Source-based morphometry reveals structural brain pattern abnormalities in 22q11.2 deletion syndrome.
22q11 deletion syndrome
gray matter volume
magnetic resonnance imaging
source-based morphometry
Journal
Human brain mapping
ISSN: 1097-0193
Titre abrégé: Hum Brain Mapp
Pays: United States
ID NLM: 9419065
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
12
11
2023
received:
31
05
2023
accepted:
19
11
2023
medline:
15
1
2024
pubmed:
15
1
2024
entrez:
15
1
2024
Statut:
ppublish
Résumé
22q11.2 deletion syndrome (22q11DS) is the most frequently occurring microdeletion in humans. It is associated with a significant impact on brain structure, including prominent reductions in gray matter volume (GMV), and neuropsychiatric manifestations, including cognitive impairment and psychosis. It is unclear whether GMV alterations in 22q11DS occur according to distinct structural patterns. Then, 783 participants (470 with 22q11DS: 51% females, mean age [SD] 18.2 [9.2]; and 313 typically developing [TD] controls: 46% females, mean age 18.0 [8.6]) from 13 datasets were included in the present study. We segmented structural T1-weighted brain MRI scans and extracted GMV images, which were then utilized in a novel source-based morphometry (SBM) pipeline (SS-Detect) to generate structural brain patterns (SBPs) that capture co-varying GMV. We investigated the impact of the 22q11.2 deletion, deletion size, intelligence quotient, and psychosis on the SBPs. Seventeen GMV-SBPs were derived, which provided spatial patterns of GMV covariance associated with a quantitative metric (i.e., loading score) for analysis. Patterns of topographically widespread differences in GMV covariance, including the cerebellum, discriminated individuals with 22q11DS from healthy controls. The spatial extents of the SBPs that revealed disparities between individuals with 22q11DS and controls were consistent with the findings of the univariate voxel-based morphometry analysis. Larger deletion size was associated with significantly lower GMV in frontal and occipital SBPs; however, history of psychosis did not show a strong relationship with these covariance patterns. 22q11DS is associated with distinct structural abnormalities captured by topographical GMV covariance patterns that include the cerebellum. Findings indicate that structural anomalies in 22q11DS manifest in a nonrandom manner and in distinct covarying anatomical patterns, rather than a diffuse global process. These SBP abnormalities converge with previously reported cortical surface area abnormalities, suggesting disturbances of early neurodevelopment as the most likely underlying mechanism.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e26553Subventions
Organisme : NIMH NIH HHS
ID : U01MH101719
Pays : United States
Organisme : NIMH NIH HHS
ID : R01MH085953
Pays : United States
Organisme : NIMH NIH HHS
ID : U01MH119741-01
Pays : United States
Organisme : NIMH NIH HHS
ID : U01MH119758
Pays : United States
Organisme : NIH HHS
ID : U54HD079125
Pays : United States
Organisme : NIH HHS
ID : R01MH107018
Pays : United States
Organisme : NIH HHS
ID : U01MH101724
Pays : United States
Organisme : NIH HHS
ID : U01MH119738
Pays : United States
Organisme : NIH HHS
ID : 5U01MH119737-04
Pays : United States
Organisme : NIH HHS
ID : R01 MH064824
Pays : United States
Organisme : NIH HHS
ID : R01MH129636
Pays : United States
Organisme : NIH HHS
ID : K01MH112774
Pays : United States
Organisme : NIH HHS
ID : R01MH129742-01
Pays : United States
Organisme : NIH HHS
ID : R01AG058854-02
Pays : United States
Organisme : NIH HHS
ID : R01MH116147-04
Pays : United States
Informations de copyright
© 2024 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.
Références
Alexander-Bloch, A., Giedd, J. N., & Bullmore, E. (2013). Imaging structural co-variance between human brain regions. Nature Reviews Neuroscience, 14(5), 322-336.
Baker, K., Chaddock, C. A., Baldeweg, T., & Skuse, D. (2011). Neuroanatomy in adolescents and young adults with 22q11 deletion syndrome: Comparison to an IQ-matched group. NeuroImage, 55(2), 491-499.
