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Open Access 25-04-2022 | Obsessive-Compulsive Disorder | Original Article

Cortico-amygdalar connectivity and externalizing/internalizing behavior in children with neurodevelopmental disorders

Authors: Hajer Nakua, Colin Hawco, Natalie J. Forde, Grace R. Jacobs, Michael Joseph, Aristotle N. Voineskos, Anne L. Wheeler, Meng-Chuan Lai, Peter Szatmari, Elizabeth Kelley, Xudong Liu, Stelios Georgiades, Rob Nicolson, Russell Schachar, Jennifer Crosbie, Evdokia Anagnostou, Jason P. Lerch, Paul D. Arnold, Stephanie H. Ameis

Published in: Brain Structure and Function | Issue 6/2022

Abstract

Background

Externalizing and internalizing behaviors contribute to clinical impairment in children with neurodevelopmental disorders (NDDs). Although associations between externalizing or internalizing behaviors and cortico-amygdalar connectivity have been found in clinical and non-clinical pediatric samples, no previous study has examined whether similar shared associations are present across children with different NDDs.

Methods

Multi-modal neuroimaging and behavioral data from the Province of Ontario Neurodevelopmental Disorders (POND) Network were used. POND participants aged 6–18 years with a primary diagnosis of autism spectrum disorder (ASD), attention-deficit/hyperactivity disorder (ADHD) or obsessive–compulsive disorder (OCD), as well as typically developing children (TDC) with T1-weighted, resting-state fMRI or diffusion weighted imaging (DWI) and parent-report Child Behavioral Checklist (CBCL) data available, were analyzed (total n = 346). Associations between externalizing or internalizing behavior and cortico-amygdalar structural and functional connectivity indices were examined using linear regressions, controlling for age, gender, and image-modality specific covariates. Behavior-by-diagnosis interaction effects were also examined.

Results

No significant linear associations (or diagnosis-by-behavior interaction effects) were found between CBCL-measured externalizing or internalizing behaviors and any of the connectivity indices examined. Post-hoc bootstrapping analyses indicated stability and reliability of these null results.

Conclusions

The current study provides evidence towards an absence of a shared linear relationship between internalizing or externalizing behaviors and cortico-amygdalar connectivity properties across a transdiagnostic sample of children with different primary NDD diagnoses and TDC. Different methodological approaches, including incorporation of multi-dimensional behavioral data (e.g., task-based fMRI) or clustering approaches may be needed to clarify complex brain-behavior relationships relevant to externalizing/internalizing behaviors in heterogeneous clinical NDD populations.

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Abramovitch A, Dar R, Mittelman A, Wilhelm S (2015) Comorbidity between attention deficit/hyperactivity disorder and obsessive-compulsive disorder across the lifespan: a systematic and critical review. Harv Rev Psychiatry 23:245–262. https://doi.org/10.1097/HRP.0000000000000050CrossRefPubMedPubMedCentral

Achenbach TM, Ruffle TM (2000) The child behavior checklist and related forms for assessing behavioral/emotional problems and competencies. Pediatr Rev 21:265–271. https://doi.org/10.1542/pir.21-8-265CrossRefPubMed

Aghajani M, Colins OF, Klapwijk ET, Veer IM, Andershed H, Popma A, van der Wee NJ, Vermeiren RRJM (2016) Dissociable relations between amygdala subregional networks and psychopathy trait dimensions in conduct-disordered juvenile offenders. Hum Brain Mapp 4033:4017–4033. https://doi.org/10.1002/hbm.23292CrossRef

Aghajani M, Klapwijk ET, van der Wee NJ, Veer IM, Rombouts SARB, Boon AE, van Beelen P, Popma A, Vermeiren RRJM, Colins OF (2017) Disorganized amygdala networks in conduct-disordered juvenile offenders with callous-unemotional traits. Biol Psychiatry 82:283–293. https://doi.org/10.1016/j.biopsych.2016.05.017CrossRefPubMed

Albaugh MD, Ducharme S, Watts R, Lewis JD (2016) Anxious/depressed symptoms are related to microstructural maturation of white matter in typically developing youths. Dev Psychopathol. https://doi.org/10.1017/S0954579416000444CrossRefPubMed

Alvarenga PG, do Rosario MC, Cesar RC, Manfro GG, Moriyama TS, Bloch MH, Shavitt RG, Hoexter MQ, Coughlin CG, Leckman JF, Miguel EC (2016) Obsessive–compulsive symptoms are associated with psychiatric comorbidities, behavioral and clinical problems: a population-based study of Brazilian school children. Eur Child Adolesc Psychiatry 25:175–182. https://doi.org/10.1007/s00787-015-0723-3CrossRefPubMed

