Long-term neuroplasticity in language networks after anterior temporal lobe resection.

IF 6.6 1区 医学 Q1 CLINICAL NEUROLOGY
Epilepsia Pub Date : 2024-11-06 DOI:10.1111/epi.18147
Maria Sablik, Marine N Fleury, Lawrence P Binding, David P Carey, Giovanni d'Avossa, Sallie Baxendale, Gavin P Winston, John S Duncan, Meneka K Sidhu
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Abstract

Objective: Anterior temporal lobe resection (ATLR) is an effective treatment for drug-resistant temporal lobe epilepsy (TLE), although language deficits may occur after both left and right ATLR. Functional reorganization of the language network has been observed in the ipsilateral and contralateral hemispheres within 12 months after ATLR, but little is known of longer-term plasticity effects. Our aim was to examine the plasticity of language functions up to a decade after ATLR, in relation to cognitive profiles.

Methods: We examined 24 TLE patients (12 left [LTLE]) and 10 controls across four time points: pre-surgery, 4 months, 12 months, and ~9 years post-ATLR. Participants underwent standard neuropsychological assessments (naming, phonemic, and categorical fluency tests) and a verbal fluency functional magnetic resonance imaging (fMRI) task. Using a flexible factorial design, we analyzed longitudinal fMRI activations from 12 months to ~9 years post-ATLR, relative to controls, with separate analyses for people with hippocampal sclerosis (HS). Change in cognitive profiles was correlated with the long-term change in fMRI activations to determine the "efficiency" of reorganized networks.

Results: LTLE patients had increased long-term engagement of the left extra-temporal and contralateral temporal regions, with better language performance linked to bilateral activation. Those with HS exhibited more widespread bilateral activations. RTLE patients showed plasticity in the left extra-temporal regions, with better language outcomes associated with these areas. Both groups of patients achieved cognitive stability over 9 years, with more than 50% of LTLE patients improving. Older age, longer epilepsy duration, and lower pre-operative cognitive reserve negatively affected long-term language performance.

Significance: Neuroplasticity continues for up to ~9 years post-epilepsy surgery in LTLE and RTLE, with effective language recovery linked to bilateral engagement of temporal and extra-temporal regions. This adaptive reorganization is associated with improved cognitive outcomes, challenging the traditional view of localized surgery effects. These findings emphasize the need for early intervention, tailored pre-operative counseling, and the potential for continued cognitive gains with extended post-ATLR rehabilitation.

前颞叶切除术后语言网络的长期神经可塑性。
目的:前颞叶切除术(ATLR)是治疗耐药性颞叶癫痫(TLE)的有效方法,但左右颞叶切除术后都可能出现语言障碍。在ATLR术后12个月内,同侧和对侧大脑半球都观察到了语言网络的功能重组,但对长期的可塑性影响却知之甚少。我们的目的是研究 ATLR 后十年内语言功能的可塑性与认知特征的关系:我们对 24 名 TLE 患者(12 名左侧患者 [LTLE])和 10 名对照组患者进行了检查,共分为四个时间点:ATLR 术前、术后 4 个月、术后 12 个月和术后约 9 年。受试者接受了标准的神经心理学评估(命名、音位和分类流利性测试)和言语流利性功能磁共振成像(fMRI)任务。我们采用灵活的因子设计,分析了ATLR后12个月至约9年期间相对于对照组的纵向fMRI激活情况,并对海马硬化症(HS)患者进行了单独分析。认知概况的变化与fMRI激活的长期变化相关联,以确定重组网络的 "效率":结果:LTLE 患者左侧颞外和对侧颞区的长期参与度增加,语言能力的提高与双侧激活有关。HS患者则表现出更广泛的双侧激活。RTLE患者的左侧颞外区域表现出可塑性,语言成绩的提高与这些区域有关。两组患者的认知能力在9年内都趋于稳定,其中超过50%的LTLE患者的认知能力有所改善。年龄越大、癫痫持续时间越长、术前认知储备越低,对长期语言表现的影响越不利:LTLE和RTLE患者在癫痫手术后的神经可塑性可持续长达约9年,语言的有效恢复与颞区和颞外区的双侧参与有关。这种适应性重组与认知结果的改善有关,挑战了手术局部效应的传统观点。这些发现强调了早期干预、量身定制的术前咨询的必要性,以及通过延长ATLR术后康复来继续提高认知能力的潜力。
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来源期刊
Epilepsia
Epilepsia 医学-临床神经学
CiteScore
10.90
自引率
10.70%
发文量
319
审稿时长
2-4 weeks
期刊介绍: Epilepsia is the leading, authoritative source for innovative clinical and basic science research for all aspects of epilepsy and seizures. In addition, Epilepsia publishes critical reviews, opinion pieces, and guidelines that foster understanding and aim to improve the diagnosis and treatment of people with seizures and epilepsy.
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