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Article

Exploring volumetric abnormalities in subcortical L-HPA axis structures in pediatric generalized anxiety disorder

Received 15 May 2023, Accepted 22 Mar 2024, Published online: 04 Apr 2024

References

  • Racine N, McArthur BA, Cooke JE, et al. Global prevalence of depressive and anxiety symptoms in children and adolescents during COVID-19: a meta-analysis. JAMA Pediatr. 2021;175(11):1142–1150. doi: 10.1001/jamapediatrics.2021.2482.
  • Tiirikainen K, Haravuori H, Ranta K, et al. Psychometric properties of the 7-item GEneralized Anxiety Disorder Scale (GAD-7) in a large representative sample of Finnish adolescents. Psychiatry Res. 2019;272:30–35. doi: 10.1016/j.psychres.2018.12.004.
  • Kessler RC, Berglund P, Demler O, et al. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005;62(6):593–602. doi: 10.1001/archpsyc.62.6.593.
  • Merikangas KR, He J, Burstein M, et al. Lifetime prevalence of mental disorders in U.S. adolescents: results from the National Comorbidity Survey Replication – Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry. 2010;49(10):980–989. doi: 10.1016/j.jaac.2010.05.017.
  • Pine DS, Cohen P, Gurley D, et al. The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Arch Gen Psychiatry. 1998;55(1):56–64. doi: 10.1001/archpsyc.55.1.56.
  • Foley DL, Goldston DB, Costello EJ, et al. Proximal psychiatric risk factors for suicidality in youth: the great smoky mountains study. Arch Gen Psychiatry. 2006;63(9):1017–1024. doi: 10.1001/archpsyc.63.9.1017.
  • Ramsawh HJ, Chavira DA. Association of childhood anxiety disorders and quality of life in a primary care sample. J Dev Behav Pediatr. 2016;37(4):269–276. doi: 10.1097/DBP.0000000000000296.
  • Sherbourne CD, Sullivan G, Craske MG, et al. Functioning and disability levels in primary care out-patients with one or more anxiety disorders. Psychol Med. 2010;40(12):2059–2068. doi: 10.1017/S0033291710000176.
  • Stein MB, Roy-Byrne PP, Craske MG, et al. Functional impact and health utility of anxiety disorders in primary care outpatients. Med Care. 2005;43(12):1164–1170. doi: 10.1097/01.mlr.0000185750.18119.fd.
  • Greenberg PE, Sisitsky T, Kessler RC, et al. The economic burden of anxiety disorders in the 1990s. J Clin Psychiatry. 1999;60(7):427–435. doi: 10.4088/JCP.v60n0702.
  • Egger HL, Costello JE, Angold A. School refusal and psychiatric disorders: a community study. J Am Acad Child Adolesc Psychiatry. 2003;42(7):797–807. doi: 10.1097/01.CHI.0000046865.56865.79.
  • Mazzone L, Ducci F, Scoto MC, et al. The role of anxiety symptoms in school performance in a community sample of children and adolescents. BMC Public Health. 2007;7(1):347. doi: 10.1186/1471-2458-7-347.
  • Maron E, Nutt D. Biological markers of generalized anxiety disorder. Dialogues Clin Neurosci. 2017;19(2):147–158. doi: 10.31887/DCNS.2017.19.2/dnutt.
  • Hilbert K, Lueken U, Beesdo-Baum K. Neural structures, functioning and connectivity in generalized anxiety disorder and interaction with neuroendocrine systems: a systematic review. J Affect Disord. 2014;158:114–126. doi: 10.1016/j.jad.2014.01.022.
  • Critchley HD, Mathias CJ, Dolan RJ. Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron. 2002;33(4):653–663. doi: 10.1016/s0896-6273(02)00588-3.
  • Roy AK, Fudge JL, Kelly C, et al. Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder. J Am Acad Child Adolesc Psychiatry. 2013;52(3):290–299.e2. doi: 10.1016/j.jaac.2012.12.010.
  • Shin LM, Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology. 2010;35(1):169–191. doi: 10.1038/npp.2009.83.
