Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-05T08:45:12.031Z Has data issue: false hasContentIssue false

Developmental relations between amygdala volume and anxiety traits: Effects of informant, sex, and age

Published online by Cambridge University Press:  21 November 2017

Katherine Rice Warnell*
Affiliation:
Texas State University
Meredith Pecukonis
Affiliation:
University of Maryland
Elizabeth Redcay
Affiliation:
University of Maryland
*
Address correspondence and reprint requests to: Katherine Rice Warnell, Department of Psychology, Texas State University, San Marcos, TX 78666; E-mail: [email protected].

Abstract

Although substantial human and animal evidence suggests a role for the amygdala in anxiety, literature linking amygdala volume to anxiety symptomatology is inconclusive, with studies finding positive, negative, and null results. Clarifying this brain–behavior relation in middle to late childhood is especially important, as this is a time both of amygdala structural maturation and the emergence of many anxiety disorders. The goal of the current study was to clarify inconsistent findings in previous literature by identifying factors moderating the relation between amygdala volume and anxiety traits in a large sample of typically developing children aged 6–13 years (N = 72). In particular, we investigated the moderating effects of informant (parent vs. child), age, and sex. We found that children's reports (i.e., self-reports) were related to amygdala volume; children who reported higher anxiety levels had smaller amygdalae. This negative relation between amygdala volume and anxiety weakened with age. There was also an independent effect of sex, such that relations were stronger in males than in females. These results indicate the importance of considering sample and informant characteristics when charting the neurobiological mechanisms underlying developmental anxiety.

Type
Regular Articles
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 Laura Anderson Kirby, Dan Levitas, Dustin Moraczewski, Jazlyn Nketia, Harrison Pierce, Eleonora Sadikova, and Kayla Velnoskey for assistance with data collection and analysis and the Maryland Neuroimaging Center and staff for project assistance.

References

Albaugh, M. D., Nguyen, T., Ducharme, S., Collins, D. L., Botteron, K. N., D'Alberto, N., … Hudziak, J. J. (2017). Age-related volumetric change of limbic structures and subclinical anxious/depressed symptomatology in typically developing children and adolescents. Biological Psychology, 124, 133140. doi:10.1016/j.biopsycho.2017.02.002Google Scholar
Bangasser, D. A., & Valentino, R. J. (2014). Sex differences in stress-related psychiatric disorders: Neurobiological perspectives. Frontiers in Neuroendocrinology, 35, 303319. doi:10.1016/j.yfrne.2014.03.008Google Scholar
Bauer, D. J., & Curran, P. J. (2005). Probing interactions in fixed and multilevel regression: Inferential and graphical techniques. Multivariate Behavioral Research, 40, 373400. doi:10.1207/s15327906mbr4003_5Google Scholar
Baur, V., Hänggi, J., & Jäncke, L. (2012). Volumetric associations between uncinate fasciculus, amygdala, and trait anxiety. BMC Neuroscience, 13, 4. doi:10.1186/1471-2202-13-4Google Scholar
Becker, E. M., Jensen-Doss, A., Kendall, P. C., Birmaher, B., & Ginsburg, G. S. (2016). All anxiety is not created equal: Correlates of parent/youth agreement vary across subtypes of anxiety. Journal of Psychopathology and Behavioral Assessment, 38, 528537. doi:10.1007/s10862-016-9544-zGoogle Scholar
Beesdo, K., Knappe, S., & Pine, D. S. (2009). Anxiety and anxiety disorders in children and adolescents: Developmental issues and implications for DSM-V. Psychiatric Clinics of North America, 32, 483524. doi:10.1016/j.psc.2009.06.002Google Scholar
