Neurology; Neurology (clinical); Cellular and Molecular Neuroscience
Abstract :
[en] Alterations in subcortical brain regions are linked to motor and non-motor symptoms in Parkinson's disease (PD). However, associations between clinical expression and regional morphological abnormalities of the basal ganglia, thalamus, amygdala and hippocampus are not well established. We analyzed 3D T1-weighted brain MRI and clinical data from 2525 individuals with PD and 1326 controls from 22 global sources in the ENIGMA-PD consortium. We investigated disease effects using mass univariate and multivariate models on the medial thickness of 27,120 vertices of seven bilateral subcortical structures. Shape differences were observed across all Hoehn and Yahr (HY) stages, as well as correlations with motor and cognitive symptoms. Notably, we observed incrementally thinner putamen from HY1, caudate nucleus and amygdala from HY2, hippocampus, nucleus accumbens, and thalamus from HY3, and globus pallidus from HY4-5. Subregions of the thalami were thicker in HY1 and HY2. Largely congruent patterns were associated with a longer time since diagnosis and worse motor symptoms and cognitive performance. Multivariate regression revealed patterns predictive of disease stage. These cross-sectional findings provide new insights into PD subcortical degeneration by demonstrating patterns of disease stage-specific morphology, largely consistent with ongoing degeneration.
Disciplines :
Neurology Radiology, nuclear medicine & imaging
Author, co-author :
Laansma, Max A ; Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands. m.laansma@amsterdamumc.nl ; Amsterdam Neuroscience, Neurodegeneration, Amsterdam, The Netherlands. m.laansma@amsterdamumc.nl
Zhao, Yuji; Department of Biomedical Engineering, Illinois Institute of Technology, Chicago, IL, USA
van Heese, Eva M ; Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands ; Amsterdam Neuroscience, Neurodegeneration, Amsterdam, The Netherlands
Bright, Joanna K; Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
Owens-Walton, Conor ; Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA
Al-Bachari, Sarah; Faculty of Health and Medicine, The University of Lancaster, Lancaster, UK ; Department of Neurology, Royal Preston Hospital, Preston, UK
Anderson, Tim J ; Department of Medicine, University of Otago, Christchurch, Christchurch, New Zealand ; New Zealand Brain Research Institute, Christchurch, New Zealand ; Neurology Department, Te Wahtu Ora-Health New Zealand Waitaha Canterbury, Christchurch, New Zealand
Assogna, Francesca; Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation, Rome, Italy
van Balkom, Tim D; Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands ; Amsterdam Neuroscience, Neurodegeneration, Amsterdam, The Netherlands ; Amsterdam UMC, Department Psychiatry, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
Berendse, Henk W; Amsterdam UMC, Department Neurology, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
Cendes, Fernando; Department of Neurology, University of Campinas-UNICAMP, Campinas, Brazil ; Brazilian Institute of Neuroscience and Neurotechnology, Campinas, Brazil
Dalrymple-Alford, John C ; New Zealand Brain Research Institute, Christchurch, New Zealand ; School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand
Debove, Ines; Department of Neurology, Inselspital, University of Bern, Bern, Switzerland
Dirkx, Michiel F ; Department of Neurology and Center of Expertise for Parkinson & Movement Disorders, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
Druzgal, Jason; Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA, USA
Emsley, Hedley C A; Lancaster Medical School, Lancaster University, Lancaster, UK ; Division of Neuroscience and Experimental Psychology, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester Academic Health Science Centre, Manchester, UK
Fouche, Jean-Paul; Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Garraux, Gaëtan ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie du système nerveux
Guimarães, Rachel P; Department of Neurology, University of Campinas-UNICAMP, Campinas, Brazil ; Brazilian Institute of Neuroscience and Neurotechnology, Campinas, Brazil
