Neural (re)organisation of language and memory: implications for neuroplasticity and cognition.

IF 7.5 1区 医学 Q1 CLINICAL NEUROLOGY Journal of Neurology, Neurosurgery, and Psychiatry Pub Date : 2025-04-10 DOI:10.1136/jnnp-2024-333871
Alena Stasenko, Erik Kaestner, Jonathan Rodriguez, Christopher Benjamin, F Scott Winstanley, Leigh Sepeta, Jessica Horsfall, Susan Y Bookheimer, Jerry J Shih, Marc A Norman, Amanda Gooding, Carrie R McDonald
{"title":"Neural (re)organisation of language and memory: implications for neuroplasticity and cognition.","authors":"Alena Stasenko, Erik Kaestner, Jonathan Rodriguez, Christopher Benjamin, F Scott Winstanley, Leigh Sepeta, Jessica Horsfall, Susan Y Bookheimer, Jerry J Shih, Marc A Norman, Amanda Gooding, Carrie R McDonald","doi":"10.1136/jnnp-2024-333871","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>In the presence of neurological insult, how language and memory networks jointly reorganise provides insights into mechanisms of neuroplasticity and can inform presurgical planning. As (re)organisation is often studied within a single cognitive modality, how language and memory interact during (re)organisation in response to epilepsy and the implications for memory outcomes is less clear. We investigated (1) the rates and patterns of joint (re)organisation and (2) their associations with pre- and postsurgical memory function.</p><p><strong>Methods: </strong>Individuals with epilepsy (n=162) from three neurosurgical centres underwent the Wada procedure. We examined colateralisation patterns (ie, concordance/discordance) between language and both global and verbal memory (n=34), and associations with clinical characteristics and preoperative and postoperative memory outcomes.</p><p><strong>Results: </strong>Overall concordance between language and memory colateralisation was minimal-to-weak across both global memory and verbal memory (kappa=0.28-0.44). Discordance was primarily observed in individuals with left-lateralised language, of whom 52% and 32% showed discordance in global and verbal memory, respectively. Discordance was most pronounced in left hemisphere epilepsy and mesial temporal sclerosis. Conversely, right-lateralised language consistently predicted right-lateralised memory (95%-100%), regardless of seizure laterality or memory type. While discordance was not associated with presurgical memory function, discordance predicted superior postsurgical memory outcomes following surgery in the language-dominant hemisphere (p<0.05; η<sub>p</sub> <sup>2</sup>=0.30).</p><p><strong>Conclusions: </strong>When language dominance is atypical, memory tends to colateralise. However, when language remains typical, concordance with memory is weak, particularly for left hemisphere seizure onset. An interhemispheric shift in language may trigger a shift in memory, possibly to maintain efficient communication between medial temporal and neocortical language networks. In contrast, memory appears able to reorganise in isolation, with discordance predicting better postsurgical memory outcomes without detriment to presurgical function. Our findings support the continued need for separate presurgical mapping of language and memory lateralisation, particularly in the case of typical language dominance and left hemisphere seizures.</p>","PeriodicalId":16418,"journal":{"name":"Journal of Neurology, Neurosurgery, and Psychiatry","volume":" ","pages":"489-499"},"PeriodicalIF":7.5000,"publicationDate":"2025-04-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12022876/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neurology, Neurosurgery, and Psychiatry","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1136/jnnp-2024-333871","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background: In the presence of neurological insult, how language and memory networks jointly reorganise provides insights into mechanisms of neuroplasticity and can inform presurgical planning. As (re)organisation is often studied within a single cognitive modality, how language and memory interact during (re)organisation in response to epilepsy and the implications for memory outcomes is less clear. We investigated (1) the rates and patterns of joint (re)organisation and (2) their associations with pre- and postsurgical memory function.

Methods: Individuals with epilepsy (n=162) from three neurosurgical centres underwent the Wada procedure. We examined colateralisation patterns (ie, concordance/discordance) between language and both global and verbal memory (n=34), and associations with clinical characteristics and preoperative and postoperative memory outcomes.