Bell-Dolan, D. J., Last, C. G., & Strauss, C. C. (1990). Symptoms of anxiety disorders in normal children. Journal of the American Academy of Child & Adolescent Psychiatry, 29, 759765. doi:10.1097/00004583-199009000-00014Google 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, 12301236. doi:10.1097/00004583-199910000-00011Google Scholar
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. (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, 545553. doi:10.1097/00004583-199704000-00018Google Scholar
Bishop, S. J., Duncan, J., & Lawrence, A. D. (2004). State anxiety modulation of the amygdala response to unattended threat-related stimuli. Journal of Neuroscience, 24, 1036410368. doi:10.1523/jneurosci.2550-04.2004Google Scholar
Bitsika, V., Sharpley, C. F., Andronicos, N. M., & Agnew, L. L. (2015). Agreement between self-vs parent-ratings of general anxiety disorder symptoms and salivary cortisol in boys with an ASD. Journal of Developmental and Physical Disabilities, 27, 467477. doi:10.1007/s10882-015-9431-7Google Scholar
Blair, K., Shaywitz, J., Smith, B. W., Rhodes, R., Geraci, M., Jones, M., … Jacobs, M. (2008). Response to emotional expressions in generalized social phobia and generalized anxiety disorder: Evidence for separate disorders. American Journal of Psychiatry, 165, 11931202. doi:10.1176/appi.ajp.2008.07071060Google Scholar
Blakeley-Smith, A., Reaven, J., Ridge, K., & Hepburn, S. (2012). Parent–child agreement of anxiety symptoms in youth with autism spectrum disorders. Research in Autism Spectrum Disorders, 6, 707716. doi:10.1016/j.rasd.2011.07.020Google Scholar
Blakemore, S. J., Burnett, S., & Dahl, R. E. (2010). The role of puberty in the developing adolescent brain. Human Brain Mapping, 31, 926933. doi:10.1002/hbm.21052Google Scholar
Bramen, J. E., Hranilovich, J. A., Dahl, R. E., Forbes, E. E., Chen, J., Toga, A. W., … Sowell, E. R. (2011). Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cerebral Cortex, 21, 636646. doi:10.1093/cercor/bhq137Google Scholar
Burgund, E. D., Kang, H. C., Kelly, J. E., Buckner, R. L., Snyder, A. Z., Petersen, S. E., & Schlaggar, B. L. (2002). The feasibility of a common stereotactic space for children and adults in fMRI studies of development. NeuroImage, 17, 184200. doi:10.1006/nimg.2002.1174Google Scholar
Comer, J. S., & Kendall, P. C. (2004). A symptom-level examination of parent–child agreement in the diagnosis of anxious youths. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 878886. doi:10.1097/01.chi.0000125092.35109.c5Google Scholar
Cosi, S., Canals, J., Hernández-Martinez, C., & Vigil-Colet, A. (2010). Parent–child agreement in SCARED and its relationship to anxiety symptoms. Journal of Anxiety Disorders, 24, 129133. doi:10.1016/j.janxdis.2009.09.008Google Scholar
De Bellis, M. D., Casey, B. J., Dahl, R. E., Birmaher, B., Williamson, D. E., Thomas, K. M., … Ryan, N. D. (2000). A pilot study of amygdala volumes in pediatric generalized anxiety disorder. Biological Psychiatry, 48, 5157. doi:10.1016/S0006-3223(00)00835-0Google Scholar
De Los Reyes, A., & Kazdin, A. E. (2005). Informant discrepancies in the assessment of childhood psychopathology: A critical review, theoretical framework, and recommendations for further study. Psychological Bulletin, 131, 483. doi:10.1037/0033-2909.131.4.483Google Scholar
Dennis, E. L., Gotlib, I. H., Thompson, P. M., & Thomason, M. E. (2011). Anxiety modulates insula recruitment in resting-state functional magnetic resonance imaging in youth and adults. Brain Connectivity, 1, 245254. doi:10.1089/brain.2011.0030Google Scholar