Helmich, Rick C; Department of Neurology and Center of Expertise for Parkinson & Movement Disorders, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, The Netherlands ; Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands
Hu, Michele; Division of Clinical Neurology, Department of Clinical Neurosciences, Oxford Parkinson's Disease Centre, Nuffield, University of Oxford, Oxford, UK
van den Heuvel, Odile A; Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands ; Amsterdam Neuroscience, Neurodegeneration, Amsterdam, The Netherlands ; Amsterdam UMC, Department Psychiatry, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
Isaev, Dmitry; Department of Biomedical Engineering, Duke University, Durham, NC, USA
Kim, Ho-Bin; Department of Neurology & Neurological Sciences, Stanford University, Palo Alto, CA, USA
Klein, Johannes C ; Division of Clinical Neurology, Department of Clinical Neurosciences, Oxford Parkinson's Disease Centre, Nuffield, University of Oxford, Oxford, UK
Lochner, Christine; SA MRC Unit on Risk and Resilience in Mental Disorders, Department of Psychiatry, Stellenbosch University, Cape Town, South Africa
McMillan, Corey T; University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA
Melzer, Tracy R ; Department of Medicine, University of Otago, Christchurch, Christchurch, New Zealand ; New Zealand Brain Research Institute, Christchurch, New Zealand ; School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand
Newman, Benjamin ; Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA, USA
Parkes, Laura M ; Division of Psychology, Communication and Human Neuroscience, School of Health Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, UK ; Geoffrey Jefferson Brain Research Centre, Manchester Academic Health Science Centre, Northern Care Alliance & University of Manchester, Manchester, UK
Pellicano, Clelia; Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation, Rome, Italy
Piras, Fabrizio; Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation, Rome, Italy
Pitcher, Toni L; Department of Medicine, University of Otago, Christchurch, Christchurch, New Zealand ; New Zealand Brain Research Institute, Christchurch, New Zealand
Poston, Kathleen L ; Department of Neurology & Neurological Sciences, Stanford University, Palo Alto, CA, USA
Rango, Mario; Excellence Center for Advanced MR Techniques and Parkinson's Disease Center, Neurology unit, Fondazione IRCCS Cà Granda Maggiore Policlinico Hospital, University of Milan, Milan, Italy ; Department of Neurosciences, Neurology Unit, Fondazione Ca' Granda, IRCCS, Ospedale Policlinico, Univeristy of Milan, Milano, Italy
Ribeiro, Leticia F; Department of Neurology, University of Campinas-UNICAMP, Campinas, Brazil ; Brazilian Institute of Neuroscience and Neurotechnology, Campinas, Brazil
Rocha, Cristiane S; Department of Neurology, University of Campinas-UNICAMP, Campinas, Brazil ; Brazilian Institute of Neuroscience and Neurotechnology, Campinas, Brazil
Rummel, Christian; Support Center for Advanced Neuroimaging, (SCAN) University Institute of Diagnostic and Interventional Neuroradiology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
Santos, Lucas S R; Department of Neurology, University of Campinas-UNICAMP, Campinas, Brazil ; Brazilian Institute of Neuroscience and Neurotechnology, Campinas, Brazil
Schmidt, Reinhold; Department of Neurology, Medical University of Graz, Graz, Austria
Schwingenschuh, Petra ; Department of Neurology, Medical University of Graz, Graz, Austria
Squarcina, Letizia; Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy
Stein, Dan J ; SA MRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry and Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Vecchio, Daniela; Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation, Rome, Italy
Vriend, Chris ; Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands ; Amsterdam UMC, Department Psychiatry, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands ; Amsterdam Neuroscience, Brain Imaging, Amsterdam, The Netherlands
Wang, Jiunjie; Department of Medical Imaging and Radiological Sciences, Chang Gung University, Taoyuan City, Taiwan ; Department of Diagnostic Radiology, Chang Gung Memorial Hospital, Keelung Branch, Keelung City, Taiwan ; Healthy Ageing Research Center, Chang Gung University, Taoyuan City, Taiwan
Weintraub, Daniel; University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA
