Leveraging the resting brain to predict memory decline after temporal lobectomy.


Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
11 2023
Historique:
revised: 28 08 2023
received: 01 06 2023
accepted: 28 08 2023
medline: 7 11 2023
pubmed: 30 8 2023
entrez: 29 8 2023
Statut: ppublish

Résumé

Predicting memory morbidity after temporal lobectomy in patients with temporal lobe epilepsy (TLE) relies on indices of preoperative temporal lobe structural and functional integrity. However, epilepsy is increasingly considered a network disorder, and memory a network phenomenon. We assessed the utility of functional network measures to predict postoperative memory changes. Seventy-two adults with TLE (37 left/35 right) underwent preoperative resting-state functional magnetic resonance imaging and pre- and postoperative neuropsychological assessment. We compared functional connectivity throughout the memory network of each patient to a healthy control template (n = 19) to identify differences in global organization. A second metric indicated the degree of integration of the to-be-resected temporal lobe with the rest of the memory network. We included these measures in a linear regression model alongside standard clinical variables as predictors of memory change after surgery. Left TLE patients with more atypical memory networks, and with greater functional integration of the to-be-resected region with the rest of the memory network preoperatively, experienced the greatest decline in verbal memory after surgery. Together, these two measures explained 44% of variance in verbal memory change, outperforming standard clinical and demographic variables. None of the variables examined was associated with visuospatial memory change in patients with right TLE. Resting-state connectivity provides valuable information concerning both the integrity of to-be-resected tissue and functional reserve across memory-relevant regions outside of the to-be-resected tissue. Intrinsic functional connectivity has the potential to be useful for clinical decision-making regarding memory outcomes in left TLE, and more work is needed to identify the factors responsible for differences seen in right TLE.

Identifiants

pubmed: 37643922
doi: 10.1111/epi.17767
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3061-3072

Informations de copyright

© 2023 International League Against Epilepsy.