  • Stein MB, Simmons AN, Feinstein JS, et al. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry. 2007;164(2):318–327. doi: 10.1176/ajp.2007.164.2.318.
  • Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialog Clin Neurosci. 2006;8(4):383–395. doi: 10.31887/DCNS.2006.8.4/ssmith.
  • Ziegler DR, Cass WA, Herman JP. Excitatory influence of the locus coeruleus in hypothalamic‐pituitary‐adrenocortical axis responses to stress. J Neuroendocrinol. 1999;11(5):361–369. doi: 10.1046/j.1365-2826.1999.00337.x.
  • Sanford LD, Suchecki D, Meerlo P. Stress, arousal, and sleep. In: Meerlo P, Benca RM, Abel T, editors. Sleep, neuronal plasticity and brain function. Vol. 25. Berlin Heidelberg: Springer; 2014. p. 379–410.
  • Herman JP, Nawreen N, Smail MA, et al. Brain mechanisms of HPA axis regulation: neurocircuitry and feedback in context Richard Kvetnansky lecture. Stress. 2020;23(6):617–632. doi: 10.1080/10253890.2020.1859475.
  • Faravelli C, Sauro CL, Godini L, et al. Childhood stressful events, HPA axis and anxiety disorders. World J Psychiatry. 2012;2(1):13–25. doi: 10.5498/wjp.v2.i1.13.
  • Cole AB, Montgomery K, Bale TL, et al. What the hippocampus tells the HPA axis: hippocampal output attenuates acute stress responses via disynaptic inhibition of CRF + PVN neurons. Neurobiol Stress. 2022;20:100473. doi: 10.1016/j.ynstr.2022.100473.
  • Dedovic K, Duchesne A, Andrews J, et al. The brain and the stress axis: the neural correlates of cortisol regulation in response to stress. Neuroimage. 2009;47(3):864–871. doi: 10.1016/j.neuroimage.2009.05.074.
  • Kirouac GJ. The paraventricular nucleus of the thalamus as an integrating and relay node in the brain anxiety network. Front Behav Neurosci. 2021;15:627633. doi: 10.3389/fnbeh.2021.627633.
  • Lowry CA. Functional subsets of serotonergic neurones: implications for control of the hypothalamic-pituitary-adrenal axis: serotonergic systems and the HPA axis. J Neuroendocrinol. 2002;14(11):911–923. doi: 10.1046/j.1365-2826.2002.00861.x.
  • O’Mara S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. J Anat. 2005;207(3):271–282. doi: 10.1111/j.1469-7580.2005.00446.x.
  • De Bellis MD, Casey BJ, Dahl RE, et al. A pilot study of amygdala volumes in pediatric generalized anxiety disorder. Biol Psychiatry. 2000;48(1):51–57. doi: 10.1016/S0006-3223(00)00835-0.
  • Gold AL, Steuber ER, White LK, et al. Cortical thickness and subcortical gray matter volume in pediatric anxiety disorders. Neuropsychopharmacology. 2017;42(12):2423–2433. doi: 10.1038/npp.2017.83.
  • Moon C-M, Jeong G-W. Abnormalities in gray and white matter volumes associated with explicit memory dysfunction in patients with generalized anxiety disorder. Acta Radiol. 2017;58(3):353–361. doi: 10.1177/0284185116649796.
  • Moon C-M, Kim G-W, Jeong G-W. Whole-brain gray matter volume abnormalities in patients with generalized anxiety disorder: voxel-based morphometry. NeuroReport. 2014;25(3):184–189. doi: 10.1097/WNR.0000000000000100.
  • Harrewijn A, Cardinale EM, Groenewold NA, et al. Cortical and subcortical brain structure in generalized anxiety disorder: findings from 28 research sites in the ENIGMA-Anxiety Working Group. Transl Psychiatry. 2021;11(1):502. doi: 10.1038/s41398-021-01622-1.
  • Davis M, Whalen PJ. The amygdala: vigilance and emotion. Mol Psychiatry. 2001;6(1):13–34. doi: 10.1038/sj.mp.4000812.
