Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study.
MRI
anterior lobe
cerebellum
epilepsy
posterior lobe
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
27 Feb 2024
27 Feb 2024
Historique:
revised:
26
12
2023
received:
20
06
2023
accepted:
03
01
2024
medline:
27
2
2024
pubmed:
27
2
2024
entrez:
27
2
2024
Statut:
aheadofprint
Résumé
The intricate neuroanatomical structure of the cerebellum is of longstanding interest in epilepsy, but has been poorly characterized within the current corticocentric models of this disease. We quantified cross-sectional regional cerebellar lobule volumes using structural magnetic resonance imaging in 1602 adults with epilepsy and 1022 healthy controls across 22 sites from the global ENIGMA-Epilepsy working group. A state-of-the-art deep learning-based approach was employed that parcellates the cerebellum into 28 neuroanatomical subregions. Linear mixed models compared total and regional cerebellar volume in (1) all epilepsies, (2) temporal lobe epilepsy with hippocampal sclerosis (TLE-HS), (3) nonlesional temporal lobe epilepsy, (4) genetic generalized epilepsy, and (5) extratemporal focal epilepsy (ETLE). Relationships were examined for cerebellar volume versus age at seizure onset, duration of epilepsy, phenytoin treatment, and cerebral cortical thickness. Across all epilepsies, reduced total cerebellar volume was observed (d = .42). Maximum volume loss was observed in the corpus medullare (d We provide robust evidence of deep cerebellar and posterior lobe subregional gray matter volume loss in patients with chronic epilepsy. Volume loss was maximal for posterior subregions implicated in nonmotor functions, relative to motor regions of both the anterior and posterior lobe. Associations between cerebral and cerebellar changes, and variability of neuroanatomical profiles across epilepsy syndromes argue for more precise incorporation of cerebellar subregional damage into neurobiological models of epilepsy.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Swiss National Science Foundation
ID : 180365
Pays : Switzerland
Organisme : HCRW_
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S00355X/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0802012
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M00841X/1
Pays : United Kingdom
Organisme : NIH HHS
ID : R01 NS106957
Pays : United States
Organisme : NIH HHS
ID : RF1 NS033310
Pays : United States
Organisme : NIH HHS
ID : R01 NS1127524
Pays : United States
Organisme : NIH HHS
ID : R01MH116147
Pays : United States
Organisme : NIH HHS
ID : P41EB015922
Pays : United States
Organisme : NIH HHS
ID : R01AG058854
Pays : United States
Informations de copyright
© 2024 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.
Références
Thijs RD, Surges R, O'Brien TJ, Sander JW. Epilepsy in adults. Lancet. 2019;393(10172):689-701. https://doi.org/10.1016/s0140-6736(18)32596-0
Téllez-Zenteno JF, Hernández-Ronquillo L. A review of the epidemiology of temporal lobe epilepsy. Epilepsy Res Treat. 2012;2012:630853. https://doi.org/10.1155/2012/630853
Hatton SN, Huynh KH, Bonilha L, Abela E, Alhusaini S, Altmann A, et al. White matter abnormalities across different epilepsy syndromes in adults: an ENIGMA-epilepsy study. Brain. 2020;143(8):2454-2473. https://doi.org/10.1093/brain/awaa200
Whelan CD, Altmann A, Botía JA, Jahanshad N, Hibar DP, Absil J, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018;141(2):391-408. https://doi.org/10.1093/brain/awx341
Kandel A, Buzsáki G. Cerebellar neuronal activity correlates with spike and wave EEG patterns in the rat. Epilepsy Res. 1993;16(1):1-9. https://doi.org/10.1016/0920-1211(93)90033-4
Kros L, Lindeman S, Eelkman Rooda OHJ, Murugesan P, Bina L, Bosman LWJ, et al. Synchronicity and rhythmicity of Purkinje cell firing during generalized spike-and-wave discharges in a natural mouse model of absence epilepsy. Front Cell Neurosci. 2017;11:346. https://doi.org/10.3389/fncel.2017.00346
Krook-Magnuson E, Szabo GG, Armstrong C, Oijala M, Soltesz I. Cerebellar directed optogenetic intervention inhibits spontaneous hippocampal seizures in a mouse model of temporal lobe epilepsy. eNeuro. 2014;1(1):ENEURO.0005-14.2014. https://doi.org/10.1523/eneuro.0005-14.2014