Références

Sherman EMS, Wiebe S, Fay-Mcclymont TB, Tellez-Zenteno J, Metcalfe A, Hernandez-Ronquillo L, et al. Neuropsychological outcomes after epilepsy surgery: systematic review and pooled estimates. Epilepsia. 2011;52(5):857-869. https://doi.org/10.1111/j.1528-1167.2011.03022.x
Harvey DJ, Naugle RI, Magleby J, Chapin JS, Najm IM, Bingaman W, et al. Relationship between presurgical memory performance on the Wechsler memory scale-III and memory change following temporal resection for treatment of intractable epilepsy. Epilepsy Behav. 2008;13(2):372-375. https://doi.org/10.1016/j.yebeh.2008.04.024
St-Laurent M, McCormick C, Cohn M, Mišić B, Giannoylis I, McAndrews MP. Using multivariate data reduction to predict postsurgery memory decline in patients with mesial temporal lobe epilepsy. Epilepsy Behav. 2014;31:220-227. https://doi.org/10.1016/j.yebeh.2013.09.043
Witt J-A, Coras R, Schramm J, Becker AJ, Elger CE, Blümcke I, et al. Relevance of hippocampal integrity for memory outcome after surgical treatment of mesial temporal lobe epilepsy. J Neurol. 2015;262(10):2214-2224. https://doi.org/10.1007/s00415-015-7831-3
Stasenko A, Kaestner E, Reyes A, Lalani SJ, Paul B, Hegde M, et al. Association between microstructural asymmetry of temporal lobe white matter and memory decline after anterior temporal lobectomy. Neurology. 2022;98(11):e1151-e1162. https://doi.org/10.1212/WNL.0000000000200047
Bonelli SB, Powell RHW, Yogarajah M, Samson RS, Symms MR, Thompson PJ, et al. Imaging memory in temporal lobe epilepsy: predicting the effects of temporal lobe resection. Brain. 2010;133(4):1186-1199. https://doi.org/10.1093/brain/awq006
Powell HWR, Richardson MP, Symms MR, Boulby PA, Thompson PJ, Duncan JS, et al. Preoperative fMRI predicts memory decline following anterior temporal lobe resection. J Neurol Neurosurg Psychiatry. 2007;79(6):686-693. https://doi.org/10.1136/jnnp.2007.115139
Rabin ML, Narayan VM, Kimberg DY, Casasanto DJ, Glosser G, Tracy JI, et al. Functional MRI predicts post-surgical memory following temporal lobectomy. Brain. 2004;127(10):2286-2298. https://doi.org/10.1093/brain/awh281
Barnett A, Audrain S, McAndrews MP. Applications of resting-state functional MR imaging to epilepsy. Neuroimaging Clin N Am. 2017;27(4):697-708. https://doi.org/10.1016/j.nic.2017.06.002
Bernhardt BC, Hong S, Bernasconi A, Bernasconi N. Imaging structural and functional brain networks in temporal lobe epilepsy. Front Hum Neurosci. 2013;7:1-14. https://doi.org/10.3389/fnhum.2013.00624
Bernhardt BC, Bonilha L, Gross DW. Network analysis for a network disorder: the emerging role of graph theory in the study of epilepsy. Epilepsy Behav. 2015;50:162-170. https://doi.org/10.1016/j.yebeh.2015.06.005
Barnett AJ, Reilly W, Dimsdale-Zucker HR, Mizrak E, Reagh Z, Ranganath C. Intrinsic connectivity reveals functionally distinct cortico-hippocampal networks in the human brain. Kaplan R, ed. PLOS Biol. 2021;19(6):e3001275. https://doi.org/10.1371/journal.pbio.3001275
McCormick C, Protzner AB, Barnett AJ, Cohn M, Valiante TA, McAndrews MP. Linking DMN connectivity to episodic memory capacity: what can we learn from patients with medial temporal lobe damage? NeuroImage Clin. 2014;5:188-196. https://doi.org/10.1016/j.nicl.2014.05.008
Roger E, Pichat C, Torlay L, David O, Renard F, Banjac S, et al. Hubs disruption in mesial temporal lobe epilepsy. A resting-state fMRI study on a language-and-memory network. Hum Brain Mapp. 2020;41(3):779-796. https://doi.org/10.1002/hbm.24839
Holmes M, Folley BS, Sonmezturk HH, Gore JC, Kang H, Abou-Khalil B, et al. Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp. 2014;35(3):735-744. https://doi.org/10.1002/hbm.22210
Doucet G, Osipowicz K, Sharan A, Sperling MR, Tracy JI. Extratemporal functional connectivity impairments at rest are related to memory performance in mesial temporal epilepsy. Hum Brain Mapp. 2013;34(9):2202-2216. https://doi.org/10.1002/hbm.22059
McCormick C, Quraan M, Cohn M, Valiante TA, McAndrews MP. Default mode network connectivity indicates episodic memory capacity in mesial temporal lobe epilepsy. Epilepsia. 2013;54(5):809-818. https://doi.org/10.1111/epi.12098
Barnett AJ, Man V, McAndrews MP. Parcellation of the hippocampus using resting functional connectivity in temporal lobe epilepsy. Front Neurol. 2019;10:1-12. https://doi.org/10.3389/fneur.2019.00920
Ives-Deliperi V, Butler JT. Mechanisms of cognitive impairment in temporal lobe epilepsy: a systematic review of resting-state functional connectivity studies. Epilepsy Behav. 2021;115:107686. https://doi.org/10.1016/j.yebeh.2020.107686