  • Lingawi NW, Laurent V, Westbrook RF, et al. Acquisition and extinction of second-order context conditioned fear: role of the amygdala. Neurobiol Learn Mem. 2021;183:107485. doi: 10.1016/j.nlm.2021.107485.
  • Sah P, Faber ESL, Lopez De Armentia M, et al. The amygdaloid complex: anatomy and physiology. Physiol Rev. 2003;83(3):803–834. doi: 10.1152/physrev.00002.2003.
  • Oshri A, Gray JC, Owens MM, et al. Adverse childhood experiences and amygdalar reduction: high-resolution segmentation reveals associations with subnuclei and psychiatric outcomes. Child Maltreat. 2019;24(4):400–410. doi: 10.1177/1077559519839491.
  • Van Der Meer D, Rokicki J, Kaufmann T, et al. Brain scans from 21,297 individuals reveal the genetic architecture of hippocampal subfield volumes. Mol Psychiatry. 2020;25(11):3053–3065. doi: 10.1038/s41380-018-0262-7.
  • Ghasemi M, Navidhamidi M, Rezaei F, et al. Anxiety and hippocampal neuronal activity: relationship and potential mechanisms. Cogn Affect Behav Neurosci. 2022;22(3):431–449. doi: 10.3758/s13415-021-00973-y.
  • Jacobson L, Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev. 1991;12(2):118–134. doi: 10.1210/edrv-12-2-118.
  • Kark SM, Birnie MT, Baram TZ, et al. Functional connectivity of the human paraventricular thalamic nucleus: insights from high field functional MRI. Front Integr Neurosci. 2021;15:662293. doi: 10.3389/fnint.2021.662293.
  • Lee S, Shin H-S. The role of mediodorsal thalamic nucleus in fear extinction. J Anal Sci Technol. 2016;7(1):13. doi: 10.1186/s40543-016-0093-6.
  • Ouhaz Z, Ba-M’hamed S, Mitchell AS, et al. Behavioral and cognitive changes after early postnatal lesions of the rat mediodorsal thalamus. Behav Brain Res. 2015;292:219–232. doi: 10.1016/j.bbr.2015.06.017.
  • Timbie C, García-Cabezas MÁ, Zikopoulos B, et al. Organization of primate amygdalar–thalamic pathways for emotions. PLoS Biol. 2020;18(2):e3000639. doi: 10.1371/journal.pbio.3000639.
  • McKlveen JM, Myers B, Flak JN, et al. Role of prefrontal cortex glucocorticoid receptors in stress and emotion. Biol Psychiatry. 2013;74(9):672–679. doi: 10.1016/j.biopsych.2013.03.024.
  • Carpenter KLH, Angold A, Chen N-K, et al. Preschool anxiety disorders (ds000144) [dataset]; 2018.
  • Carpenter KLH, Angold A, Chen N-K, et al. Preschool anxiety disorders predict different patterns of amygdala–prefrontal connectivity at school-age. PLOS One. 2015;10(1):e0116854. doi: 10.1371/journal.pone.0116854.
  • Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis: I. Segmentation surface reconstruction. NeuroImage. 1999;9:179–194. doi: 10.1006/nimg.1998.0395.
  • Dale AM, Sereno I. Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci. 1993;5(2):162–176. doi: 10.1162/jocn.1993.5.2.162.
  • Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A. 2000;97(20):11050–11055. doi: 10.1073/pnas.200033797.
  • Fischl B, Liu A, Dale AM. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging. 2001;20(1):70–80. doi: 10.1109/42.906426.
  • Fischl B, Salat DH, Busa E, et al. Whole brain segmentation. Neuron. 2002;33(3):341–355. doi: 10.1016/S0896-6273(02)00569-X.
  • Fischl B, Salat DH, Van Der Kouwe AJW, et al. Sequence-independent segmentation of magnetic resonance images. Neuroimage. 2004;23(Suppl. 1):S69–S84. doi: 10.1016/j.neuroimage.2004.07.016.
  • Ségonne F, Dale AM, Busa E, et al. A hybrid approach to the skull stripping problem in MRI. Neuroimage. 2004;22(3):1060–1075. doi: 10.1016/j.neuroimage.2004.03.032.
