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Predictors of long-term memory and network connectivity 10 years after anterior temporal lobe resection

Lookup NU author(s): Professor Peter TaylorORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2024 The Author(s). Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.Objective: Anterior temporal lobe resection (ATLR) effectively controls seizures in medically refractory temporal lobe epilepsy but risks significant episodic memory decline. Beyond 1 year postoperatively, the influence of preoperative clinical factors on episodic memory and long-term network plasticity remain underexplored. Ten years post-ATLR, we aimed to determine biomarkers of successful memory network reorganization and establish presurgical features' lasting impact on memory function. Methods: Twenty-five ATLR patients (12 left-sided) and 10 healthy controls underwent a memory-encoding functional magnetic resonance imaging paradigm alongside neuropsychometry 10 years postsurgery. Generalized psychophysiological interaction analyses modeled network functional connectivity of words/faces remembered, seeding from the medial temporal lobes (MTLs). Differences in successful memory connectivity were assessed between controls and left/right ATLR. Multivariate regressions and mixed-effect models probed preoperative phenotypes' effects on long-term memory outcomes. Results: Ten years post-ATLR, lower baseline functioning (verbal and performance intelligence quotient) and a focal memory impairment preoperatively predicted worse long-term memory outcomes. Poorer verbal memory was significantly associated with longer epilepsy duration and earlier onset age. Relative to controls, successful word and face encoding involved increased functional connectivity from both or remnant MTL seeds and contralesional parahippocampus/hippocampus after left/right ATLR. Irrespective of surgical laterality, successful memory encoding correlated with increased MTL-seeded connectivity to frontal (bilateral insula, right anterior cingulate), right parahippocampal, and bilateral fusiform gyri. Ten years postsurgery, better memory performance was correlated with contralateral frontal plasticity, which was disrupted with longer epilepsy duration. Significance: Our findings underscore the enduring nature of functional network reorganizations to provide long-term cognitive support. Ten years post-ATLR, successful memory formation featured stronger connections near resected areas and contralateral regions. Preoperative network disruption possibly influenced effectiveness of postoperative plasticity. These findings are crucial for enhancing long-term memory prediction and strategies for lasting memory rehabilitation.


Publication metadata

Author(s): Fleury MN, Binding LP, Taylor P, Xiao F, Giampiccolo D, Caciagli L, Buck S, Winston GP, Thompson PJ, Baxendale S, Koepp MJ, Duncan JS, Sidhu MK

Publication type: Article

Publication status: Published

Journal: Epilepsia

Year: 2024

Pages: epub ahead of print

Online publication date: 11/07/2024

Acceptance date: 25/06/2024

Date deposited: 24/07/2024

ISSN (print): 0013-9580

ISSN (electronic): 1528-1167

Publisher: John Wiley and Sons Inc

URL: https://doi.org/10.1111/epi.18058

DOI: 10.1111/epi.18058

Data Access Statement: Anonymized data are available upon request

PubMed id: 38990127


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Funding

Funder referenceFunder name
MRC (G0802012, MR/M00841X/1
MR/T04294X/1
MR/X031039/1
UCLH Biomedical Research Centre (grant 229811)
Wellcome Trust (grant 083148)
Wellcome Trust Innovation Program (106882/Z/15/Z, 218380/Z/19/Z)

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