Derntl, B., Windischberger, C., Robinson, S., Kryspin-Exner, I., Gur, R. C., Moser, E., & Habel, U. (2009). Amygdala activity to fear and anger in healthy young males is associated with testosterone. Psychoneuroendocrinology, 34, 687693. doi:10.1016/j.psyneuen.2008.11.007Google Scholar
Dickie, E. W., & Armony, J. L. (2008). Amygdala responses to unattended fearful faces: Interaction between sex and trait anxiety. Psychiatry Research: Neuroimaging, 162, 5157. doi:10.1016/j.pscychresns.2007.08.002Google Scholar
Dirks, M. A., De Los Reyes, A., Briggs-Gowan, M., Cella, D., & Wakschlag, L. S. (2012). Annual Research Review: Embracing not erasing contextual variability in children's behavior—Theory and utility in the selection and use of methods and informants in developmental psychopathology. Journal of Child Psychology and Psychiatry, 53, 558574. doi:10.1111/j.1469-7610.2012.02537.xGoogle Scholar
Dirks, M. A., Weersing, V. R., Warnick, E., Gonzalez, A., Alton, M., Dauser, C., … Woolston, J. (2014). Parent and youth report of youth anxiety: Evidence for measurement invariance. Journal of Child Psychology and Psychiatry, 55, 284291. doi:10.1111/jcpp.12159Google Scholar
Engel, N. A., Rodrigue, J. R., & Geffken, G. R. (1994). Parent-child agreement on ratings of anxiety in children. Psychological Reports, 75, 12511260. doi:10.2466/pr0.1994.75.3.1251Google Scholar
Etkin, A., Klemenhagen, K. C., Dudman, J. T., Rogan, M. T., Hen, R., Kandel, E. R., & Hirsch, J. (2004). Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron, 44, 10431055. doi:10.1016/j.neuron.2004.12.006Google Scholar
Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164, 14761488. doi:10.1176/appi.ajp.2007.07030504Google Scholar
Fisler, M. S., Federspiel, A., Horn, H., Dierks, T., Schmitt, W., Wiest, R., … Soravia, L. M. (2013). Spider phobia is associated with decreased left amygdala volume: A cross-sectional study. BMC Psychiatry, 13, 70. doi:10.1186/1471-244X-13-70Google Scholar
Frick, P. J., Silverthorn, P., & Evans, C. (1994). Assessment of childhood anxiety using structured interviews: Patterns of agreement among informants and association with maternal anxiety. Psychological Assessment, 6, 372. doi:10.1037/1040-3590.6.4.372Google Scholar
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., & Abbamonte, M. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34, 418432.Google Scholar
Gabard-Durnam, L. J., Flannery, J., Goff, B., Gee, D. G., Humphreys, K. L., Telzer, E., … Tottenham, N. (2014). The development of human amygdala functional connectivity at rest from 4 to 23 years: A cross-sectional study. NeuroImage, 95, 193207. doi:10.1016/j.neuroimage.2014.03.038Google Scholar
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, 45844593. doi:10.1523/jneurosci.3446-12.2013Google Scholar
Ghosh, S. S., Kakunoori, S., Augustinack, J., Nieto-Castanon, A., Kovelman, I., Gaab, N., … Fischl, B. (2010). Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11years of age. NeuroImage, 53, 8593. doi:10.1016/j.neuroimage.2010.05.075Google Scholar
Grupe, D. W., & Nitschke, J. B. (2013). Uncertainty and anticipation in anxiety: An integrated neurobiological and psychological perspective. Nature Reviews Neuroscience, 14, 488501. doi:10.1038/nrn3524Google Scholar
Hahn, A., Stein, P., Windischberger, C., Weissenbacher, A., Spindelegger, C., Moser, E., … Lanzenberger, R. (2011). Reduced resting-state functional connectivity between amygdala and orbitofrontal cortex in social anxiety disorder. NeuroImage, 56, 881889. doi:10.1016/j.neuroimage.2011.02.064Google Scholar
Hamann, S. (2005). Sex differences in the responses of the human amygdala. Neuroscientist, 11, 288293. doi:10.1177/1073858404271981Google Scholar