Ameis SH, Ducharme S, Albaugh MD, Hudziak JJ, Botteron KN, Lepage C, Zhao L, Khundrakpam B, Collins DL, Lerch JP, Wheeler A, Schachar R, Evans AC, Karama S (2014) Cortical thickness, cortico-amygdalar networks, and externalizing behaviors in healthy children. Biol Psychiatry 75:65–72. https://doi.org/10.1016/j.biopsych.2013.06.008CrossRefPubMed

Ameis SH, Lerch JP, Taylor MJ, Lee W, Viviano JD, Pipitone J, Nazeri A, Croarkin PE, Voineskos AN, Lai MC, Crosbie J, Brian J, Soreni N, Schachar R, Szatmari P, Arnold PD, Anagnostou E (2016) A diffusion tensor imaging studyin children with ADHD, autism spectrum disorder, OCD, and matched controls: distinct and non-distinct white matter disruption and dimensional brain-behavior relationships. Am J Psychiatry 173:1213–1222. https://doi.org/10.1176/appi.ajp.2016.15111435CrossRefPubMed

Anderson AW (2001) Theoretical analysis of the effects of noise on diffusion tensor imaging. Magn Reson Med 46:1174–1188. https://doi.org/10.1002/mrm.1315CrossRefPubMed

Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078. https://doi.org/10.1016/j.neuroimage.2015.10.019CrossRefPubMed

Andersson JLR, Graham MS, Zsoldos E, Sotiropoulos SN (2016) Incorporating outlier detection and replacement into a non-parametric framework for movement and distortion correction of diffusion MR images. Neuroimage 141:556–572. https://doi.org/10.1016/j.neuroimage.2016.06.058CrossRefPubMed

Andre QR, Geeraert BL, Lebel C (2020) Brain structure and internalizing and externalizing behavior in typically developing children and adolescents. Brain Struct Funct. https://doi.org/10.1007/s00429-019-01973-yCrossRefPubMed

Anholt GE, Cath DC, Van Oppen P, Eikelenboom M, Smit JH, Van Megen H, Van Balkom AJLM (2010) Autism and adhd symptoms in patients with ocd: are they associated with specific oc symptom dimensions or oc symptom severity. J Autism Dev Disord 40:580–589. https://doi.org/10.1007/s10803-009-0922-1CrossRefPubMed

Antshel KM, Zhang-James Y, Faraone SV (2013) The comorbidity of ADHD and autism spectrum disorder. Expert Rev Neurother 13:1117–1128. https://doi.org/10.1586/14737175.2013.840417CrossRefPubMed

Arim RG, Kohen DE, Garner RE, Lach LM, Brehaut JC, MacKenzie MJ, Rosenbaum PL (2015) Psychosocial functioning in children with neurodevelopmental disorders and externalizing behavior problems. Disabil Rehabil 37:345–354. https://doi.org/10.3109/09638288.2014.919361CrossRefPubMed

Backhausen LL, Herting MM, Buse J, Roessner V, Smolka MN, Vetter NC (2016) Quality control of structural MRI images applied using FreeSurfer-a hands-on workflow to rate motion artifacts. Front Neurosci 10:1–10. https://doi.org/10.3389/fnins.2016.00558CrossRef

Bauminger N, Solomon M, Rogers SJ (2010) Externalizing and internalizing behaviors in ASD. Autism Res 3:101–112. https://doi.org/10.1002/aur.131CrossRefPubMedPubMedCentral

Bos MGN, Wierenga LM, Blankenstein NE, Schreuders E, Tamnes CK, Crone EA (2018) Longitudinal structural brain development and externalizing behavior in adolescence. J Child Psychol Psychiatry Allied Discip 59:1061–1072. https://doi.org/10.1111/jcpp.12972CrossRef

Bradley EA, Summers JA, Wood HL, Bryson SE (2004) Comparing rates of psychiatric and behavior disorders in adolescents and young adults with severe intellectual disability with and without autism. J Autism Dev Disord 34:151–161. https://doi.org/10.1023/B:JADD.0000022606.97580.19CrossRefPubMed

Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, Snyder AZ (2004) A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23:724–738. https://doi.org/10.1016/j.neuroimage.2004.06.018CrossRefPubMed

Button K, Ioannidis J, Mokrysz C et al (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14:365–376. https://doi.org/10.1038/nrn3475CrossRefPubMed

Carlisi CO, Norman LJ, Lukito SS, Radua J, Mataix-Cols D, Rubia K (2017) Comparative multimodal meta-analysis of structural and functional brain abnormalities in autism spectrum disorder and obsessive-compulsive disorder. Biol Psychiatry 82:83–102. https://doi.org/10.1016/j.biopsych.2016.10.006CrossRefPubMed