Bearden, C. E.,Woodin, M. F., Wang, P., Moss, E., McGinn D.M., Zackai, E., Emannuel, B., & Tyrone, D. C. (2001). The neurocognitive phenotype of the 22q11.2 deletion syndrome: Selective deficit in visual-spatial memory. Journal of Clinical Experimental Neuropsychology, 23(4), 447-464.
Beckmann, C. F., Mackay, C. E., Filippini, N., & Smith, S. M. (2009). Group comparison of resting-state FMRI data using multi-subject ICA and dual regression: Organization for Human Brain Mapping 2009 Annual Meeting. NeuroImage, 47(suppl 1), S148.
Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., & Golani, I. (2001). Controlling the false discovery rate in behavior genetics research. Behavioural Brain Research, 125(1-2), 279-284.
Blagojevic, C., Heung, T., Theriault, M., Tomita-Mitchell, A., Chakraborty, P., Kernohan, K., Bulman, D. E., & Bassett, A. S. (2021). Estimate of the contemporary live-birth prevalence of recurrent 22q11.2 deletions: A cross-sectional analysis from population-based newborn screening. CMAJ Open, 9(3), E802-E809.
Campbell, L. E., Daly, E., Toal, F., Stevens, A., Azuma, R., Catani, M., Ng, V., van Amelsvoort, T., Chitnis, X., Cutter, W., Murphy, D. G. M., & Murphy, K. C. (2006). Brain and behaviour in children with 22q11.2 deletion syndrome: A volumetric and voxel-based morphometry MRI study. Brain, 129(5), 1218-1228.
Chen, A. A., Beer, J. C., Tustison, N. J., Cook, P. A., Shinohara, R. T., Shou, H., & The Alzheimer's Disease Neuroimaging Initiative. (2022). Mitigating site effects in covariance for machine learning in neuroimaging data. Human Brain Mapping, 43(4), 1179-1195.
Chen, J., Liu, J., Calhoun, V. D., Arias-Vasquez, A., Zwiers, M. P., Gupta, C. N., Franke, B., & Turner, J. A. (2014). Exploration of scanning effects in multi-site structural MRI studies. Journal of Neuroscience Methods, 230, 37-50.
Cheon, E. J., Bearden, C. E., Sun, D., Ching, C. R. K., Andreassen, O. A., Schmaal, L., Veltman, D. J., Thomopoulos, S. I., Kochunov, P., Jahanshad, N., Thompson, P. M., Turner, J. A., & van Erp, T. G. M. (2022). Cross disorder comparisons of brain structure in schizophrenia, bipolar disorder, major depressive disorder, and 22q11.2 deletion syndrome: A review of ENIGMA findings. Psychiatry and Clinical Neurosciences, 76(5), 140-161.
Ching, C. R., Gutman, B. A., Sun, D., Villalon-Reina, J., Ragothaman, A., Isaev, D., Zavaliangos-Petropulu, A., Lin, A., Jonas, R. K., Kushan, L., Pacheco-Hansen, L., Vajdi, A., Forsyth, J. K., Jalbrzikowski, M., Bakker, G., van Amelsvoort, T., Antshel, K. M., Fremont, W., Kates, W. R., … Bearden, C. E.. (2020). Mapping subcortical brain alterations in 22q11.2 deletion syndrome: Effects of deletion size and convergence with idiopathic neuropsychiatric illness. American Journal of Psychiatry, 177(7), 589-600.
Chow, E. W., Ho, A., Wei, C., Voormolen, E. H. J., Crawley, A. P., & Bassett, A. S. (2011). Association of schizophrenia in 22q11.2 deletion syndrome and gray matter volumetric deficits in the superior temporal gyrus. American Journal of Psychiatry, 168(5), 522-529.
Colloby, S. J., Nathan, P. J., Bakker, G., Lawson, R. A., Yarnall, A. J., Burn, D. J., O'Brien, J. T., & Taylor, J. P. (2021). Spatial covariance of cholinergic muscarinic M1/M4 receptors in Parkinson's disease. Movement Disorders, 36(8), 1879-1888.
