Atypical intrinsic neural timescales in temporal lobe epilepsy.
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
revised:
06
02
2023
received:
08
12
2022
accepted:
08
02
2023
medline:
14
4
2023
pubmed:
11
2
2023
entrez:
10
2
2023
Statut:
ppublish
Résumé
Temporal lobe epilepsy (TLE) is the most common pharmacoresistant epilepsy in adults. Here we profiled local neural function in TLE in vivo, building on prior evidence that has identified widespread structural alterations. Using resting-state functional magnetic resonance imaging (rs-fMRI), we mapped the whole-brain intrinsic neural timescales (INT), which reflect temporal hierarchies of neural processing. Parallel analysis of structural and diffusion MRI data examined associations with TLE-related structural compromise. Finally, we evaluated the clinical utility of INT. We studied 46 patients with TLE and 44 healthy controls from two independent sites, and mapped INT changes in patients relative to controls across hippocampal, subcortical, and neocortical regions. We examined region-specific associations to structural alterations and explored the effects of age and epilepsy duration. Supervised machine learning assessed the utility of INT for identifying patients with TLE vs controls and left- vs right-sided seizure onset. Relative to controls, TLE showed marked INT reductions across multiple regions bilaterally, indexing faster changing resting activity, with strongest effects in the ipsilateral medial and lateral temporal regions, and bilateral sensorimotor cortices as well as thalamus and hippocampus. Findings were similar, albeit with reduced effect sizes, when correcting for structural alterations. INT reductions in TLE increased with advancing disease duration, yet findings differed from the aging effects seen in controls. INT-derived classifiers discriminated patients vs controls (balanced accuracy, 5-fold: 76% ± 2.65%; cross-site, 72%-83%) and lateralized the focus in TLE (balanced accuracy, 5-fold: 96% ± 2.10%; cross-site, 95%-97%), with high accuracy and cross-site generalizability. Findings were consistent across both acquisition sites and robust when controlling for motion and several methodological confounds. Our findings demonstrate atypical macroscale function in TLE in a topography that extends beyond mesiotemporal epicenters. INT measurements can assist in TLE diagnosis, seizure focus lateralization, and monitoring of disease progression, which emphasizes promising clinical utility.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
998-1011Subventions
Organisme : NINDS NIH HHS
ID : R56 NS099348
Pays : United States
Informations de copyright
© 2023 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.
Références
Whelan CD, Altmann A, Botia 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.
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):2454-73.
Lariviere S, Rodríguez-Cruces R, Royer J, Caligiuri ME, Gambardella A, Concha L, et al. Network-based atrophy modeling in the common epilepsies: a worldwide ENIGMA study. Sci Adv. 2020;6(47):eabc6457.
Schindler KA, Bialonski S, Horstmann M-T, Elger CE, Lehnertz K. Evolving functional network properties and synchronizability during human epileptic seizures. Chaos. 2008;18(3):33119.
Pereira FRS, Alessio A, Sercheli MS, Pedro T, Bilevicius E, Rondina JM, et al. Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci. 2010;11(1):66.
Bernhardt BC, Bernasconi A, Liu M, Hong S-J, Caldairou B, Goubran M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol. 2016;80(1):142-53.
Li H, Ding F, Chen C, Huang P, Xu J, Chen Z, et al. Dynamic functional connectivity in modular organization of the hippocampal network marks memory phenotypes in temporal lobe epilepsy. Hum Brain Mapp. 2021;43(6):1917-29.
Lariviere S, Weng Y, Vos de Wael R, Royer J, Frauscher B, Wang Z, et al. Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and predictors of surgical outcome. Epilepsia. 2020;61(6):1221-33.
Yang S, Zhang Z, Chen H, Meng Y, Li J, Li Z, et al. Temporal variability profiling of the default mode across epilepsy subtypes. Epilepsia. 2021;62(1):61-73.
Maturana MI, Meisel C, Dell K, Karoly PJ, D'Souza W, Grayden DB, et al. Critical slowing down as a biomarker for seizure susceptibility. Nat Commun. 2020;11(1):2172.