  • Ségonne F, Pacheco J, Fischl B. Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging. 2007;26(4):518–529. doi: 10.1109/TMI.2006.887364.
  • Iglesias JE, Augustinack JC, Nguyen K, et al. A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: application to adaptive segmentation of in vivo MRI. Neuroimage. 2015;115:117–137. doi: 10.1016/j.neuroimage.2015.04.042.
  • Saygin ZM, Kliemann D, Iglesias JE, et al. High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: manual segmentation to automatic atlas. Neuroimage. 2017;155:370–382. doi: 10.1016/j.neuroimage.2017.04.046.
  • Iglesias JE, Insausti R, Lerma-Usabiaga G, et al. A probabilistic atlas of the human thalamic nuclei combining ex vivo MRI and histology (arXiv:1806.08634). arXiv; 2018. Available from: http://arxiv.org/abs/1806.08634
  • Sämann PG, Iglesias JE, Gutman B, et al. FreeSurfer‐based segmentation of hippocampal subfields: a review of methods and applications, with a novel quality control procedure for ENIGMA studies and other collaborative efforts. Hum Brain Mapp. 2022;43(1):207–233. doi: 10.1002/hbm.25326.
  • Shapiro SS, Wilk MB. An analysis of variance test for normality (complete samples). Biometrika. 1965;52(3–4):591–611. doi: 10.1093/biomet/52.3-4.591.
  • Franz L, Angold A, Copeland W, et al. Preschool anxiety disorders in pediatric primary care: prevalence and comorbidity. J Am Acad Child Adolesc Psychiatry. 2013;52(12):1294–1303.e1. doi: 10.1016/j.jaac.2013.09.008.
  • Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B (Methodol). 1995;57(1):289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x.
  • Bourne VJ, Vladeanu M. Lateralisation for processing facial emotion and anxiety: contrasting state, trait and social anxiety. Neuropsychologia. 2011;49(5):1343–1349. doi: 10.1016/j.neuropsychologia.2011.02.008.
  • Kolesar TA, Bilevicius E, Wilson AD, et al. Systematic review and meta-analyses of neural structural and functional differences in generalized anxiety disorder and healthy controls using magnetic resonance imaging. Neuroimage Clin. 2019;24:102016. doi: 10.1016/j.nicl.2019.102016.
  • McEwen BS, Nasca C, Gray JD. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology. 2016;41(1):3–23. doi: 10.1038/npp.2015.171.
  • McEwen BS, Eiland L, Hunter RG, et al. Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology. 2012;62(1):3–12. doi: 10.1016/j.neuropharm.2011.07.014.
  • McKinnon MC, Yucel K, Nazarov A, et al. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci. 2009;34(1):41–54.
  • Fu CHY, Fan Y, Davatzikos C. Widespread morphometric abnormalities in major depression. Neuroimaging Clin N Am. 2020;30(1):85–95. doi: 10.1016/j.nic.2019.09.008.
  • Huang Y, Coupland NJ, Lebel RM, et al. Structural changes in hippocampal subfields in major depressive disorder: a high-field magnetic resonance imaging study. Biol Psychiatry. 2013;74(1):62–68. doi: 10.1016/j.biopsych.2013.01.005.
  • Teicher MH, Anderson CM, Polcari A. Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci U S A. 2012;109(9):E563–E572. doi: 10.1073/pnas.1115396109.
  • Zhang L, Hu X, Lu L, et al. Abnormalities of hippocampal shape and subfield volumes in medication-free patients with obsessive–compulsive disorder. Hum Brain Mapp. 2019;40(14):4105–4113. doi: 10.1002/hbm.24688.
  • Vattimo EFQ, Dos Santos AC, Hoexter MQ, et al. Higher volumes of hippocampal subfields in pediatric obsessive-compulsive disorder. Psychiatry Res Neuroimaging. 2021;307:111200. doi: 10.1016/j.pscychresns.2020.111200.
  • Radley JJ, Sawchenko PE. Evidence for involvement of a limbic paraventricular hypothalamic inhibitory network in hypothalamic-pituitary-adrenal axis adaptations to repeated stress: integration of cortical influences on HPA axis. J Comp Neurol. 2015;523(18):2769–2787. doi: 10.1002/cne.23815.