Dai, R., Herold, C. J., Wang, X., Kong, L., & Schröder, J. (2023). Structural brain networks in schizophrenia based on nonnegative matrix factorization. Psychiatry Research: Neuroimaging, 334, 111690.
Fiksinski, A. M., Breetvelt, E. J., Lee, Y. J., Boot, E., Butcher, N., Palmer, L., Chow, E. W. C., Kahn, R. S., Vorstman, J. A. S., & Bassett, A. S. (2019). Neurocognition and adaptive functioning in a genetic high-risk model of schizophrenia. Psychological Medicine, 49(6), 1047-1054.
Fortin, J.-P., Cullen, N., Sheline, Y. I., Taylor, W. D., Aselcioglu, I., Cook, P. A., Adams, P., Cooper, C., Fava, M., McGrath, P. J., McInnis, M., Phillips, M. L., Trivedi, M. H., Weissman, M. M., & Shinohara, R. T. (2018). Harmonization of cortical thickness measurements across scanners and sites. NeuroImage, 167, 104-120.
Ge, R., Ding, S., Keeling, T., Honer, W. G., Frangou, S., & Vila-Rodriguez, F. (2021). SS-detect: Development and validation of a new strategy for source-based morphometry in multiscanner studies. Journal of Neuroimaging, 31(2), 261-271.
Ge, R., Downar, J., Blumberger, D. M., Daskalakis, Z. J., Lam, R. W., & Vila-Rodriguez, F. (2019). Structural network integrity of the central executive network is associated with the therapeutic effect of rTMS in treatment resistant depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 92, 217-225.
Ge, R., Hassel, S., Arnott, S. R., Davis, A. D., Harris, J. K., Zamyadi, M., Milev, R., Frey, B. N., Strother, S. C., Müller, D. J., Rotzinger, S., MacQueen, G. M., Kennedy, S. H., Lam, R. W., & Vila-Rodriguez, F. (2021). Structural covariance pattern abnormalities of insula in major depressive disorder: A CAN-BIND study report. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 111, 110194.
Ge, R., Liu, X., Long, D., Frangou, S., & Vila-Rodriguez, F. (2021). Sex effects on cortical morphological networks in healthy young adults. NeuroImage, 233, 117945.
Glaser, B., Mumme, D. L., Blasey, C., Morris, M. A., Dahoun, S. P., Antonarakis, S. E., Reiss, A. L., & Eliez, S. (2002). Language skills in children with velocardiofacial syndrome (deletion 22q11.2). Journal of Pediatrics, 140(6), 753-758.
Gothelf, D., Hoeft, F., Ueno, T., Sugiura, L., Lee, A. D., Thompson, P., & Reiss, A. L. (2011). Developmental changes in multivariate neuroanatomical patterns that predict risk for psychosis in 22q11.2 deletion syndrome. Journal of Psychiatric Research, 45(3), 322-331.
Gupta, C. N., Calhoun, V. D., Rachakonda, S., Chen, J., Patel, V., Liu, J., Segall, J., Franke, B., Zwiers, M. P., Arias-Vasquez, A., Buitelaar, J., Fisher, S. E., Fernandez, G., van Erp, T. G. M., Potkin, S., Ford, J., Mathalon, D., McEwen, S., Lee, H. J., … Turner, J. A. (2015). Patterns of gray matter abnormalities in schizophrenia based on an international mega-analysis. Schizophrenia Bulletin, 41(5), 1133-1142.
Gupta, C. N., Turner, J. A., & Calhoun, V. D. (2019). Source-based morphometry: A decade of covarying structural brain patterns. Brain Structure and Function, 224(9), 3031-3044.