Scheid BH, Ashourvan A, Stiso J, Davis KA, Mikhail F, Pasqualetti F, et al. Time-evolving controllability of effective connectivity networks during seizure progression. Proc Natl Acad Sci U S A. 2021;118(5):e2006436118.
Watanabe T, Rees G, Masuda N. Atypical intrinsic neural timescale in autism. Elife. 2019;8:e42256.
Gao R, van den Brink RL, Pfeffer T, Voytek B. Neuronal timescales are functionally dynamic and shaped by cortical microarchitecture. Elife. 2020;9:9e61277.
Wolff A, Berberian N, Golesorkhi M, Gomez-Pilar J, Zilio F, Northoff G. Intrinsic neural timescales: temporal integration and segregation. Trends Cogn Sci. 2022;26(2):159-73.
Raut RV, Snyder AZ, Raichle ME. Hierarchical dynamics as a macroscopic organizing principle of the human brain. Proc Natl Acad Sci U S A. 2020;117(34):20890-7.
Ito T, Hearne LJ, Cole MW. A cortical hierarchy of localized and distributed processes revealed via dissociation of task activations, connectivity changes, and intrinsic timescales. Neuroimage. 2020;221:117141.
Li S, Wang X-J. Hierarchical timescales in the neocortex: mathematical mechanism and biological insights. Proc Natl Acad Sci U S A. 2022;119(6):e2110274119.
Weng Y, Lariviere S, Caciagli L, Vos de Wael R, Rodriguez-Cruces R, Royer J, et al. Macroscale and microcircuit dissociation of focal and generalized human epilepsies. Commun Biol. 2020;3(1):244.
Fadaie F, Lee HM, Caldairou B, Gill RS, Sziklas V, Crane J, et al. Atypical functional connectome hierarchy impacts cognition in temporal lobe epilepsy. Epilepsia. 2021;62(11):2589-603.
Suárez LE, Markello RD, Betzel RF, Misic B. Linking structure and function in macroscale brain networks. Trends Cogn Sci. 2020;24(4):302-15.
Royer J, Rodríguez-Cruces R, Tavakol S, Lariviere S, Herholz P, Li Q, et al. An open MRI dataset for multiscale neuroscience. Sci Data. 2022;9(1):569.
Rodriguez-Cruces R, Bernhardt BC, Concha L. Multidimensional associations between cognition and connectome organization in temporal lobe epilepsy. Neuroimage. 2020;213:116706.
Bernasconi N, Bernasconi A, Caramanos Z, Antel SB, Andermann F, Arnold DL. Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region. Brain. 2003;126(Pt 2):462-9.
Cruces RR, Royer J, Herholz P, Lariviere S, de Wael RV, Paquola C, et al. Micapipe: a pipeline for multimodal neuroimaging and connectome analysis. Neuroimage. 2022;263:119612.
Wengler K, Goldberg AT, Chahine G, Horga G. Distinct hierarchical alterations of intrinsic neural timescales account for different manifestations of psychosis. Elife. 2020;9:e56151.
Bernhardt BC, Bernasconi N, Concha L, Bernasconi A. Cortical thickness analysis in temporal lobe epilepsy: reproducibility and relation to outcome. Neurology. 2010;74(22):1776-84.
Worsley KJ, Taylor JE, Carbonell F, Chung MK, Duerden E, Bernhardt B, et al. SurfStat: a Matlab toolbox for the statistical analysis of univariate and multivariate surface and volumetric data using linear mixed effects models and random field theory. Neuroimage. 2009;47:47S102.
Liu M, Bernhardt BC, Hong SJ, Caldairou B, Bernasconi A, Bernasconi N. The superficial white matter in temporal lobe epilepsy: a key link between structural and functional network disruptions. Brain. 2016;139(Pt 9):2431-40.
Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage. 2014;84:320-41.
Vos de Wael R, Benkarim O, Paquola C, Lariviere S, Royer J, Tavakol S, et al. BrainSpace: a toolbox for the analysis of macroscale gradients in neuroimaging and connectomics datasets. Commun Biol. 2020;3(1):103.