Results: Overall concordance between language and memory colateralisation was minimal-to-weak across both global memory and verbal memory (kappa=0.28-0.44). Discordance was primarily observed in individuals with left-lateralised language, of whom 52% and 32% showed discordance in global and verbal memory, respectively. Discordance was most pronounced in left hemisphere epilepsy and mesial temporal sclerosis. Conversely, right-lateralised language consistently predicted right-lateralised memory (95%-100%), regardless of seizure laterality or memory type. While discordance was not associated with presurgical memory function, discordance predicted superior postsurgical memory outcomes following surgery in the language-dominant hemisphere (p<0.05; ηp 2=0.30).

Conclusions: When language dominance is atypical, memory tends to colateralise. However, when language remains typical, concordance with memory is weak, particularly for left hemisphere seizure onset. An interhemispheric shift in language may trigger a shift in memory, possibly to maintain efficient communication between medial temporal and neocortical language networks. In contrast, memory appears able to reorganise in isolation, with discordance predicting better postsurgical memory outcomes without detriment to presurgical function. Our findings support the continued need for separate presurgical mapping of language and memory lateralisation, particularly in the case of typical language dominance and left hemisphere seizures.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
语言和记忆的神经(重新)组织:对神经可塑性和认知的影响。
背景:在存在神经损伤的情况下,语言和记忆网络如何共同重组提供了神经可塑性机制的见解,并可以为术前计划提供信息。由于(再)组织通常在单一认知模式下进行研究,语言和记忆在癫痫(再)组织过程中如何相互作用以及对记忆结果的影响尚不清楚。我们研究了(1)关节(再)组织的速率和模式,(2)它们与术前和术后记忆功能的关系。方法:来自三个神经外科中心的癫痫患者(n=162)接受了Wada手术。我们检查了语言与全局记忆和言语记忆之间的侧边模式(即一致性/不一致性)(n=34),以及与临床特征和术前和术后记忆结果的关联。结果:在整体记忆和言语记忆中,语言和记忆侧边化之间的总体一致性从最小到弱(kappa=0.28-0.44)。这种不一致主要发生在左偏侧语言的个体中,其中52%和32%的人在全局记忆和言语记忆方面分别表现出不一致。这种不一致在左半球癫痫和内侧颞叶硬化中最为明显。相反,无论癫痫发作的侧边性或记忆类型如何,右偏侧语言始终预测右偏侧记忆(95%-100%)。虽然不一致性与手术前记忆功能无关,但不一致性预测手术后语言优势半球的术后记忆结果(pp 2=0.30)。结论:当语言优势是非典型时,记忆倾向于附带。然而,当语言保持典型时,与记忆的一致性很弱,特别是在左半球癫痫发作时。语言的半球间转移可能引发记忆的转移,可能是为了维持内侧颞叶和新皮层语言网络之间的有效交流。相比之下,记忆似乎能够在孤立的情况下重组,不一致预示着更好的术后记忆结果,而不会损害手术前的功能。我们的研究结果支持手术前对语言和记忆侧化进行单独测绘的持续需求,特别是在典型的语言优势和左半球癫痫的情况下。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
CiteScore
15.70
自引率
1.80%
发文量
888
审稿时长
6 months
期刊介绍: The Journal of Neurology, Neurosurgery & Psychiatry (JNNP) aspires to publish groundbreaking and cutting-edge research worldwide. Covering the entire spectrum of neurological sciences, the journal focuses on common disorders like stroke, multiple sclerosis, Parkinson’s disease, epilepsy, peripheral neuropathy, subarachnoid haemorrhage, and neuropsychiatry, while also addressing complex challenges such as ALS. With early online publication, regular podcasts, and an extensive archive collection boasting the longest half-life in clinical neuroscience journals, JNNP aims to be a trailblazer in the field.
期刊最新文献
Adherence to the MIND diet and longitudinal brain structural changes over a decade: evidence from the Framingham heart study offspring cohort. Vitamin D intake and multiple sclerosis risk in the Norwegian Mother, Father and Child cohort. Metabolic profiles associated with fat loss in Parkinson's disease. Metabolic brain networks in dementia with Lewy bodies: from prodromal to manifest disease stages. Epilepsy-related premature mortality in adults with intellectual disability in England: a population-based analysis.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1