Wiest, Roland; Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, University Hospital Bern, Bern, Switzerland
Yasuda, Clarissa L ; Department of Neurology, University of Campinas-UNICAMP, Campinas, Brazil ; Brazilian Institute of Neuroscience and Neurotechnology, Campinas, Brazil
Jahanshad, Neda; Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA
Thompson, Paul M; Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA
van der Werf, Ysbrand D ; Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands ; Amsterdam Neuroscience, Neurodegeneration, Amsterdam, The Netherlands
Gutman, Boris A; Department of Biomedical Engineering, Illinois Institute of Technology, Chicago, IL, USA
MJFF - Michael J. Fox Foundation for Parkinson's Research FNIH - Foundation for the National Institutes of Health NINDS - National Institute of Neurological Disorders and Stroke
A. Draoui O. El Hiba A. Aimrane A. El Khiat H. Gamrani Parkinson’s disease: from bench to bedside Rev. Neurol. 2020 176 543 559 1:STN:280:DC%2BB3Mbpt1aksA%3D%3D 31928746
F. Nemmi U. Sabatini O. Rascol P. Péran Parkinson’s disease and local atrophy in subcortical nuclei: insight from shape analysis Neurobiol. Aging 2015 36 424 433 25174648
R.A.L. Menke K. Szewczyk‐Krolikowski Comprehensive morphometry of subcortical grey matter structures in early‐stage Parkinson’s disease Hum. Brain Mapp. 2014 35 1681 1690 23861334
H.M. Lee et al. Subcortical grey matter changes in untreated, early stage Parkinson’s disease without dementia Parkinsonism Relat. Disord. 2014 20 622 626 24703894
N.W. Sterling et al. Striatal shape in Parkinson’s disease Neurobiol. Aging 2013 34 2510 2516 23820588 3742686
S. Rahayel et al. Brain atrophy in Parkinson’s disease with polysomnography-confirmed REM sleep behavior disorder Sleep 2019 42 zsz062 30854555 6559168
E.M. Nyberg et al. Morphologic changes in the mesolimbic pathway in Parkinson’s disease motor subtypes Parkinsonism Relat. Disord. 2015 21 536 540 25817514 4424152
J.J. Tanner N.R. McFarland C.C. Price Striatal and hippocampal atrophy in idiopathic Parkinson’s disease patients without dementia: a morphometric analysis Front. Neurol. 2017 8 139 28450849 5389981
S.J. Chung et al. Subcortical shape analysis of progressive mild cognitive impairment in Parkinson’s disease Mov. Disord. 2017 32 1447 1456 28737237
E. Mak N. Bergsland M.G. Dwyer R. Zivadinov N. Kandiah Subcortical atrophy is associated with cognitive impairment in mild Parkinson disease: a combined investigation of volumetric changes, cortical thickness, and vertex-based shape analysis AJNR Am. J. Neuroradiol. 2014 35 2257 2264 1:STN:280:DC%2BC2cbnslOhtw%3D%3D 25082821 7965324
Devignes, Q. et al. Posterior cortical cognitive deficits are associated with structural brain alterations in mild cognitive impairment in Parkinson’s disease. Front. Aging Neurosci. https://doi.org/10.3389/fnagi.2021.668559 (2021).
A. Garg S. Appel-Cresswell K. Popuri M.J. McKeown M.F. Beg Morphological alterations in the caudate, putamen, pallidum, and thalamus in Parkinson’s disease Front. Neurosci. 2015 9 101 25873854 4379878
H.C. Baggio et al. Resting-state frontostriatal functional connectivity in Parkinson’s disease-related apathy Mov. Disord. 2015 30 671 679 25600482
M.E. Caligiuri et al. Alterations of putaminal shape in de novo Parkinson’s disease Mov. Disord. 2016 31 676 683 1:CAS:528:DC%2BC28XnsVWjsLw%3D 26879753
N. D’Cruz et al. Thalamic morphology predicts the onset of freezing of gait in Parkinson’s disease NPJ Parkinsons Dis. 2021 7 20 33654103 7925565
S. Gazzina et al. Subcortical matter in the α-synucleinopathies spectrum: an MRI pilot study J. Neurol. 2016 263 1575 1582 1:CAS:528:DC%2BC28XovVaisL8%3D 27230856
L. Gong et al. Striatum shape hypertrophy in early stage Parkinson’s disease with excessive daytime sleepiness Front. Neurosci. 2019 13 1353 31992965
L. Hopes et al. Magnetic resonance imaging features of the nigrostriatal system: Biomarkers of Parkinson’s disease stages? PLoS One 2016 11 e0147947 27035571 4818028
M.J. McKeown et al. Shape (but not volume) changes in the thalami in Parkinson disease BMC Neurol. 2008 8 18412976 2386499
Peralta, M., Baxter, J. S. H., Khan, A. R., Haegelen, C. & Jannin, P. Striatal shape alteration as a staging biomarker for Parkinson’s disease. Neuroimage Clin. https://doi.org/10.1016/j.nicl.2020.102272 (2020).