Burt JB, Helmer M, Shinn M, Anticevic A, Murray JD. Generative modeling of brain maps with spatial autocorrelation. Neuroimage. 2020;220:117038.
Lariviere S, Royer J, Rodríguez-Cruces R, Paquola C, Caligiuri ME, Gambardella A, et al. Structural network alterations in focal and generalized epilepsy assessed in a worldwide ENIGMA study follow axes of epilepsy risk gene expression. Nat Commun. 2022;13(1):4320.
Lariviere S, Paquola C, Park B-y, Royer J, Wang Y, Benkarim O, et al. The ENIGMA toolbox: multiscale neural contextualization of multisite neuroimaging datasets. Nat Methods. 2021;18:698-700.
Chang CC, Lin CJ. LIBSVM: a library for support vector machines. ACM Trans Intell Syst Technol. 2011;2(3):1-27.
Shinn M, Hu A, Turner L, Noble S, Preller KH, Ji JL, et al. Spatial and temporal autocorrelation weave complexity in brain networks. bioRxiv. 2022.
Paquola C, Bethlehem RA, Seidlitz J, Wagstyl K, Romero-Garcia R, Whitaker KJ, et al. Shifts in myeloarchitecture characterise adolescent development of cortical gradients. Elife. 2019;8:8.
Zeng H, Pizarro R, Nair VA, La C, Prabhakaran V. Alterations in regional homogeneity of resting-state brain activity in mesial temporal lobe epilepsy. Epilepsia. 2013;54(4):658-66.
Meisel C. Antiepileptic drugs induce subcritical dynamics in human cortical networks. Proc Natl Acad Sci U S A. 2020;117(20):11118-25.
Girardi-Schappo M, Fadaie F, Lee HM, Caldairou B, Sziklas V, Crane J, et al. Altered communication dynamics reflect cognitive deficits in temporal lobe epilepsy. Epilepsia. 2021;62(4):1022-33.
Pitkänen A, Sutula TP. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol. 2002;1(3):173-81.
Davis KA, Nanga RPR, Das S, Chen SH, Hadar PN, Pollard JR, et al. Glutamate imaging (GluCEST) lateralizes epileptic foci in nonlesional temporal lobe epilepsy. Sci Transl Med. 2015;7(309):309ra161.
Galovic M, van Dooren VQH, Postma T, Vos SB, Caciagli L, Borzi G, et al. Progressive cortical thinning in patients with focal epilepsy. JAMA Neurol. 2019;76(10):1230-9.
Akman CI, Ichise M, Olsavsky A, Tikofsky RS, Heertum RLV, Gilliam F. Epilepsy duration impacts on brain glucose metabolism in temporal lobe epilepsy: results of voxel-based mapping. Epilepsy Behav. 2010;17(3):373-80.
Kaestner E, Reyes A, Chen A, Rao J, Macari AC, Choi JY, et al. Atrophy and cognitive profiles in older adults with temporal lobe epilepsy are similar to mild cognitive impairment. Brain. 2021;144(1):236-50.
Tai XY, Koepp M, Duncan JS, Fox N, Thompson P, Baxendale S, et al. Hyperphosphorylated tau in patients with refractory epilepsy correlates with cognitive decline: a study of temporal lobe resections. Brain. 2016;139(9):2441-55.
Sisodiya SM, Whelan CD, Hatton SN, Huynh K, Altmann A, Ryten M, et al. The ENIGMA-epilepsy working group: mapping disease from large data sets. Hum Brain Mapp. 2022;43(1):113-28.
Gleichgerrcht E, Munsell BC, Alhusaini S, Alvim MKM, Bargalló N, Bender B, et al. Artificial intelligence for classification of temporal lobe epilepsy with ROI-level MRI data: a worldwide ENIGMA-epilepsy study. Neuroimage Clin. 2021;31:31102765.
Narasimhan S, Gonzalez HFJ, Johnson GW, Wills KE, Paulo DL, Morgan VL, et al. Functional connectivity between mesial temporal and default mode structures may help lateralize surgical temporal lobe epilepsy. J Neurosurg. 2022;137(6):1571-81.