Doucet GE, He X, Sperling M, Sharan A, Tracy JI. Gray matter abnormalities in temporal lobe epilepsy: relationships with resting-state functional connectivity and episodic memory performance. Biagini G, ed. PLoS One. 2016;11(5):e0154660. https://doi.org/10.1371/journal.pone.0154660
Audrain S, McAndrews MP. Cognitive and functional correlates of accelerated long-term forgetting in temporal lobe epilepsy. Cortex. 2019;110:101-114. https://doi.org/10.1016/j.cortex.2018.03.022
Fleury M, Buck S, Binding LP, Caciagli L, Vos SB, Winston GP, et al. Episodic memory network connectivity in temporal lobe epilepsy. Epilepsia. 2022;63(10):2597-2622. https://doi.org/10.1111/epi.17370
Gaillard WD, Balsamo L, Xu B, Mckinney C, Papero PH, Weinstein S, et al. fMRI language task panel improves determination of language dominance. Neurology. 2004;63(8):1403-1408. https://doi.org/10.1212/01.WNL.0000141852.65175.A7
Barnett A, Marty-Dugas J, McAndrews MP. Advantages of sentence-level fMRI language tasks in presurgical language mapping for temporal lobe epilepsy. Epilepsy Behav. 2014;32:114-120. https://doi.org/10.1016/j.yebeh.2014.01.010
McAndrews MP, Barnett A. Clinical utility of resting state functional MRI. In: Habas C, editor. The neuroimaging of brain diseases: structural and functional advances. Cham: Springer International Publishing; 2018. p. 59-79. https://doi.org/10.1007/978-3-319-78926-2_3
Audrain S, Barnett AJ, McAndrews MP. Language network measures at rest indicate individual differences in naming decline after anterior temporal lobe resection. Hum Brain Mapp. 2018;39:4404-4419. https://doi.org/10.1002/hbm.24281
Dulay MF, Busch RM. Prediction of neuropsychological outcome after resection of temporal and extratemporal seizure foci. Neurosurg Focus. 2012;32(3):E4. https://doi.org/10.3171/2012.1.FOCUS11340
Binder JR, Sabsevitz DS, Swanson SJ, Hammeke TA, Raghavan M, Mueller WM. Use of preoperative functional MRI to predict verbal memory decline after temporal lobe epilepsy surgery. Epilepsia. 2008;49(8):1377-1394. https://doi.org/10.1111/j.1528-1167.2008.01625.x
Busch RM, Hogue O, Miller M, Ferguson L, McAndrews MP, Hamberger M, et al. Nomograms to predict verbal memory decline after temporal lobe resection in adults with epilepsy. Neurology. 2021;97(3):e263-e274. https://doi.org/10.1212/WNL.0000000000012221
Mansouri A, Fallah A, McAndrews MP, Cohn M, Mayor D, Andrade D, et al. Neurocognitive and seizure outcomes of selective Amygdalohippocampectomy versus anterior temporal lobectomy for mesial temporal lobe epilepsy. Epilepsy Res Treat. 2014;2014:1-8. https://doi.org/10.1155/2014/306382
Barnett AJ, Park MTM, Pipitone J, Chakravarty MM, McAndrews MP. Functional and structural correlates of memory in patients with mesial temporal lobe epilepsy. Front Neurol. 2015;6:1-9. https://doi.org/10.3389/fneur.2015.00103
Fan L, Li H, Zhuo J, Zhang Y, Wang J, Chen L, et al. The human Brainnetome Atlas: a new brain atlas based on connectional architecture. Cereb Cortex. 2016;26(8):3508-3526. https://doi.org/10.1093/cercor/bhw157
Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage. 2010;52(3):1059-1069. https://doi.org/10.1016/j.neuroimage.2009.10.003
Fornito A, Zalesky A, Breakspear M. Graph analysis of the human connectome: promise, progress, and pitfalls. Neuroimage. 2013;80:426-444. https://doi.org/10.1016/j.neuroimage.2013.04.087
Doucet G, Rider R, Taylor N, Skidmore C, Sharan A, Sperling M, et al. Presurgery resting-state local graph-theory measures predict neurocognitive outcomes after brain surgery in temporal lobe epilepsy. Epilepsia. 2015;56(4):517-526. https://doi.org/10.1111/epi.12936
Badre D, Wagner AD. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia. 2007;45(13):2883-2901. https://doi.org/10.1016/j.neuropsychologia.2007.06.015
Liakakis G, Nickel J, Seitz RJ. Diversity of the inferior frontal gyrus-a meta-analysis of neuroimaging studies. Behav Brain Res. 2011;225(1):341-347. https://doi.org/10.1016/j.bbr.2011.06.022
Berl MM, Balsamo LM, Xu B, Moore EN, Weinstein SL, Conry JA, et al. Seizure focus affects regional language networks assessed by fMRI. Neurology. 2005;65(10):1604-1611. https://doi.org/10.1212/01.wnl.0000184502.06647.28
Brázdil M, Zákopčan J, Kuba R, Fanfrdlová Z, Rektor I. Atypical hemispheric language dominance in left temporal lobe epilepsy as a result of the reorganization of language functions. Epilepsy Behav. 2003;4(4):414-419. https://doi.org/10.1016/S1525-5050(03)00119-7
Weber B, Wellmer J, Reuber M, Mormann F, Weis S, Urbach H, et al. Left hippocampal pathology is associated with atypical language lateralization in patients with focal epilepsy. Brain. 2006;129(2):346-351. https://doi.org/10.1093/brain/awh694