Castellanos-Ryan N, Struve M, Whelan R, Banaschewski T, Barker GJ, Bokde ALW, Bromberg U, Büchel C, Flor H, Fauth-Bühler M, Frouin V, Gallinat J, Gowland P, Heinz A, Lawrence C, Martinot JL, Nees F, Paus T, Pausova Z, Rietschel M, Robbins TW, Smolka MN, Schumann G, Garavan H, Conrod PJ (2014) Neural and cognitive correlates of the common and specific variance across externalizing problems in young adolescence. Am J Psychiatry 171:1310–1319. https://doi.org/10.1176/appi.ajp.2014.13111499CrossRefPubMed

Catani M, Dell’Acqua F, Thiebaut de Schotten M (2013) A revised limbic system model for memory, emotion and behaviour. Neurosci Biobehav Rev 37:1724–1737. https://doi.org/10.1016/j.neubiorev.2013.07.001CrossRefPubMed

Choi E, Vandewouw M, Taylor M, Arnold P, Brian J, Crosbie J, Kelley E, Lai M, Liu X, Schachar R, Lerch J, Anagnostou E (2020) Beyond diagnosis: cross-diagnostic features in canonical resting-state networks in children with neurodevelopmental disorders. Neuroimage Clin 28:102476. https://doi.org/10.1016/j.nicl.2020.102476CrossRefPubMedPubMedCentral

Ciric R, Rosen AFG, Erus G, Cieslak M, Adebimpe A, Cook PA, Bassett DS, Davatzikos C, Wolf DH, Satterthwaite TD (2018) Mitigating head motion artifact in functional connectivity MRI. Nat Protoc 13:2801–2826. https://doi.org/10.1038/s41596-018-0065-yCrossRefPubMedPubMedCentral

Dajani DR, Llabre MM, Nebel MB, Mostofsky SH, Uddin LQ (2016) Heterogeneity of executive functions among comorbid neurodevelopmental disorders. Sci Rep 6:1–10. https://doi.org/10.1038/srep36566CrossRef

Dajani DR, Burrows CA, Odriozola P, Baez A, Nebel MB, Mostofsky SH, Uddin LQ (2019) Investigating functional brain network integrity using a traditional and novel categorical scheme for neurodevelopmental disorders. NeuroImage Clin 21:101678. https://doi.org/10.1016/j.nicl.2019.101678CrossRefPubMedPubMedCentral

Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021CrossRefPubMed

Dickie EW, Ameis SH, Shahab S, Calarco N, Smith DE, Miranda D, Viviano JD, Voineskos AN (2018) Personalized intrinsic network topography mapping and functional connectivity deficits in autism spectrum disorder. Biol Psychiatry 84:278–286. https://doi.org/10.1016/j.biopsych.2018.02.1174CrossRefPubMedPubMedCentral

Dickie EW, Anticevic A, Smith DE, Coalson TS, Manogaran M, Calarco N, Viviano JD, Glasser MF, Van Essen DC, Voineskos AN (2019) Ciftify: a framework for surface-based analysis of legacy MR acquisitions. Neuroimage 197:818–826. https://doi.org/10.1016/j.neuroimage.2019.04.078CrossRefPubMed

Ducharme S, Hudziak JJ, Botteron KN, Ganjavi H, Lepage C, Collins DL, Albaugh MD, Evans AC, Karama S (2011) Right anterior cingulate cortical thickness and bilateral striatal volume correlate with child behavior checklist aggressive behavior scores in healthy children. Biol Psychiatry 70:283–290. https://doi.org/10.1016/j.biopsych.2011.03.015CrossRefPubMedPubMedCentral

Ducharme S, Albaugh MD, Hudziak JJ, Botteron KN, Nguyen TV, Truong C, Evans AC, Karama S (2014) Anxious/depressed symptoms are linked to right ventromedial prefrontal cortical thickness maturation in healthy children and young adults. Cereb Cortex 24:2941–2950. https://doi.org/10.1093/cercor/bht151CrossRefPubMed

Dwyer SB, Nicholson JM, Battistutta D (2006) Parent and teacher identification of children at risk of developing internalizing or externalizing mental health problems: a comparison of screening methods. Prev Sci 7:343–357. https://doi.org/10.1007/s11121-006-0026-5CrossRefPubMed

Efron B, Tibshirani R(1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Stat Sci 1(1):54–75. https://www.jstor.org/stable/2245500

Eklund A, Nichols TE, Knutsson H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci U S A 113:7900–7905. https://doi.org/10.1073/pnas.1602413113CrossRefPubMedPubMedCentral