R. Prashanth S.D. Roy P.K. Mandal S. Ghosh High-accuracy classification of Parkinson’s disease through shape analysis and surface fitting in 123I-Ioflupane SPECT imaging IEEE J. Biomed. Health Inf. 2017 21 794 802 1:STN:280:DC%2BC1c7otlyjsw%3D%3D
L.J. de Schipper et al. Regional structural hippocampal differences between dementia with Lewy bodies and Parkinson’s disease J. Parkinsons Dis. 2019 9 775 783 31524178 6839604
D. Sigirli et al. Statistical shape analysis of putamen in early-onset Parkinson’s disease Clin. Neurol. Neurosurg. 2021 209 106936 34530266
S. Sivaranjini C.M. Sujatha Morphological analysis of subcortical structures for assessment of cognitive dysfunction in Parkinson’s disease using multi-atlas based segmentation Cogn. Neurodyn. 2021 15 835 845 1:STN:280:DC%2BB2cnls1Kqug%3D%3D 34603545 8448821
G. Vervoort et al. Structural brain alterations in motor subtypes of Parkinson’s disease: evidence from probabilistic tractography and shape analysis PLoS One 2016 11 e0157743 27314952 4912098
G. Varoquaux V. Cheplygina Machine learning for medical imaging: methodological failures and recommendations for the future NPJ Digit Med. 2022 5 48 35413988 9005663
M.A. Laansma et al. International multicenter analysis of brain structure across clinical stages of Parkinson’s disease Mov. Disord. 2021 36 2583 2594 34288137 8595579
Y.J. Zhao et al. Progression of Parkinson’s disease as evaluated by Hoehn and Yahr stage transition times Mov. Disord. 2010 25 710 716 20213822
E. Sarasso F. Agosta N. Piramide M. Filippi Progression of grey and white matter brain damage in Parkinson’s disease: a critical review of structural MRI literature J. Neurol. 2021 268 3144 3179 32378035
S.J. Chung et al. Patterns of striatal dopamine depletion in early Parkinson’s disease: prognostic relevance Neurology 2020 95 e280 e290 1:CAS:528:DC%2BB3cXhsFOisr%2FN 32616674
M. Oh et al. Subregional patterns of preferential striatal dopamine transporter loss differ in Parkinson’s disease, progressive supranuclear palsy, and multiple-system atrophy J. Nucl. Med. 2012 53 399 406 1:CAS:528:DC%2BC38XlvVGhurs%3D 22323779
S.J. Kish K. Shannak O. Hornykiewicz Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease. Pathophysiologic and clinical implications N. Engl. J. Med. 1988 318 876 880 1:STN:280:DyaL1c7nsV2jtg%3D%3D 3352672
O. Hornykiewicz Biochemical aspects of Parkinson’s disease Neurology 1998 51 S2 S9 1:CAS:528:DyaK1cXlsFeit7Y%3D 9711973
H. Braak E. Ghebremedhin U. Rüb H. Bratzke K. Del Tredici Stages in the development of Parkinson’s disease-related pathology Cell Tissue Res. 2004 318 121 134 15338272
M.A. Hely W.G.J. Reid M.A. Adena G.M. Halliday J.G.L. Morris The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years Mov. Disord. 2008 23 837 844 18307261
D. Aarsland et al. Cognitive decline in Parkinson’s disease Nat. Rev. Neurol. 2017 13 217 231 28257128 5643027
D. Aarsland et al. Parkinson’s disease-associated cognitive impairment Nat. Rev. Dis. Prim. 2021 7 47 34210995
X. Jia et al. Longitudinal study of gray matter changes in Parkinson’s disease AJNR Am. J. Neuroradiol. 2015 36 2219 2226 1:STN:280:DC%2BC283htFWksw%3D%3D 26359153 7964292
R.C. Helmich M.J.R. Janssen W.J.G. Oyen B.R. Bloem I. Toni Pallidal dysfunction drives a cerebellothalamic circuit into Parkinson’s tremor Ann. Neurol. 2011 69 269 281 21387372
C. Owens-Walton et al. Increased functional connectivity of thalamic subdivisions in patients with Parkinson’s disease PLoS One 2019 14 e0222002 1:CAS:528:DC%2BC1MXhvF2ju73J 31483847 6726201
J. Dong S. Hawes J. Wu W. Le H. Cai Connectivity and functionality of the globus pallidus externa under normal conditions and Parkinson’s disease Front. Neural Circuits 2021 15 645287 1:CAS:528:DC%2BB3MXhvFKjs77K 33737869 7960779
C.A. Ingham S.H. Hood M.J. Mijnster R.A. Baldock G.W. Arbuthnott Plasticity of striatopallidal terminals following unilateral lesion of the dopaminergic nigrostriatal pathway: a morphological study Exp. Brain Res. 1997 116 39 49 1:STN:280:DyaK2svkvFentg%3D%3D 9305813
C. Charroud L. Turella Subcortical grey matter changes associated with motor symptoms evaluated by the Unified Parkinson’s disease Rating Scale (part III): A longitudinal study in Parkinson’s disease Neuroimage Clin. 2021 31 102745 34225020 8264213
M.A. García-Cabezas B. Rico M.A. Sánchez-González C. Cavada Distribution of the dopamine innervation in the macaque and human thalamus Neuroimage 2007 34 965 984 17140815
Rüb, U., Del Tredici, K., Schultz, C. & Ghebremedhin, E. Parkinson’s disease: the thalamic components of the limbic loop are severely impaired by α-synuclein immunopositive inclusion body pathology. Neurobiol. Aging23, 245–254 (2002).