Gur, R. E., Bassett, A. S., McDonald-McGinn, D. M., Bearden, C. E., Chow, E., Emanuel, B. S., Owen, M., Swillen, A., van den Bree, M., Vermeesch, J., Vorstman, J. A. S., Warren, S., Lehner, T., Morrow, B., & The International 22q11.2 Deletion Syndrome Brain Behavior Consortium. (2017). A neurogenetic model for the study of schizophrenia spectrum disorders: The international 22q11.2 deletion syndrome brain behavior consortium. Molecular Psychiatry, 22(12), 1664-1672.
Hafkemeijer, A., Altmann-Schneider, I., de Craen, A. J. M., Slagboom, P. E., van der Grond, J., & Rombouts, S. A. R. B. (2014). Associations between age and gray matter volume in anatomical brain networks in middle-aged to older adults. Aging Cell, 13(6), 1068-1074.
Hopkins, S. E., Chadehumbe, M., Blaine Crowley, T., Zackai, E. H., Bilaniuk, L. T., & McDonald-McGinn, D. M. (2018). Neurologic challenges in 22q11.2 deletion syndrome. American Journal of Medical Genetics-Part A, 176(10), 2140-2145.
Li, H., Smith, S. M., Gruber, S., Lukas, S. E., Silveri, M. M., Hill, K. P., Killgore, W. D. S., & Nickerson, L. D. (2020). Denoising scanner effects from multimodal MRI data using linked independent component analysis. NeuroImage, 208, 116388.
Li, Y. O., Adalı, T., & Calhoun, V. D. (2007). Estimating the number of independent components for functional magnetic resonance imaging data. Human Brain Mapping, 28(11), 1251-1266.
Lin, A., Ching, C. R. K., Vajdi, A., Sun, D., Jonas, R. K., Jalbrzikowski, M., Kushan-Wells, L., Pacheco Hansen, L., Krikorian, E., Gutman, B., Dokoru, D., Helleman, G., Thompson, P. M., & Bearden, C. E. (2017). Mapping 22q11.2 gene dosage effects on brain morphometry. Journal of Neuroscience, 37(26), 6183-6199.
Linton, S. R., Popa, A. M., Luck, S. J., Bolden, K., Carter, C. S., Niendam, T. A., & Simon, T. J. (2020). Neural and behavioral measures suggest that cognitive and affective functioning interactions mediate risk for psychosis-proneness symptoms in youth with chromosome 22q11.2 deletion syndrome. American Journal of Medical Genetics-Part A, 182(7), 1615-1630.
Luo, L., Xu, L., Jung, R., Pearlson, G., Adali, T., & Calhoun, V. D. (2012). Constrained source-based morphometry identifies structural networks associated with default mode network. Brain Connectivity, 2(1), 33-43.
Luo, N., Sui, J., Abrol, A., Lin, D., Chen, J., Vergara, V. M., Fu, Z., du, Y., Damaraju, E., Xu, Y., Turner, J. A., & Calhoun, V. D. (2020). Age-related structural and functional variations in 5,967 individuals across the adult lifespan. Human Brain Mapping, 41(7), 1725-1737.
McDonald-McGinn, D. M., Sullivan, K. E., Marino, B., Philip, N., Swillen, A., Vorstman, J. A. S., Zackai, E. H., Emanuel, B. S., Vermeesch, J. R., Morrow, B. E., Scambler, P. J., & Bassett, A. S. (2015). 22q11.2 deletion syndrome. Nature Reviews Disease Primers, 1(1), 1-19.
Mechelli, A., Friston, K. J., Frackowiak, R. S., & Price, C. J. (2005). Structural covariance in the human cortex. Journal of Neuroscience, 25(36), 8303-8310.
Mei, T., Llera, A., Floris, D., Forde N., Tillmann, J., Durston, S., Moessnang, C., Banaschewski, T., Holt, R., Baron-Cohen, S., Rausch, A., Loth, E., Dell'Acqua, F., Charman, T., Murphy, D., Ecker, C., Beckmann, C. F., & Buiterlaar, J. F. (2020). Gray matter covariations and core symptoms of autism: The EU-AIMS Longitudinal European Autism Project. Molecular Autism, 11, 86.