Esteban O, Birman D, Schaer M, Koyejo OO, Poldrack RA, Gorgolewski KJ (2017) MRIQC: advancing the automatic prediction of image quality in MRI from unseen sites. PLoS One 12:e0184661. https://doi.org/10.1371/journal.pone.0184661CrossRefPubMedPubMedCentral

Esteban O, Markiewicz CJ, Blair RW, Moodie CA, Isik AI, Erramuzpe A, Kent JD, Goncalves M, DuPre E, Snyder M, Oya H, Ghosh SS, Wright J, Durnez J, Poldrack RA, Gorgolewski KJ (2019) fMRIPrep: a robust preprocessing pipeline for functional MRI. Nat Methods 16:111–116. https://doi.org/10.1038/s41592-018-0235-4CrossRefPubMed

Etkin A, Egner T, Peraza DM, Kandel ER, Hirsch J (2006) Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51:871–882. https://doi.org/10.1016/j.neuron.2006.07.029CrossRefPubMed

Fair DA, Bathula D, Nikolas MA, Nigg JT (2012) Distinct neuropsychological subgroups in typically developing youth inform heterogeneity in children with ADHD. Proc Natl Acad Sci U S A 109:6769–6774. https://doi.org/10.1073/pnas.1115365109CrossRefPubMedPubMedCentral

Feczko E, Miranda-Dominguez O, Marr M, Graham AM, Nigg JT, Fair DA (2019) The heterogeneity problem: approaches to identify psychiatric subtypes. Trends Cogn Sci 23:584–601. https://doi.org/10.1016/j.tics.2019.03.009CrossRefPubMedPubMedCentral

Fedorov A, Beichel R, Kalpathy-Cramer J, Finet J, Fillion-Robin JC, Pujol S, Bauer C, Jennings D, Fennessy F, Sonka M, Buatti J, Aylward S, Miller JV, Pieper S, Kikinis R (2012) 3D slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging 30:1323–1341. https://doi.org/10.1016/j.mri.2012.05.001CrossRefPubMedPubMedCentral

Ghandour RM, Sherman LJ, Vladutiu CJ, Ali MM, Lynch SE, Bitsko RH, Blumberg SJ (2019) Prevalence and treatment of depression, anxiety, and conduct problems in US children. J Pediatr 206:256-267.e3. https://doi.org/10.1016/j.jpeds.2018.09.021CrossRefPubMed

Hariri AR, Mattay VS, Tessitore A, Fera F, Weinberger DR (2003) Neocortical modulation of the amygdala response to fearful stimuli. Biol Psychiatry 53:494–501. https://doi.org/10.1016/S0006-3223(02)01786-9CrossRefPubMed

Havdahl KA, von Tetzchner S, Huerta M, Lord C, Bishop SL (2016) Utility of the child behavior checklist as a screener for autism spectrum disorder. Autism Res 9:33–42. https://doi.org/10.1002/aur.1515CrossRefPubMed

He Y, Byrge L, Kennedy DP (2020) Nonreplication of functional connectivity differences in autism spectrum disorder across multiple sites and denoising strategies. Hum Brain Mapp. https://doi.org/10.1002/hbm.24879CrossRefPubMedPubMedCentral

Hill AP, Zuckerman KE, Hagen AD, Kriz DJ, Duvall SW, Van Santen J, Nigg J, Fair D, Fombonne E (2014) Aggressive behavior problems in children with autism spectrum disorders: prevalence and correlates in a large clinical sample. Res Autism Spectr Disord 8:1121–1133. https://doi.org/10.1016/j.rasd.2014.05.006CrossRefPubMedPubMedCentral

Himberg J, Hyvarinen A, Esposito F (2004) Validating the independent components of neuroimaging time series via clustering and visualization. Neuroimage 22:1214–1222. https://doi.org/10.1016/j.neuroimage.2004.03.027CrossRefPubMed

Ibrahim K, Eilbott JA, Ventola P, He G, Pelphrey KA, McCarthy G, Sukhodolsky DG (2019) Reduced amygdala-prefrontal functional connectivity in children with autism spectrum disorder and co-occurring disruptive behavior. Biol Psychiatry Cogn Neurosci Neuroimaging 4:1031–1041. https://doi.org/10.1016/j.bpsc.2019.01.009CrossRefPubMedPubMedCentral

Ickowicz A, Schachar RJ, Sugarman R, Chen SX, Millette C, Cook L (2006) The parent interview for child symptoms. Can J Psychiatry 51:325–328. https://doi.org/10.1177/070674370605100508CrossRefPubMed

Ioannidis JPA (2018) Why most published research findings are false. Get Good Res Integr Biomed Sci 2:2–8. https://doi.org/10.1371/journal.pmed.0020124CrossRef