Hayano, F., Nakamura, M., Asami, T., Uehara, K., Yoshida, T., Roppongi, T., … Hirayasu, Y. (2009). Smaller amygdala is associated with anxiety in patients with panic disorder. Psychiatry and Clinical Neurosciences, 63, 266276. doi:10.1111/j.1440-1819.2009.01960.xGoogle Scholar
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.Google Scholar
Hilbert, K., Lueken, U., Muehlhan, M., & Beesdo-Baum, K. (2017). Separating generalized anxiety disorder from major depression using clinical, hormonal, and structural MRI data: A multimodal machine learning study. Brain and Behavior. Advance online publication. doi:10.1002/brb3.633Google Scholar
Hilbert, K., Pine, D. S., Muehlhan, M., Lueken, U., Steudte-Schmiedgen, S., & Beesdo-Baum, K. (2015). Gray and white matter volume abnormalities in generalized anxiety disorder by categorical and dimensional characterization. Psychiatry Research: Neuroimaging, 234, 314320. doi:10.1016/j.pscychresns.2015.10.009Google Scholar
Hölzel, B. K., Carmody, J., Evans, K. C., Hoge, E. A., Dusek, J. A., Morgan, L., … Lazar, S. W. (2009). Stress reduction correlates with structural changes in the amygdala. Social Cognitive and Affective Neuroscience, 5, 1117. doi:10.1093/scan/nsp034Google Scholar
Hu, S., Pruessner, J. C., Coupé, P., & Collins, D. L. (2013). Volumetric analysis of medial temporal lobe structures in brain development from childhood to adolescence. NeuroImage, 74, 276287. doi:10.1016/j.neuroimage.2013.02.032Google Scholar
Hyde, L. W., Gorka, A., Manuck, S. B., & Hariri, A. R. (2011). Perceived social support moderates the link between threat-related amygdala reactivity and trait anxiety. Neuropsychologia, 49, 651656. doi:10.1016/j.neuropsychologia.2010.08.025Google Scholar
Job, D. E., Dickie, D. A., Rodriguez, D., Robson, A., Danso, S., Pernet, C., … Waiter, G. D. (2017). A brain imaging repository of normal structural MRI across the life course: Brain Images of Normal Subjects (BRAINS). NeuroImage, 144, 299304. doi:10.1016/j.neuroimage.2016.01.027Google Scholar
Kaczkurkin, A. N., Moore, T. M., Ruparel, K., Ciric, R., Calkins, M. E., Shinohara, R. T., … Gennatas, E. D. (2016). Elevated amygdala perfusion mediates developmental sex differences in trait anxiety. Biological Psychiatry, 80, 775785. doi:10.1016/j.biopsych.2016.04.021Google Scholar
Kalmar, J. H., Wang, F., Chepenik, L. G., Womer, F. Y., Jones, M. M., Pittman, B., … Blumberg, H. P. (2009). Relation between amygdala structure and function in adolescents with bipolar disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 636642. doi:10.1097/CHI.0b013e31819f6fbcGoogle Scholar
Kaufman, A. S., & Kaufman, N. L. (2004). Kaufman Brief Intelligence Test (2nd ed.). Bloomington, MN: Pearson.Google Scholar
Kessel, E. M., Kujawa, A., Hajcak Proudfit, G., & Klein, D. N. (2015). Neural reactivity to monetary rewards and losses differentiates social from generalized anxiety in children. Journal of Child Psychology and Psychiatry, 56, 792800. doi:10.1111/jcpp.12355Google Scholar
Kessler, R. C., Angermeyer, M., Anthony, J. C., De Graaf, R. O. N., Demyttenaere, K., Gasquet, I., … Kawakami, N. (2007). Lifetime prevalence and age-of-onset distributions of mental disorders in the World Health Organization's World Mental Health Survey Initiative. World Psychiatry, 6, 168176.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, 593602. doi:10.1001/archpsyc.62.6.593Google Scholar
Kim, M. J., Gee, D. G., Loucks, R. A., Davis, F. C., & Whalen, P. J. (2011). Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cerebral Cortex, 21, 16671673. doi:10.1093/cercor/bhq237Google Scholar
Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011). The structural and functional connectivity of the amygdala: From normal emotion to pathological anxiety. Behavioural Brain Research, 223, 403410. doi:10.1016/j.bbr.2011.04.025Google Scholar