Figueiredo P, Santana I, Teixeira J, Cunha C, Machado E, Sales F, et al. Adaptive visual memory reorganization in right medial temporal lobe epilepsy. Epilepsia. 2008;49(8):1395-1408. https://doi.org/10.1111/j.1528-1167.2008.01629.x
Li H, Ji C, Zhu L, Huang P, Jiang B, Xu X, et al. Reorganization of anterior and posterior hippocampal networks associated with memory performance in mesial temporal lobe epilepsy. Clin Neurophysiol. 2017;128(5):830-838. https://doi.org/10.1016/j.clinph.2017.02.018
Cheung M-C, Chan AS, Lam JMK, Chan Y-L. Pre- and postoperative fMRI and clinical memory performance in temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 2009;80(10):1099-1106. https://doi.org/10.1136/jnnp.2009.173161
Powell HWR, Richardson MP, Symms MR, Boulby PA, Thompson PJ, Duncan JS, et al. Reorganization of verbal and nonverbal memory in temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsia. 2007;48(8):1512-1525. https://doi.org/10.1111/j.1528-1167.2007.01053.x
Bonelli SB, Thompson PJ, Yogarajah M, Powell RH, Samson RS, McEvoy AW, et al. Memory reorganization following anterior temporal lobe resection: a longitudinal functional MRI study. Brain. 2013;136(6):1889-1900. https://doi.org/10.1093/brain/awt105
Limotai C, McLachlan RS, Hayman-Abello S, Hayman-Abello B, Brown S, Bihari F, et al. Memory loss and memory reorganization patterns in temporal lobe epilepsy patients undergoing anterior temporal lobe resection, as demonstrated by pre-versus post-operative functional MRI. J Clin Neurosci. 2018;55:38-44. https://doi.org/10.1016/j.jocn.2018.06.020
Griffin S, Tranel D. Age of seizure onset, functional reorganization, and neuropsychological outcome in temporal lobectomy. J Clin Exp Neuropsychol. 2007;29(1):13-24. https://doi.org/10.1080/13803390500263568
Sidhu MK, Stretton J, Winston GP, Bartlett P, McEvoy AW, Symms MR, et al. Memory network plasticity after temporal lobe resection: a longitudinal functional imaging study. Brain. 2016;139(2):415-430. https://doi.org/10.1093/brain/awv365
Tononi G, Sporns O, Edelman GM. Measures of degeneracy and redundancy in biological networks. Proc Natl Acad Sci USA. 1999;96(6):3257-3262. https://doi.org/10.1073/pnas.96.6.3257
Morgan VL, Rogers BP, Anderson AW, Landman BA, Englot DJ. Divergent network properties that predict early surgical failure versus late recurrence in temporal lobe epilepsy. J Neurosurg. 2020;132(5):1324-1333. https://doi.org/10.3171/2019.1.JNS182875
Morgan VL, Sainburg LE, Johnson GW, Janson A, Levine KK, Rogers BP, et al. Presurgical temporal lobe epilepsy connectome fingerprint for seizure outcome prediction. Brain Commun. 2022;4(3):1-13. https://doi.org/10.1093/braincomms/fcac128
Carboni M, Rubega M, Iannotti GR, De Stefano P, Toscano G, Tourbier S, et al. The network integration of epileptic activity in relation to surgical outcome. Clin Neurophysiol. 2019;130(12):2193-2202. https://doi.org/10.1016/j.clinph.2019.09.006
Stasenko A, Kaestner E, Arienzo D, Schadler AJ, Helm JL, Shih JJ, et al. Preoperative white matter network organization and memory decline after epilepsy surgery. J Neurosurg. 2023;1-12. https://doi.org/10.3171/2023.4.JNS23347
Besson P, Dinkelacker V, Valabregue R, Thivard L, Leclerc X, Baulac M, et al. Structural connectivity differences in left and right temporal lobe epilepsy. Neuroimage. 2014;100:135-144. https://doi.org/10.1016/j.neuroimage.2014.04.071
Pittau F, Grova C, Moeller F, Dubeau F, Gotman J. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. Epilepsia. 2012;53(6):1013-1023. https://doi.org/10.1111/j.1528-1167.2012.03464.x
Chiang S, Stern JM, Engel J, Levin HS, Haneef Z. Differences in graph theory functional connectivity in left and right temporal lobe epilepsy. Epilepsy Res. 2014;108(10):1770-1781. https://doi.org/10.1016/j.eplepsyres.2014.09.023

Auteurs

Sam Audrain (S)

Division of Clinical and Computational Neuroscience, Krembil Research Institute, University Health Network, Toronto, Ontario, Canada.

Alexander Barnett (A)

Department of Psychology, University of Toronto, Toronto, Ontario, Canada.

Pedram Mouseli (P)

Division of Clinical and Computational Neuroscience, Krembil Research Institute, University Health Network, Toronto, Ontario, Canada.
Centre for Multimodal Sensorimotor and Pain Research, Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada.

Mary Pat McAndrews (MP)

Division of Clinical and Computational Neuroscience, Krembil Research Institute, University Health Network, Toronto, Ontario, Canada.
Department of Psychology, University of Toronto, Toronto, Ontario, Canada.

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