Moberg, P. J., Richman, M. J., Roalf, D. R., Morse, C. L., Graefe, A. C., Brennan, L., Vickers, K., Tsering, W., Kamath, V., Turetsky, B. I., Gur, R. C., & Gur, R. E. (2018). Neurocognitive functioning in patients with 22q11.2 deletion syndrome: A meta-analytic review. Behavior Genetics, 48(4), 259-270.
Neufeld, N. H., Kaczkurkin, A. N., Sotiras, A., Mulsant, B. H., Dickie, E. W., Flint, A. J., Meyers, B. S., Alexopoulos, G. S., Rothschild, A. J., Whyte, E. M., Mah, L., Nierenberg, J., Hoptman, M. J., Davatzikos, C., Satterthwaite, T. D., & Voineskos, A. N. (2020). Structural brain networks in remitted psychotic depression. Neuropsychopharmacology, 45(7), 1223-1231.
Park, H., Quide, Y., Schofield, P. R., Williams, L. M., & Gatt, J. M. (2022). Grey matter covariation and the role of emotion reappraisal in mental wellbeing and resilience after early life stress exposure. Translational Psychiatry, 12, 85.
Piervincenzi, C., Fanella, M., Petsas, N., Frascarelli, M., Morano, A., Accinni, T., di Fabio, F., di Bonaventura, C., Berardelli, A., & Pantano, P. (2022). Structural cerebellar abnormalities and parkinsonism in patients with 22q11.2 deletion syndrome. Brain Sciences, 12(11), 1533.
Pomponio, R., Erus, G., Habes, M., Doshi, J., Srinivasan, D., Mamourian, E., Bashyam, V., Nasrallah, I. M., Satterthwaite, T. D., Fan, Y., Launer, L. J., Masters, C. L., Maruff, P., Zhuo, C., Völzke, H., Johnson, S. C., Fripp, J., Koutsouleris, N., Wolf, D. H., … Davatzikos, C. (2020). Harmonization of large MRI datasets for the analysis of brain imaging patterns throughout the lifespan. NeuroImage, 208, 116450.
Pontillo, M., Menghini, D., & Vicari, S. (2019). Neurocognitive profile and onset of psychosis symptoms in children, adolescents and young adults with 22q11 deletion syndrome: A longitudinal study. Schizophrenia Research, 208, 76-81.
Raichle, M. E. (2015). The brain's default mode network. Annual Review of Neuroscience, 38(25), 433-447.
Rakic, P. (1988). Specification of cerebral cortical areas. Science, 241(4862), 170-176.
Rakic, P. (1995). Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America, 92(25), 11323-11327.
Sandini, C., Scariati, E., Padula, M. C., Schneider, M., Schaer, M., van de Ville, D., & Eliez, S. (2018). Cortical dysconnectivity measured by structural covariance is associated with the presence of psychotic symptoms in 22q11.2 deletion syndrome. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(5), 433-442.
Schmitt, J. E., Vandekar, S., Yi, J., Calkins, M. E., Ruparel, K., Roalf, D. R., Whinna, D., Souders, M. C., Satterthwaite, T. D., Prabhakaran, K., McDonald-McGinn, D. M., Zackai, E. H., Gur, R. C., Emanuel, B. S., & Gur, R. E. (2015). Aberrant cortical morphometry in the 22q11.2 deletion syndrome. Biological Psychiatry, 78(2), 135-143.
Schmitt, J. E., DeBevits, J., Roalf, D., Ruparel, K., Gallagher, R. S., Gur, R. C., Alexander-Bloch, A., Emo, T., Alam, S., Steinberg, J., Akers, W., Khairy, K., Crowley, T. B., Emanuel, B., Zakharenko, S. S., McDonadl-McGinn, D. M., & Gur, R. E. (2022). A comprehensive analysis of cerebellar volumes in the 22q11.2 deletion syndrome. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 8(1), 79-90.
Seitz-Holland, J., Lyons, M., Kushan, L., Lin, A., Villalon-Reina, J. E., Cho, K., Zhang, F., Billah, T., Bouix, S., Kubicki, M., Bearden, C. E., & Pasternak, O. (2021). Opposing white matter microstructure abnormalities in 22q11.2 deletion and duplication carriers. Translational Psychiatry, 11, 580.