Kircanski, K., Zhang, S., Stringaris, A., Wiggins, J. L., Towbin, K. E., Pine, D. S., … Brotman, M. A. (2017). Empirically derived patterns of psychiatric symptoms in youth: A latent profile analysis. Journal of Affective Disorders, 216, 109116. doi:10.1016/j.jad.2016.09.016Google Scholar
Lagattuta, K. H., Sayfan, L., & Bamford, C. (2012). Do you know how I feel? Parents underestimate worry and overestimate optimism compared to child self-report. Journal of Experimental Child Psychology, 113, 211232. doi:10.1016/j.jecp.2012.04.001Google Scholar
Lewinsohn, P. M., Gotlib, I. H., Lewinsohn, M., Seeley, J. R., & Allen, N. B. (1998). Gender differences in anxiety disorders and anxiety symptoms in adolescents. Journal of Abnormal Psychology, 107, 109. doi:10.1037/0021-843X.107.1.109Google Scholar
Lyons-Ruth, K., Pechtel, P., Yoon, S. A., Anderson, C. M., & Teicher, M. H. (2016). Disorganized attachment in infancy predicts greater amygdala volume in adulthood. Behavioural Brain Research, 308, 8393. doi:10.1016/j.bbr.2016.03.050Google Scholar
Maeng, L. Y., & Milad, M. R. (2015). Sex differences in anxiety disorders: Interactions between fear, stress, and gonadal hormones. Hormones and Behavior, 76, 106117. doi:10.1016/j.yhbeh.2015.04.002Google Scholar
Martel, M. M., Markon, K., & Smith, G. T. (2017). Research Review: Multi-informant integration in child and adolescent psychopathology diagnosis. Journal of Child Psychology and Psychiatry, 58, 116128. doi:10.1111/jcpp.12611Google Scholar
McMenamin, B. W., & Marsolek, C. J. (2013). Can theories of visual representation help to explain asymmetries in amygdala function? Cognitive, Affective, & Behavioral Neuroscience, 13, 211224. doi:10.3758/s13415-012-0139-1Google Scholar
McQueeny, T., Padula, C. B., Price, J., Medina, K. L., Logan, P., & Tapert, S. F. (2011). Gender effects on amygdala morphometry in adolescent marijuana users. Behavioural Brain Research, 224, 128134. doi:10.1016/j.bbr.2011.05.031Google Scholar
Milham, M. P., Nugent, A. C., Drevets, W. C., Dickstein, D. S., Leibenluft, E., Ernst, M., … Pine, D. S. (2005). Selective reduction in amygdala volume in pediatric anxiety disorders: A voxel-based morphometry investigation. Biological Psychiatry, 57, 961966. doi:10.1016/j.biopsych.2005.01.038Google Scholar
Montag, C., Weber, B., Fliessbach, K., Elger, C., & Reuter, M. (2009). The BDNF Val66Met polymorphism impacts parahippocampal and amygdala volume in healthy humans: Incremental support for a genetic risk factor for depression. Psychological Medicine, 39, 18311839. doi:10.1017/S0033291709005509Google Scholar
Morey, R. A., Petty, C. M., Xu, Y., Hayes, J. P., Wagner, H. R., Lewis, D. V., … McCarthy, G. (2009). A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. NeuroImage, 45, 855866. doi:10.1016/j.neuroimage.2008.12.033Google Scholar
Mueller, S. C., Aouidad, A., Gorodetsky, E., Goldman, D., Pine, D. S., & Ernst, M. (2013). Gray matter volume in adolescent anxiety: An impact of the brain-derived neurotrophic factor val 66 met polymorphism? Journal of the American Academy of Child & Adolescent Psychiatry, 52, 184195. doi:10.1016/j.jaac.2012.11.016Google Scholar
Muris, P., Merckelbach, H., Van Brakel, A., & Mayer, A. B. (1999). The revised version of the Screen for Child Anxiety Related Emotional Disorders (SCARED-R): Further evidence for its reliability and validity. Anxiety, Stress & Coping, 12, 411425. doi:10.1080/10615809908249319Google Scholar
Pereira, A. I., Muris, P., Barros, L., Goes, R., Marques, T., & Russo, V. (2015). Agreement and discrepancy between mother and child in the evaluation of children's anxiety symptoms and anxiety life interference. European Child & Adolescent Psychiatry, 24, 327337. doi:10.1007/s00787-014-0583-2Google Scholar