Jacob C, Gross-Lesch S, Jans T, Geissler J, Reif A, Dempfle A, Lesch KP (2014) Internalizing and externalizing behavior in adult ADHD. ADHD Atten Deficit Hyperact Disord 6:101–110. https://doi.org/10.1007/s12402-014-0128-zCrossRef

Jacobs G, Voineskos A, Hawco C, Stefanik L, Forde N, Dickie E, Lai M-C, Szatmari P, Schachar R, Crosbie J, Arnold P, Goldenberg A, Erdman L, Lerch J, Anagnostou E, Ameis S (2020) Integration of brain and behavior measures for identification of data-driven groups cutting across children with ASD, ADHD, or OCD. Neuropsychopharmacol 46:647–653. https://doi.org/10.1038/s41386-020-00902-6CrossRef

Jang J, Matson JL, Williams LW, Tureck K, Goldin RL, Cervantes PE (2013) Rates of comorbid symptoms in children with ASD, ADHD, and comorbid ASD and ADHD. Res Dev Disabil 34:2369–2378. https://doi.org/10.1016/j.ridd.2013.04.021CrossRefPubMed

Kern JK, Geier DA, King PG, Sykes LK, Mehta JA, Geier MR (2015) Shared brain connectivity issues, symptoms, and comorbidities in autism spectrum disorder, attention deficit/hyperactivity disorder, and Tourette syndrome. Brain Connect 5:321–335. https://doi.org/10.1089/brain.2014.0324CrossRefPubMed

Korhonen M, Luoma I, Salmelin RK, Helminen M, Kaltiala-Heino R, Tamminen T (2014) The trajectories of child’s internalizing and externalizing problems, social competence and adolescent self-reported problems in a Finnish normal population sample. Sch Psychol Int 35:561–579. https://doi.org/10.1177/0143034314525511CrossRef

Kushki A, Anagnostou E, Hammill C, Duez P, Brian J, Iaboni A, Schachar R, Crosbie J, Arnold P, Lerch JP (2019) Examining overlap and homogeneity in ASD, ADHD, and OCD: a data-driven, diagnosis-agnostic approach. Transl Psychiatry. https://doi.org/10.1038/s41398-019-0631-2CrossRefPubMedPubMedCentral

Lai MC, Kassee C, Besney R, Bonato S, Hull L, Mandy W, Szatmari P, Ameis SH (2019) Prevalence of co-occurring mental health diagnoses in the autism population: a systematic review and meta-analysis. Lancet Psychiatry 6:819–829. https://doi.org/10.1016/S2215-0366(19)30289-5CrossRefPubMed

Lawson RA, Papadakis AA, Higginson CI, Barnett JE, Wills MC, Strang JF, Wallace GL, Kenworthy L (2015) Everyday executive function impairments predict comorbid psychopathology in autism spectrum and attention deficit hyperactivity disorders. Neuropsychology 29:445–453. https://doi.org/10.1037/neu0000145CrossRefPubMed

Lewin AB, Wood JJ, Gunderson S, Murphy TK, Storch EA (2011) Phenomenology of comorbid autism spectrum and obsessive-compulsive disorders among children. J Dev Phys Disabil 23:543–553. https://doi.org/10.1007/s10882-011-9247-zCrossRef

Lionel AC, Crosbie J, Barbosa N, Goodale T, Thiruvahindrapuram B, Rickaby J, Gazzellone M, Carson AR, Howe JL, Wang Z, Wei J, Stewart AFR, Roberts R, McPherson R, Fiebig A, Franke A, Schreiber S, Zwaigenbaum L, Fernandez BA, Roberts W, Arnold PD, Szatmari P, Marshall CR, Schachar R, Scherere SW (2011) Rare copy number variation discovery and cross-disorder comparisons identify risk genes for ADHD. Sci Transl Med. https://doi.org/10.1126/scitranslmed.3002464CrossRefPubMed