Shashi, V., Kwapil, T. R., Kaczorowski, J., Berry, M. N., Santos, C. S., Howard, T. D., Goradia, D., Prasad, K., Vaibhav, D., Rajarethinam, R., Spence, E., & Keshavan, M. S. (2010). Evidence of gray matter reduction and dysfunction in chromosome 22q11.2 deletion syndrome. Psychiatry Research: Neuroimaging, 181(1), 1-8.
Simon, T. J., Ding, L., Bish, J. P., McDonald-McGinn, D. M., Zackai, E. H., & Gee, J. (2005). Volumetric, connective, and morphologic changes in the brains of children with chromosome 22q11.2 deletion syndrome: An integrative study. NeuroImage, 25(1), 169-180.
Simon, T. J., Bearden, C. E., McDonald-McGinn, D., & Zackai, E. (2005). Visuospatial and numerical cognitive deficits in children with chromosome 22q11.2 deletion syndrome. Cortex, 41(2), 145-155.
Sotiras, A., Resnick, S. M., & Davatzikos, C. (2015). Finding imaging patterns of structural covariance via non-negative matrix factorization. NeuroImage, 108, 1-16.
Sotiras, A., Toledo, J. B., Gur, R. E., Gur, R. C., Satterthwaite, T. D., & Davatzikos, C. (2017). Patterns of coordinated cortical remodeling during adolescence and their associations with functional specialization and evolutionary expansion. Proceedings of the National Academy of Sciences of the United States of America, 114(13), 3527-3532.
Steenwijk, M. D., Geurts, J. J. G., Daams, M., Tijms, B. M., Wink, A. M., Balk, L. J., Tewarie, P. K., Uitdehaag, B. M. J., Barkhof, F., Vrenken, H., & Pouwels, P. J. W. (2015). Cortical atrophy patterns in multiple sclerosis are non-random and clinically relevant. Brain, 139(1), 115-126.
Sun, D., Ching, C. R. K., Lin, A., Forsyth, J. K., Kushan, L., Vajdi, A., Jalbrzikowski, M., Hansen, L., Villalon-Reina, J. E., Qu, X., Jonas, R. K., van Amelsvoort, T., Bakker, G., Kates, W. R., Antshel, K. M., Fremont, W., Campbell, L. E., McCabe, K. L., Daly, E., … Bearden, C. E. (2020). Large-scale mapping of cortical alterations in 22q11.2 deletion syndrome: Convergence with idiopathic psychosis and effects of deletion size. Molecular Psychiatry, 25, 1822-1834.
Sun, D., Rakesh, G., Haswell, C. C., Logue, M., Baird, C. L., O'Leary, E. N., Cotton, A. S., Xie, H., Tamburrino, M., Chen, T., Dennis, E. L., Jahanshad, N., Salminen, L. E., Thomopoulos, S. I., Rashid, F., Ching, C. R. K., Koch, S. B. J., Frijling, J. L., Nawijn, L., … Morey, R. A. (2022). A comparison of methods to harmonize cortical thickness measurements across scanners and sites. NeuroImage, 261, 119509.
Tan, G. M., Arnone, D., McIntosh, A. M., & Ebmeier, K. P. (2009). Meta-analysis of magnetic resonance imaging studies in chromosome 22q11.2 deletion syndrome (velocardiofacial syndrome). Schizophrenia Research, 115(2-3), 173-181.
Ten Donkelaar, H. J., den Dunnen, W., Lammens, M., Wesseling, P., Willemsen, M., & Hori, A. (2003). Development and developmental disorders of the human cerebellum. Journal of Neurology, 250(9), 1025-1036.
Thompson, E., Mohammadi-Nejad, A. R., Robinson, E. C., Andersson, J. L. R., Jbabdi, S., Glasser, M. F., Bastiani, M., & Sotiropoulos, S. N. (2020). Non-negative data-driven mapping of structural connections with application to the neonatal brain. NeuroImage, 222, 117273.