S. Haufe et al. On the interpretation of weight vectors of linear models in multivariate neuroimaging Neuroimage 2014 87 96 110 24239590
R. Nandhagopal et al. Longitudinal progression of sporadic Parkinson’s disease: a multi-tracer positron emission tomography study Brain 2009 132 2970 2979 1:STN:280:DC%2BD1MjhvVKnsg%3D%3D 19690093
Z.S. Nasreddine et al. The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment J. Am. Geriatr. Soc. 2005 53 695 699 15817019
C.G. Goetz et al. Movement Disorder Society-sponsored revision of the unified Parkinson’s Ddisease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results Mov. Disord. 2008 23 2129 2170 19025984
Daniel, H. Kosuke, I., Gary, K, & Elizabeth, A.S. MatchIt: nonparametric preprocessing for parametric causal inference. J. Stat. Softw. https://doi.org/10.18637/jss.v042.i08 (2011)
A.M. Dale B. Fischl M.I. Sereno Cortical surface-based analysis. I. Segmentation and surface reconstruction Neuroimage 1999 9 179 194 1:STN:280:DyaK1M7jt1Gisg%3D%3D 9931268
F. Ségonne et al. A hybrid approach to the skull stripping problem in MRI Neuroimage 2004 22 1060 1075 15219578
B. Fischl M.I. Sereno A.M. Dale Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system Neuroimage 1999 9 195 207 1:STN:280:DyaK1M7jt1Gisw%3D%3D 9931269
B. Fischl A. Liu A.M. Dale Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex IEEE Trans. Med. Imaging 2001 20 70 80 1:STN:280:DC%2BD3MzjvV2ksw%3D%3D 11293693
F. Ségonne J. Pacheco B. Fischl Geometrically accurate topology-correction of cortical surfaces using nonseparating loops IEEE Trans. Med. Imaging 2007 26 518 529 17427739
B. Fischl M.I. Sereno R.B. Tootell A.M. Dale High-resolution intersubject averaging and a coordinate system for the cortical surface Hum. Brain Mapp. 1999 8 272 284 1:STN:280:DC%2BD3c%2FosVCgug%3D%3D 10619420 6873338
Gutman, B. A., Wang, Y., Rajagopalan, P., Toga, A. W. Thompson, P. M. Shape matching with medial curves and 1-D group-wise registration. In 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI) 716–719 (IEEE, 2012).
Gutman, B. A., Madsen, S. K., Toga, A. W. & Thompson, P. M. A Family of fast spherical registration algorithms for cortical shapes. In Multimodal Brain Image Analysis 246–257 (Springer International Publishing, 2013).
B.A. Gutman et al. Proc. IEEE Int. Symp. Biomed. Imaging 2015 2015 1402 1406 26413211 4578221
D. Bates M. Mächler B. Bolker S. Walker Fitting linear mixed-effects models using lme4 J. Stat. Softw. 2015 67 1 48
C.G. Goetz G.T. Stebbins B.C. Tilley Calibration of unified Parkinson’s disease rating scale scores to Movement Disorder Society-unified Parkinson’s disease rating scale scores Mov. Disord. 2012 27 1239 1242 22886777
B.A. Gutman et al. A meta-analysis of deep brain structural shape and asymmetry abnormalities in 2,833 individuals with schizophrenia compared with 3,929 healthy volunteers via the ENIGMA Consortium Hum. Brain Mapp. 2022 43 352 372 34498337
A.F. Alexander-Bloch et al. On testing for spatial correspondence between maps of human brain structure and function Neuroimage 2018 178 540 551 29860082
Dohmatob, E. D., Gramfort, A., Thirion, B. & Varoquaux, G. Benchmarking solvers for TV-ℓ1 least-squares and logistic regression in brain imaging. 2014 International Workshop on Pattern Recognition in Neuroimaging (PRNI, Tübingen, 2014); https://doi.org/10.1109/prni.2014.6858516.
Nir, T. M. et al. Alzheimer’s disease classification with novel microstructural metrics from diffusion-weighted MRI. In Computational Diffusion MRI 41–54 (Springer International Publishing, Cham, 2016).
A. de Pierrefeu et al. Structured sparse principal components analysis with the TV-elastic net penalty IEEE Trans. Med. Imaging 2018 37 396 407 28880163