Phares, V., & Danforth, J. S. (1994). Adolescents’, parents’, and teachers’ distress over adolescents’ behavior. Journal of Abnormal Child Psychology, 22, 721732. doi:10.1007/BF02171998Google Scholar
Preacher, K. J., Curran, P. J., & Bauer, D. J. (2006). Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31, 437448. doi:10.3102/10769986031004437Google Scholar
Qin, S., Young, C. B., Duan, X., Chen, T., Supekar, K., & Menon, V. (2014). Amygdala subregional structure and intrinsic functional connectivity predicts individual differences in anxiety during early childhood. Biological Psychiatry, 75, 892900. doi:10.1016/j.biopsych.2013.10.006Google Scholar
Rogers, M. A., Yamasue, H., Abe, O., Yamada, H., Ohtani, T., Iwanami, A., … Kasai, K. (2009). Smaller amygdala volume and reduced anterior cingulate gray matter density associated with history of post-traumatic stress disorder. Psychiatry Research: Neuroimaging, 174, 210216. doi:10.1016/j.pscychresns.2009.06.001Google Scholar
Salbach-Andrae, H., Klinkowski, N., Lenz, K., & Lehmkuhl, U. (2009). Agreement between youth-reported and parent-reported psychopathology in a referred sample. European Child & Adolescent Psychiatry, 18, 136143. doi:10.1007/s00787-008-0710-zGoogle Scholar
Saygin, Z. M., Osher, D. E., Augustinack, J., Fischl, B., & Gabrieli, J. D. (2011). Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography. NeuroImage, 56, 13531361. doi:10.1016/j.neuroimage.2011.03.006Google Scholar
Scaini, S., Ogliari, A., De Carolis, L., Bellodi, L., Di Serio, C., & Brombin, C. (2017). Evaluation of mother-child agreement and factorial structures of the SCARED questionnaire in an Italian clinical sample. Frontiers in Psychology, 8, 242. doi:10.3389/fpsyg.2017.00242Google Scholar
Schienle, A., Ebner, F., & Schäfer, A. (2011). Localized gray matter volume abnormalities in generalized anxiety disorder. European Archives of Psychiatry and Clinical Neuroscience, 261, 303307. doi:10.1007/s00406-010-0147-5Google Scholar
Schoemaker, D., Buss, C., Head, K., Sandman, C. A., Davis, E. P., Chakravarty, M. M., … Pruessner, J. C. (2016). Hippocampus and amygdala volumes from magnetic resonance images in children: Assessing accuracy of FreeSurfer and FSL against manual segmentation. NeuroImage, 129, 114. doi:10.1016/j.neuroimage.2016.01.038Google Scholar
Sehlmeyer, C., Dannlowski, U., Schöning, S., Kugel, H., Pyka, M., Pfleiderer, B., … Konrad, C. (2011). Neural correlates of trait anxiety in fear extinction. Psychological Medicine, 41, 789798. doi:10.1017/S0033291710001248Google Scholar
Sergerie, K., Chochol, C., & Armony, J. L. (2008). The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies. Neuroscience & Biobehavioral Reviews, 32, 811830. doi:10.1016/j.neubiorev.2007.12.002Google Scholar
Shin, L. M., & Liberzon, I. (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology, 35, 169191. doi:10.1038/npp.2009.83Google Scholar
Siegle, G. J., Konecky, R. O., Thase, M. E., & Carter, C. S. (2003). Relationships between amygdala volume and activity during emotional information processing tasks in depressed and never-depressed individuals. Annals of the New York Academy of Sciences, 985, 481484. doi:10.1111/j.1749-6632.2003.tb07105.xGoogle Scholar
Sisk, C. L., & Zehr, J. L. (2005). Pubertal hormones organize the adolescent brain and behavior. Frontiers in Neuroendocrinology, 26, 163174. doi:10.1016/j.yfrne.2005.10.003Google Scholar
Spampinato, M. V., Wood, J. N., De Simone, V., & Grafman, J. (2009). Neural correlates of anxiety in healthy volunteers: A voxel-based morphometry study. Journal of Neuropsychiatry and Clinical Neurosciences, 21, 199205. doi:10.1176/jnp.2009.21.2.199Google Scholar