  • Chen Y, Cui Q, Fan Y-S, et al. Progressive brain structural alterations assessed via causal analysis in patients with generalized anxiety disorder. Neuropsychopharmacology. 2020;45(10):1689–1697. doi: 10.1038/s41386-020-0704-1.
  • Rosenberg DR, Benazon NR, Gilbert A, et al. Thalamic volume in pediatric obsessive–compulsive disorder patients before and after cognitive behavioral therapy. Biol Psychiatry. 2000;48(4):294–300. doi: 10.1016/S0006-3223(00)00902-1.
  • Weeland CJ, Kasprzak S, De Joode NT, et al. The thalamus and its subnuclei—a gateway to obsessive-compulsive disorder. Transl Psychiatry. 2022;12(1):70. doi: 10.1038/s41398-022-01823-2.
  • Abdallah CG, Coplan JD, Jackowski A, et al. A pilot study of hippocampal volume and N-acetylaspartate (NAA) as response biomarkers in riluzole-treated patients with GAD. Eur Neuropsychopharmacol. 2013;23(4):276–284. doi: 10.1016/j.euroneuro.2012.05.009.
  • Madonna D, Delvecchio G, Soares JC, et al. Structural and functional neuroimaging studies in generalized anxiety disorder: a systematic review. Braz J Psychiatry. 2019;41(4):336–362. doi: 10.1590/1516-4446-2018-0108.
  • Du Y, Li H, Xiao H, et al. Illness severity moderated association between trait anxiety and amygdala-based functional connectivity in generalized anxiety disorder. Front Behav Neurosci. 2021;15:637426. doi: 10.3389/fnbeh.2021.637426.
  • Gottschalk MG, Domschke K. Genetics of generalized anxiety disorder and related traits. Dialog Clin Neurosci. 2017;19(2):159–168. doi: 10.31887/DCNS.2017.19.2/kdomschke.
  • Sawalha J, Yousefnezhad M, Selvitella AM, et al. Predicting pediatric anxiety from the temporal pole using neural responses to emotional faces. Sci Rep. 2021;11(1):16723. doi: 10.1038/s41598-021-95987-4.
  • Basten U, Hilger K, Fiebach CJ. Where smart brains are different: a quantitative meta-analysis of functional and structural brain imaging studies on intelligence. Intelligence. 2015;51:10–27. doi: 10.1016/j.intell.2015.04.009.
  • Pangelinan MM, Zhang G, VanMeter JW, et al. Beyond age and gender: relationships between cortical and subcortical brain volume and cognitive-motor abilities in school-age children. Neuroimage. 2011;54(4):3093–3100. doi: 10.1016/j.neuroimage.2010.11.021.
  • Hedges EP, Dimitrov M, Zahid U, et al. Reliability of structural MRI measurements: the effects of scan session, head tilt, inter-scan interval, acquisition sequence, FreeSurfer version and processing stream. Neuroimage. 2022;246:118751. doi: 10.1016/j.neuroimage.2021.118751.
  • Brown EM, Pierce ME, Clark DC, et al. Test–retest reliability of FreeSurfer automated hippocampal subfield segmentation within and across scanners. Neuroimage. 2020;210:116563. doi: 10.1016/j.neuroimage.2020.116563.
  • Brown GG, Ostrowitzki S, Stein MB, et al. Temporal profile of brain response to alprazolam in patients with generalized anxiety disorder. Psychiatry Res. 2015;233(3):394–401. doi: 10.1016/j.pscychresns.2015.06.016.
  • Ask H, Cheesman R, Jami ES, et al. Genetic contributions to anxiety disorders: where we are and where we are heading. Psychol Med. 2021;51(13):2231–2246. doi: 10.1017/S0033291720005486.
  • Waszczuk MA, Zavos HMS, Gregory AM, et al. The phenotypic and genetic structure of depression and anxiety disorder symptoms in childhood, adolescence, and young adulthood. JAMA Psychiatry. 2014;71(8):905–916. doi: 10.1001/jamapsychiatry.2014.655.