Lionel AC, Tammimies K, Vaags AK, Rosenfeld JA, Ahn JW, Merico D, Noor A, Runke CK, Pillalamarri VK, Carter MT, Gazzellone MJ, Thiruvahindrapuram B, Fagerberg C, Laulund LW, Pellecchia G, Lamoureux S, Deshpande C, Clayton-Smith J, White AC, Leather S, Trounce J, Bedford HM, Hatchwell E, Eis PS, Yuen RKC, Walker S, Uddin M, Geraghty MT, Nikkel SM, Tomiak EM, Fernandez BA, Soreni N, Crosbie J, Arnold PD, Schachar RJ, Roberts W, Paterson AD, So J, Szatmari P, Chrysler C, Woodbury-Smith M, Lowry RB, Zwaigenbaum L, Mandyam D, Wei J, MacDonald JR, Howe JL, Nalpathamkalam T, Wang Z, Tolson D, Cobb DS, Wilks TM, Sorensen MJ, Bader PI, An Y, Wu BL, Musumeci SA, Romano C, Postorivo D, Nardone AM, Monica MD, Scarano G, Zoccante L, Novara F, Zuffardi O, Ciccone R, Antona V, Carella M, Zelante L, Cavalli P, Poggiani C, Cavallari U, Argiropoulos B, Chernos J, Brasch-Andersen C, Speevak M, Fichera M, Ogilvie CM, Shen Y, Hodge JC, Talkowski ME, Stavropoulos DJ, Marshall CR, Scherer SW (2014) Disruption of the ASTN2/TRIM32 locus at 9q33.1 is a risk factor in males for autism spectrum disorders, ADHD and other neurodevelopmental phenotypes. Hum Mol Genet 23:2752–2768. https://doi.org/10.1093/hmg/ddt669CrossRefPubMed

Littell WM (1960) The wechsler intelligence scale for children: review of a decade of research. Psychological Bulletin 57(2):132–156. https://doi.org/10.1037/h0044513CrossRefPubMed

Lombardo M, Lai MC, Baron-Cohen S (2019) Big Data approaches to decomposing heterogeniety across the autism spectrum. Mol Psychiatry 24:1435–1450. https://doi.org/10.1038/s41380-018-0321-0CrossRefPubMedPubMedCentral

Lord C, Rutter M, Le Couteur A (1994) Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24(5):659–685. https://doi.org/10.1007/BF02172145CrossRefPubMed

Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, Dilavore PC, Pickles A, Rutter M (2000) The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30:205–223. https://doi.org/10.1023/A:1005592401947CrossRefPubMed

Luking KR, Repovs G, Belden AC, Gaffrey MS, Botteron KN, Luby JL, Barch DM (2011) Functional connectivity of the amygdala in early-childhood-onset depression. J Am Acad Child Adolesc Psychiatry 50:1027-1041.e3. https://doi.org/10.1016/j.jaac.2011.07.019CrossRefPubMedPubMedCentral

Marek S, Tervo-Clemmens B, Calabro FJ et al (2022) Reproducible brain-wide association studies require thousands of individuals. Nature 603:654–660. https://doi.org/10.1038/s41586-022-04492-9CrossRef

Masi G, Millepiedi S, Mucci M, Bertini N, Pfanner C, Arcangeli F (2006) Comorbidity of obsessive-compulsive disorder and attention-deficit/ hyperactivity disorder in referred children and adolescents. Compr Psychiatry 47:42–47. https://doi.org/10.1016/j.comppsych.2005.04.008CrossRefPubMed

Masouleh SK, Eickhoff SB, Hoffstaedter F, Genon S (2019) Empirical examination of the replicability of associations between brain structure and psychological variables. Elife 8:1–25. https://doi.org/10.7554/eLife.43464CrossRef

Mazurek MO, Kanne SM, Wodka EL (2013) Physical aggression in children and adolescents with autism spectrum disorders. Res Autism Spectr Disord 7:455–465. https://doi.org/10.1016/j.rasd.2012.11.004CrossRef

McIntosh A, Lobaugh N (2004) Partial least square analysis of neuroimaging data: applications and advances. Neuroimage 23:S250–S263. https://doi.org/10.1016/j.neuroimage.2004.07.020CrossRefPubMed

Mito H, Matsuura N, Mukai K, Yanagisawa Y, Nakajima A, Motoyama M, Arikawa A, Yamanishi K, Matsunaga H (2014) The impacts of elevated autism spectrum disorder traits on clinical and psychosocial features and long-term treatment outcome in adult patients with obsessive-compulsive disorder. Compr Psychiatry 55:1526–1533. https://doi.org/10.1016/j.comppsych.2014.05.005CrossRefPubMed

Mohamed Ali O, Vandermeer MRJ, Sheikh HI, Joanisse MF, Hayden EP (2019) Girls’ internalizing symptoms and white matter tracts in Cortico-Limbic circuitry. NeuroImage Clin 21:101650. https://doi.org/10.1016/j.nicl.2018.101650CrossRefPubMed

Noordermeer SDS, Luman M, Oosterlaan J (2016) A systematic review and meta-analysis of neuroimaging in oppositional defiant disorder (ODD) and conduct disorder (CD) taking attention-deficit hyperactivity disorder (ADHD) into account. Neuropsychol Rev 26:44–72. https://doi.org/10.1007/s11065-015-9315-8CrossRefPubMedPubMedCentral