Seto H, Shimizu M, Watanabe N, Wu Y, Kageyama M, Kamisaki Y, et al. Contralateral cerebellar activation in frontal lobe epilepsy detected by ictal Tc-99m HMPAO brain SPECT. Clin Nucl Med. 1997;22(3):194-195. https://doi.org/10.1097/00003072-199703000-00018
Bohnen NI, O'Brien TJ, Mullan BP, So EL. Cerebellar changes in partial seizures: clinical correlations of quantitative SPECT and MRI analysis. Epilepsia. 1998;39(6):640-650. https://doi.org/10.1111/j.1528-1157.1998.tb01433.x
Marcián V, Mareček R, Koriťáková E, Pail M, Bareš M, Brázdil M. Morphological changes of cerebellar substructures in temporal lobe epilepsy: a complex phenomenon, not mere atrophy. Seizure. 2018;54:51-57. https://doi.org/10.1016/j.seizure.2017.12.004
Sandok EK, O'Brien TJ, Jack CR, So EL. Significance of cerebellar atrophy in intractable temporal lobe epilepsy: a quantitative MRI study. Epilepsia. 2000;41(10):1315-1320. https://doi.org/10.1111/j.1528-1157.2000.tb04611.x
De Marcos FA, Ghizoni E, Kobayashi E, Li LM, Cendes F. Cerebellar volume and long-term use of phenytoin. Seizure. 2003;12(5):312-315. https://doi.org/10.1016/s1059-1311(02)00267-4
Hermann BP, Bayless K, Hansen R, Parrish J, Seidenberg M. Cerebellar atrophy in temporal lobe epilepsy. Epilepsy Behav. 2005;7(2):279-287. https://doi.org/10.1016/j.yebeh.2005.05.022
McDonald CR, Hagler DJ Jr, Ahmadi ME, Tecoma E, Iragui V, Dale AM, et al. Subcortical and cerebellar atrophy in mesial temporal lobe epilepsy revealed by automatic segmentation. Epilepsy Res. 2008;79(2-3):130-138. https://doi.org/10.1016/j.eplepsyres.2008.01.006
Oyegbile TO, Bayless K, Dabbs K, Jones J, Rutecki P, Pierson R, et al. The nature and extent of cerebellar atrophy in chronic temporal lobe epilepsy. Epilepsia. 2011;52(4):698-706. https://doi.org/10.1111/j.1528-1167.2010.02937.x
Hagemann G, Lemieux L, Free SL, Krakow K, Everitt AD, Kendall BE, et al. Cerebellar volumes in newly diagnosed and chronic epilepsy. J Neurol. 2002;249(12):1651-1658. https://doi.org/10.1007/s00415-002-0843-9
Marcián V, Filip P, Bareš M, Brázdil M. Cerebellar dysfunction and ataxia in patients with epilepsy: coincidence, consequence, or cause? Tremor Other Hyperkinet Mov (NY). 2016;6:376. https://doi.org/10.7916/d8kh0nbt
Bonilha L, Rorden C, Castellano G, Pereira F, Rio PA, Cendes F, et al. Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Arch Neurol. 2004;61(9):1379-1384. https://doi.org/10.1001/archneur.61.9.1379
Szabó CA, Lancaster JL, Lee S, Xiong JH, Cook C, Mayes BN, et al. MR imaging volumetry of subcortical structures and cerebellar hemispheres in temporal lobe epilepsy. AJNR Am J Neuroradiol. 2006;27(10):2155-2160.
Ibdali M, Hadjivassiliou M, Grünewald RA, Shanmugarajah PD. Cerebellar degeneration in epilepsy: a systematic review. Int J Environ Res Public Health. 2021;18(2):473. https://doi.org/10.3390/ijerph18020473
Keller SS, Wieshmann UC, Mackay CE, Denby CE, Webb J, Roberts N. Voxel based morphometry of grey matter abnormalities in patients with medically intractable temporal lobe epilepsy: effects of side of seizure onset and epilepsy duration. J Neurol Neurosurg Psychiatry. 2002;73(6):648-655. https://doi.org/10.1136/jnnp.73.6.648
Keller SS, Wilke M, Wieshmann UC, Sluming VA, Roberts N. Comparison of standard and optimized voxel-based morphometry for analysis of brain changes associated with temporal lobe epilepsy. NeuroImage. 2004;23(3):860-868. https://doi.org/10.1016/j.neuroimage.2004.07.030
Park KM, Han YH, Kim TH, Mun CW, Shin KJ, Ha SY, et al. Cerebellar white matter changes in patients with newly diagnosed partial epilepsy of unknown etiology. Clin Neurol Neurosurg. 2015;138:25-30. https://doi.org/10.1016/j.clineuro.2015.07.017
Riley JD, Franklin DL, Choi V, Kim RC, Binder DK, Cramer SC, et al. Altered white matter integrity in temporal lobe epilepsy: association with cognitive and clinical profiles. Epilepsia. 2010;51(4):536-545. https://doi.org/10.1111/j.1528-1167.2009.02508.x
Larsell O. The development of the cerebellum in man in relation to its comparative anatomy. J Comp Neurol. 1947;87(2):85-129. https://doi.org/10.1002/cne.900870203
