Keaveney, L., & Kreppner, J. M. (2000). The effects of global severe privation on cognitive competence: Extension and longitudinal follow-up. English and Romanian Adoptees Study Team. Child Development, 71, 376–390.Google Scholar
O'Donovan, A., Hughes, B. M., Slavich, G. M., Lynch, L., Cronin, M. T., O'Farrelly, C., & Malone, K. M. (2010). Clinical anxiety, cortisol and interleukin-6: Evidence for specificity in emotion-biology relationships. Brain, Behavior, and Immunity, 24, 1074–1077. doi:10.1016/j.bbi.2010.03.003Google Scholar
Oei, N. Y., Everaerd, W. T., Elzinga, B. M., van Well, S., & Bermond, B. (2006). Psychosocial stress impairs working memory at high loads: An association with cortisol levels and memory retrieval. Stress, 9, 133–141. doi:10.1080/10253890600965773Google Scholar
Payne, C., Machado, C. J., Bliwise, N. G., & Bachevalier, J. (2010). Maturation of the hippocampal formation and amygdala in Macaca mulatta: A volumetric magnetic resonance imaging study. Hippocampus, 20, 922–935. doi:10.1002/hipo.20688Google Scholar
Pine, D. S., & Cohen, J. A. (2002). Trauma in children and adolescents: Risk and treatment of psychiatric sequelae. Biological Psychiatry, 51, 519–531.Google Scholar
Quevedo, K., Johnson, A., Loman, M., Lafavor, T., & Gunnar, M. (2012). The confluence of adverse early experience and puberty on the cortisol awakening response. International Journal of Behavioral Development, 36, 19–28. doi:10.1177/0165025411406860Google Scholar
Quirk, G. J., & Beer, J. S. (2006). Prefrontal involvement in the regulation of emotion: Convergence of rat and human studies. Current Opinion in Neurobiology, 16, 723–727. doi:10.1016/j.conb.2006.07.004Google Scholar
Rapee, R. M., & Szollos, A. A. (2002). Developmental antecedents of clinical anxiety in childhood. Behavior Change, 19, 146–157.Google Scholar
Raver, C., McCoy, D. C., Lowenstein, A. E., & Pess, R. (2013). Predicting individual differences in low-income children's executive control from early to middle childhood. Developmental Science, 16, 394–408. doi:10.1111/desc.12027Google Scholar
Roozendaal, B. (2002). Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory, 78, 578–595.Google Scholar
Rutter, M. (1998). Developmental catch-up, and deficit, following adoption after severe global early privation. English and Romanian Adoptees (ERA) Study Team. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39, 465–476.Google Scholar
Rutter, M., Beckett, C., Castle, J., Colvert, E., Kreppner, J., Mehta, M., … Sonuga-Barke, E. (2007). Effects of profound early institutional deprivation: An overview of findings from a UK longitudinal study of Romanian adoptees. European Journal of Developmental Psychology, 4, 332–350.Google Scholar
Sari, B. A., Koster, E. H., Pourtois, G., & Derakshan, N. (2016). Training working memory to improve attentional control in anxiety: A proof-of-principle study using behavioral and electrophysiological measures. Biological Psychology, 121(Pt. B), 203–212. doi:10.1016/j.biopsycho.2015.09.008Google Scholar
Schmeichel, B. J., & Demaree, H. A. (2010). Working memory capacity and spontaneous emotion regulation: High capacity predicts self-enhancement in response to negative feedback. Emotion, 10, 739–744. doi:10.1037/a0019355Google Scholar
Schmeichel, B. J., Volokhov, R. N., & Demaree, H. A. (2008). Working memory capacity and the self-regulation of emotional expression and experience. Journal of Personality and Social Psychology, 95, 1526–1540. doi:10.1037/a0013345Google Scholar
Silvers, J. A., Goff, B., Gabard-Durnam, L. J., Gee, D. G., Fareri, D. S., Caldera, C., & Tottenham, N. (2017). Vigilance, the amygdala, and anxiety in youths with a history of institutional care. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2, 493–501. doi:10.1016/j.bpsc.2017.03.016Google Scholar
Silvers, J. A., Lumian, D. S., Gabard-Durnam, L., Gee, D. G., Goff, B., Fareri, D. S., … Tottenham, N. (2016). Previous institutionalization is followed by broader amygdala-hippocampal-PFC network connectivity during aversive learning in human development. Journal of Neuroscience, 36, 6420–6430. doi:10.1523/JNEUROSCI.0038-16.2016Google Scholar
Smyke, A. T., Koga, S. F., Johnson, D. E., Fox, N. A., Marshall, P. J., Nelson, C. A., & Zeanah, C. H. (2007). The caregiving context in institution-reared and family-reared infants and toddlers in Romania. Journal of Child Psychology and Psychiatry, 48, 210–218. doi:10.1111/j.1469-7610.2006.01694.xGoogle Scholar
Tibu, F., Sheridan, M. A., McLaughlin, K. A., Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2016). Disruptions of working memory and inhibition mediate the association between exposure to institutionalization and symptoms of attention deficit hyperactivity disorder. Psychological Medicine, 46, 529–541. doi:10.1017/S0033291715002020Google Scholar
Tottenham, N. (2012a). Human amygdala development in the absence of species-expected caregiving. Developmental Psychobiology, 54, 598–611. doi:10.1002/dev.20531Google Scholar
Tottenham, N. (2012b). Risk and developmental heterogeneity in previously institutionalized children. Journal of Adolescent Health, 51(2, Suppl.), S29–S33. doi:10.1016/j.jadohealth.2012.04.004Google Scholar
Tottenham, N., & Gabard-Durnam, L. J. (2017). The developing amygdala: A student of the world and a teacher of the cortex. Current Opinion in Psychology, 17, 55–60. doi:10.1016/j.copsyc.2017.06.012Google Scholar
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.Google Scholar
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T., Nurse, M., Gilhooly, T., … Casey, B. J. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and emotion regulation difficulties. Developmental Science, 13, 46–61.Google Scholar
Ulfig, N., Setzer, M., & Bohl, J. (2003). Ontogeny of the human amygdala. Annals of the New York Academy of Sciences, 985, 22–33.Google Scholar
Vantieghem, M. R., Gabard-Durnam, L., Goff, B., Flannery, J., Humphreys, K. L., Telzer, E. H., … Tottenham, N. (2017). Positive valence bias and parent-child relationship security moderate the association between early institutional caregiving and internalizing symptoms. Development and Psychopathology, 29, 519–533. doi:10.1017/S0954579417000153Google Scholar
von Allmen, D. Y., Wurmitzer, K., & Klaver, P. (2014). Hippocampal and posterior parietal contributions to developmental increases in visual short-term memory capacity. Cortex, 59, 95–102. doi:10.1016/j.cortex.2014.07.010Google Scholar
Vreeburg, S. A., Zitman, F. G., van Pelt, J., Derijk, R. H., Verhagen, J. C., van Dyck, R., … Penninx, B. W. (2010). Salivary cortisol levels in persons with and without different anxiety disorders. Psychosomatic Medicine, 72, 340–347. doi:10.1097/PSY.0b013e3181d2f0c8Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: The Psychological Corporation.Google Scholar
Wren, F. J., Berg, E. A., Heiden, L. A., Kinnamon, C. J., Ohlson, L. A., Bridge, J. A., … Bernal, M. P. (2007). Childhood anxiety in a diverse primary care population: Parent-child reports, ethnicity and SCARED factor structure. Journal of the American Academy of Child & Adolescent Psychiatry, 46, 332–340. doi:10.1097/chi.0b013e31802f1267Google Scholar