Sripada, R. K., Wang, X., Sripada, C. S., & Liberzon, I. (2012). Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. Journal of Psychiatry and Neuroscience, 37, 241. doi:10.1503/jpn.110069Google Scholar
Strawn, J. R., Hamm, L., Fitzgerald, D. A., Fitzgerald, K. D., Monk, C. S., & Phan, K. L. (2015). Neurostructural abnormalities in pediatric anxiety disorders. Journal of Anxiety Disorders, 32, 8188. doi:10.1016/j.janxdis.2015.03.004Google Scholar
Su, L., Wang, K., Fan, F., Su, Y., & Gao, X. (2008). Reliability and validity of the Screen for Child Anxiety Related Emotional Disorders (SCARED) in Chinese children. Journal of Anxiety Disorders, 22, 612621. doi:10.1016/j.janxdis.2007.05.011Google Scholar
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., … Thomas, K. M. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13, 4661. doi:10.1111/j.1467-7687.2009.00852.xGoogle Scholar
Tovote, P., Fadok, J. P., & Lüthi, A. (2015). Neuronal circuits for fear and anxiety. Nature Reviews Neuroscience, 6, 317331. doi:10.1038/nrn3945Google Scholar
Uematsu, A., Matsui, M., Tanaka, C., Takahashi, T., Noguchi, K., Suzuki, M., & Nishijo, H. (2012). Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLOS ONE, 7, e46970. doi:10.1371/journal.pone.0046970Google Scholar
van der Plas, E. A., Boes, A. D., Wemmie, J. A., Tranel, D., & Nopoulos, P. (2010). Amygdala volume correlates positively with fearfulness in normal healthy girls. Social Cognitive and Affective Neuroscience, 5, 424431. doi:10.1093/scan/nsq009Google Scholar
Van Petten, C. (2004). Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: Review and meta-analysis. Neuropsychologia, 42, 13941413. doi:j.neuropsychologia.2004.04.006Google Scholar
van Wingen, G. A., Zylicz, S. A., Pieters, S., Mattern, C., Verkes, R. J., Buitelaar, J. K., & Fernández, G. (2009). Testosterone increases amygdala reactivity in middle-aged women to a young adulthood level. Neuropsychopharmacology, 34, 539547. doi:10.1038/npp.2008.2Google Scholar
Weems, C. F., Klabunde, M., Russell, J. D., Reiss, A. L., & Carrión, V. G. (2015). Post-traumatic stress and age variation in amygdala volumes among youth exposed to trauma. Social Cognitive and Affective Neuroscience, 10, 16611667. doi:10.1093/scan/nsv053Google Scholar
Weitkamp, K., Romer, G., Rosenthal, S., Wiegand-Grefe, S., & Daniels, J. (2010). German Screen for Child Anxiety Related Emotional Disorders (SCARED): Reliability, validity, and cross-informant agreement in a clinical sample. Child and Adolescent Psychiatry and Mental Health, 4, 19. doi:10.1186/1753-2000-4-19Google Scholar
Westenberg, P. M., Gullone, E., Bokhorst, C. L., Heyne, D. A., & King, N. J. (2007). Social evaluation fear in childhood and adolescence: Normative developmental course and continuity of individual differences. British Journal of Developmental Psychology, 25, 471483. doi:10.1348/026151006X173099Google Scholar
Wierenga, L. M., Langen, M., Oranje, B., & Durston, S. (2014). Unique developmental trajectories of cortical thickness and surface area. NeuroImage, 87, 120126. doi:10.1016/j.neuroimage.2013.11.010Google 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, 332340. doi:10.1097/chi.0b013e31802f1267Google Scholar
Wren, F. J., Bridge, J. A., & Birmaher, B. (2004). Screening for childhood anxiety symptoms in primary care: Integrating child and parent reports. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 13641371. doi:10.1097/01.chi.0000138350.60487.d3Google Scholar
Yang, R. J., Mozhui, K., Karlsson, R. M., Cameron, H. A., Williams, R. W., & Holmes, A. (2008). Variation in mouse basolateral amygdala volume is associated with differences in stress reactivity and fear learning. Neuropsychopharmacology, 33, 25952604. doi:10.1038/sj.npp.1301665Google Scholar