Pardoe HR, Kucharsky Hiess R, Kuzniecky R (2016) Motion and morphometry in clinical and nonclinical populations. Neuroimage 135:177–185. https://doi.org/10.1016/j.neuroimage.2016.05.005CrossRefPubMed

Parkes L, Fulcher B, Yücel M, Fornito A (2018) An evaluation of the efficacy, reliability, and sensitivity of motion correction strategies for resting-state functional MRI. Neuroimage 171:415–436. https://doi.org/10.1016/j.neuroimage.2017.12.073CrossRefPubMed

Paulesu E, Sambugaro E, Torti T, Danelli L, Ferri F, Scialfa G, Sberna M, Ruggiero GM (2010) Neural correlates of worry in generalized anxiety disorder and in normal controls: a functional MRI study. Psychol Med. https://doi.org/10.1017/S0033291709005649CrossRefPubMed

Poldrack RA, Baker CI, Durnez J, Gorgolewski KJ, Matthews PM, Munafò MR, Nichols TE, Poline JB, Vul E, Yarkoni T (2017) Scanning the horizon: towards transparent and reproducible neuroimaging research. Nat Rev Neurosci 18:115–126. https://doi.org/10.1038/nrn.2016.167CrossRefPubMedPubMedCentral

Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154. https://doi.org/10.1016/j.neuroimage.2011.10.018CrossRefPubMed

Qin S, Young CB, Duan X, Chen T, Supekar K, Menon V (2014) Amygdala subregional structure and intrinsic functional connectivity predicts individual differences in anxiety during early childhood. Biol Psychiatry 75:892–900. https://doi.org/10.1016/j.biopsych.2013.10.006CrossRefPubMed

Raz N, Gunning-Dixon F, Head D, Rodrigue KM, Williamson A, Acker JD (2004) Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol Aging 25:377–396. https://doi.org/10.1016/S0197-4580(03)00118-0CrossRefPubMed

Reef J, Diamantopoulou S, Van Meurs I, Verhulst FC, Van Der Ende J (2011) Developmental trajectories of child to adolescent externalizing behavior and adult DSM-IV disorder: results of a 24-year longitudinal study. Soc Psychiatry Psychiatr Epidemiol 46:1233–1241. https://doi.org/10.1007/s00127-010-0297-9CrossRefPubMed

Rushworth MFS, Noonan MAP, Boorman ED, Walton ME, Behrens TE (2011) Frontal cortex and reward-guided learning and decision-making. Neuron 70:1054–1069. https://doi.org/10.1016/j.neuron.2011.05.014CrossRefPubMed

Satterthwaite TD, Wolf DH, Loughead J, Ruparel K, Elliott MA, Hakonarson H, Gur RC, Gur RE (2012) Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 60:623–632. https://doi.org/10.1016/j.neuroimage.2011.12.063CrossRefPubMed

Saxbe D, Lyden H, Gimbel SI, Sachs M, Del Piero LB, Margolin G, Kaplan JT (2018) Longitudinal associations between family aggression, externalizing behavior, and the structure and function of the amygdala. J Res Adolesc 28:134–149. https://doi.org/10.1111/jora.12349CrossRefPubMed

Scahill L, Riddle MA, McSwiggin-Hardin M, Ort SI, King RA, Goodman WK, Cicchetti D, Leckman JF (1997) Children’s Yale-brown obsessive compulsive scale: reliability and validity. J Am Acad Child Adolesc Psychiatry 36:844–852. https://doi.org/10.1097/00004583-199706000-00023CrossRefPubMed

Simmons JP, Nelson LD, Simonsohn U (2011) False-positive psychology: undisclosed flexibility in data collection and analysis allows presenting anything as significant. Psychol Sci 22:1359–1366. https://doi.org/10.1177/0956797611417632CrossRefPubMed

Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44(1):83−98. https://doi.org/10.1016/j.neuroimage.2008.03.061CrossRefPubMed

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219. https://doi.org/10.1016/j.neuroimage.2004.07.051CrossRef

Stoddard J, Tseng WL, Kim P, Chen G, Yi J, Donahue L, Brotman MA, Towbin KE, Pine DS, Leibenluft E (2017) Association of irritability and anxiety with the neural mechanisms of implicit face emotion processing in youths with psychopathology. JAMA Psychiat 74:95–103. https://doi.org/10.1001/jamapsychiatry.2016.3282CrossRef

Stoycos SA, Piero LD, Margolin G, Kaplan JT, Saxbe DE (2017) Neural correlates of inhibitory spillover in adolescence: associations with internalizing symptoms. Soc Cogn Affect Neurosci 12:1637–1646. https://doi.org/10.1093/scan/nsx098CrossRefPubMedPubMedCentral