Carass A, Cuzzocreo JL, Han S, Hernandez-Castillo CR, Rasser PE, Ganz M, et al. Comparing fully automated state-of-the-art cerebellum parcellation from magnetic resonance images. NeuroImage. 2018;183:150-172. https://doi.org/10.1016/j.neuroimage.2018.08.003
Han S, Carass A, He Y, Prince JL. Automatic cerebellum anatomical parcellation using U-net with locally constrained optimization. NeuroImage. 2020;218:116819. https://doi.org/10.1016/j.neuroimage.2020.116819
Ney GC, Lantos G, Barr WB, Schaul N. Cerebellar atrophy in patients with long-term phenytoin exposure and epilepsy. Arch Neurol. 1994;51(8):767-771. https://doi.org/10.1001/archneur.1994.00540200043014
Blümcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, et al. International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a task force report from the ILAE commission on diagnostic methods. Epilepsia. 2013;54(7):1315-1329. https://doi.org/10.1111/epi.12220
Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, et al. ILAE classification of the epilepsies: position paper of the ILAE commission for classification and terminology. Epilepsia. 2017;58(4):512-521. https://doi.org/10.1111/epi.13709
Kerestes R, Han S, Balachander S, Hernandez-Castillo C, Prince JL, Diedrichsen J, et al. A standardized pipeline for examining human cerebellar Grey matter morphometry using structural magnetic resonance imaging. J Vis Exp. 2022;(180). https://doi.org/10.3791/63340
R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2023.
Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex. 2005;15(11):1676-1689. https://doi.org/10.1093/cercor/bhi044
Satterthwaite FE. An approximate distribution of estimates of variance components. Biometrics. 1946;2(6):110-114.
Schmahmann JD. An emerging concept. The cerebellar contribution to higher function. Arch Neurol. 1991;48(11):1178-1187. https://doi.org/10.1001/archneur.1991.00530230086029
Schmahmann JD, Pandya DN. Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. J Comp Neurol. 1989;289(1):53-73. https://doi.org/10.1002/cne.902890105
Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322-2345. https://doi.org/10.1152/jn.00339.2011
King M, Hernandez-Castillo CR, Poldrack RA, Ivry RB, Diedrichsen J. Functional boundaries in the human cerebellum revealed by a multi-domain task battery. Nat Neurosci. 2019;22(8):1371-1378. https://doi.org/10.1038/s41593-019-0436-x
Guo CC, Tan R, Hodges JR, Hu X, Sami S, Hornberger M. Network-selective vulnerability of the human cerebellum to Alzheimer's disease and frontotemporal dementia. Brain. 2016;139(Pt 5):1527-1538. https://doi.org/10.1093/brain/aww003
Liang KJ, Carlson ES. Resistance, vulnerability and resilience: a review of the cognitive cerebellum in aging and neurodegenerative diseases. Neurobiol Learn Mem. 2020;170:106981. https://doi.org/10.1016/j.nlm.2019.01.004
Coan AC, Cendes F. Understanding the spectrum of temporal lobe epilepsy: contributions for the development of individualized therapies. Expert Rev Neurother. 2013;13(12):1383-1394. https://doi.org/10.1586/14737175.2013.857604
Bernhardt BC, Fadaie F, Liu M, Caldairou B, Gu S, Jefferies E, et al. Temporal lobe epilepsy: hippocampal pathology modulates connectome topology and controllability. Neurology. 2019;92(19):e2209-e2220. https://doi.org/10.1212/wnl.0000000000007447
Bernhardt BC, Bernasconi A, Liu M, Hong SJ, Caldairou B, Goubran M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol. 2016;80(1):142-153. https://doi.org/10.1002/ana.24691
Liu M, Concha L, Lebel C, Beaulieu C, Gross DW. Mesial temporal sclerosis is linked with more widespread white matter changes in temporal lobe epilepsy. Neuroimage Clin. 2012;1(1):99-105. https://doi.org/10.1016/j.nicl.2012.09.010
French JA, Bebin M, Dichter MA, Engel J Jr, Hartman AL, Jóźwiak S, et al. Antiepileptogenesis and disease modification: clinical and regulatory issues. Epilepsia Open. 2021;6(3):483-492. https://doi.org/10.1002/epi4.12526
Phuong TH, Houot M, Méré M, Denos M, Samson S, Dupont S. Cognitive impairment in temporal lobe epilepsy: contributions of lesion, localization and lateralization. J Neurol. 2021;268(4):1443-1452. https://doi.org/10.1007/s00415-020-10307-6