Thompson, P. M., Jahansha, N., Ching, C. R. K., Salminen, L., Thomopoulos, S., Bright, J., Baune, B., Bertolin, S., Bralten, J., Bruin, W., Bulow, R., Chen, J., Chye, Y., Dannlowski, U., de Kovel, C. G. F., Donohoe, G., Eyler, L., Faraone, S. V., Favre, P., … the ENIGMA Consortium. (2020). ENIGMA and global neuroscience: A decade of large-scale studies of the brain in health and disease across more than 40 countries. Translational Psychiatry, 10, 100.
Van Den Heuvel, E., Manders, E., Swillen, A., & Zink, I. (2018). Atypical language characteristics and trajectories in children with 22q11.2 deletion syndrome. Journal of Communication Disorders, 75, 37-56.
Villalón-Reina, J. E., Martínez, K., Qu, X., Ching, C. R. K., Nir, T. M., Kothapalli, D., Corbin, C., Sun, D., Lin, A., Forsyth, J. K., Kushan, L., Vajdi, A., Jalbrzikowski, M., Hansen, L., Jonas, R. K., van Amelsvoort, T., Bakker, G., Kates, W. R., Antshel, K. M., … Bearden, C. E. (2020). Altered white matter microstructure in 22q11. 2 deletion syndrome: A multisite diffusion tensor imaging study. Molecular Psychiatry, 25(11), 2818-2831.
Vorstman, J. A., Breetvelt, E., Duijff, S., Eliez, S., Schneider, M., Jalbrzikowski, M., Armando, M., Vicari, S., Shashi, V., Hooper, S. R., Chow, E. W. C., Fung, W. L. A., Butcher, N., Young, D. A., McDonald-McGinn, D. M., Vogels, A., van Amelsvoort, T., Gothelf, D., Weinberger, R., … Bassett, A. S. (2015). Cognitive decline preceding the onset of psychosis in patients with 22q11.2 deletion syndrome. JAMA Psychiatry, 72(4), 377-385.
Wang, N., Zeng, W., & Chen, L. (2012). A fast-FENICA method on resting state fMRI data. Journal of Neuroscience Methods, 209(1), 1-12.
Winkler, A. M., Kochunov, P., Blangero, J., Almasy, L., Zilles, K., Fox, P. T., Duggirala, R., & Glahn, D. C. (2010). Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. NeuroImage, 53(3), 1135-1146.
Woodin, M., Wang, P. P., Aleman, D., McDonald-McGinn, D., Zackai, E., & Moss, E. (2001). Neuropsychological profile of children and adolescents with the 22q11.2 microdeletion. Genetics in Medicine, 3(1), 34-39.
Xu, L., Groth, K. M., Pearlson, G., Schretlen, D. J., & Calhoun, V. D. (2009). Source-based morphometry: The use of independent component analysis to identify gray matter differences with application to schizophrenia. Human Brain Mapping, 30(3), 711-724.
Yarkoni, T., Poldrack, R. A., Nichols, T. E., van Essen, D. C., & Wager, T. D. (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 8(8), 665-670.
Zhao, Y., Guo, T., Fiksinski, A., Breetvelt, E., McDonald-McGinn, D. M., Crowley, T. B., Diacou, A., Schneider, M., Eliez, S., Swillen, A., Breckpot, J., Vermeesch, J., Chow, E. W. C., Gothelf, D., Duijff, S., Evers, R., van Amelsvoort, T. A., van den Bree, M., Owen, M., … International 22q11.2 Brain and Behavior Consortium. (2018). Variance of IQ is partially dependent on deletion type among 1,427 22q11.2 deletion syndrome subjects. American Journal of Medical Genetics-Part A, 176(10), 2172-2181.
Zielinski, B. A., Gennatas, E. D., Zhou, J., & Seeley, W. W. (2010). Network-level structural covariance in the developing brain. Proceedings of the National Academy of Sciences of the United States of America, 107(42), 18191-18196.