Tax CM, Grussu F, Kaden E, Ning L, Rudrapatna U, John Evans C, St-Jean S, Leemans A, Koppers S, Merhof D, Ghosh A, Tanno R, Alexander DC, Zappalà S, Charron C, Kusmia S, Linden DE, Jones DK, Veraart J (2019) Cross-scanner and cross-protocol diffusion MRI data harmonisation: a benchmark database and evaluation of algorithms. Neuroimage 195:285–299. https://doi.org/10.1016/j.neuroimage.2019.01.077CrossRefPubMed

Torp NC, Dahl K, Skarphedinsson G, Compton S, Thomsen PH, Weidle B, Hybel K, Valderhaug R, Melin K, Nissen JB, Ivarsson T (2015) Predictors associated with improved cognitive-behavioral therapy outcome in pediatric obsessive-compulsive disorder. J Am Acad Child Adolesc Psychiatry 54:200-207.e1. https://doi.org/10.1016/j.jaac.2014.12.007CrossRefPubMed

Uddin LQ, Dajani DR, Voorhies W, Bednarz H, Kana RK (2017) Progress and roadblocks in the search for brain-based biomarkers of autism and attention-deficit/hyperactivity disorder. Transl Psychiatry 7:e1218. https://doi.org/10.1038/tp.2017.164CrossRefPubMedPubMedCentral

Van Der Meer JMJ, Oerlemans AM, Van Steijn DJ, Lappenschaar MGA, De Sonneville LMJ, Buitelaar JK, Rommelse NNJ (2012) Are autism spectrum disorder and attention-deficit/hyperactivity disorder different manifestations of one overarching disorder? Cognitive and symptom evidence from a clinical and population-based sample. J Am Acad Child Adolesc Psychiatry 51:1160-1172.e3. https://doi.org/10.1016/j.jaac.2012.08.024CrossRefPubMed

Van Dijk KRA, Hedden T, Venkataraman A, Evans KC, Lazar SW, Buckner RL (2010) Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J Neurophysiol 103:297–321. https://doi.org/10.1152/jn.00783.2009CrossRefPubMed

Vanderwal T, Kelly C, Eilbott J, Mayes LC, Castellanos FX (2015) Inscapes: a movie paradigm to improve compliance in functional magnetic resonance imaging. Neuroimage 122:222–232. https://doi.org/10.1016/j.neuroimage.2015.07.069CrossRefPubMed

Veraart J, Novikov DS, Christiaens D, Ades-aron B, Sijbers J, Fieremans E (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406. https://doi.org/10.1016/j.neuroimage.2016.08.016CrossRefPubMed

Vijayakumar N, Allen NB, Dennison M, Byrne ML, Simmons JG, Whittle S (2017) Cortico-amygdalar maturational coupling is associated with depressive symptom trajectories during adolescence. Neuroimage 156:403–411. https://doi.org/10.1016/j.neuroimage.2017.05.051CrossRefPubMed

Xia CH, Ma Z, Ciric R, Gu S, Betzel RF, Kaczkurkin AN, Calkins ME, Cook PA, García de la Garza A, Vandekar SN, Cui Z, Moore TM, Roalf DR, Ruparel K, Wolf DH, Davatzikos C, Gur RC, Gur RE, Shinohara RT, Bassett DS, Satterthwaite TD (2018) Linked dimensions of psychopathology and connectivity in functional brain networks. Nat Commun 9:1–14. https://doi.org/10.1038/s41467-018-05317-yCrossRef

Zald D, Lahey B (2017) Implications of the hierarchical structure of psychopathology for psychiatric neuroimaging. Biol Psychiatry: CNNI 2:310–317. https://doi.org/10.1016/j.bpsc.2017.02.003CrossRef

Title: Cortico-amygdalar connectivity and externalizing/internalizing behavior in children with neurodevelopmental disorders
Authors: Hajer Nakua
Colin Hawco
Natalie J. Forde
Grace R. Jacobs
Michael Joseph
Aristotle N. Voineskos
Anne L. Wheeler
Meng-Chuan Lai
Peter Szatmari
Elizabeth Kelley
Xudong Liu
Stelios Georgiades
Rob Nicolson
Russell Schachar
Jennifer Crosbie
Evdokia Anagnostou
Jason P. Lerch
Paul D. Arnold
Stephanie H. Ameis
Publication date: 25-04-2022
Publisher: Springer Berlin Heidelberg
Keywords: Obsessive-Compulsive Disorder
Autism Spectrum Disorder
Published in: Brain Structure and Function / Issue 6/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-022-02483-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Cortico-amygdalar connectivity and externalizing/internalizing behavior in children with neurodevelopmental disorders

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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