Stasenko Alena, Kaestner Erik, Rodriguez Jonathan, Benjamin Christopher, Winstanley F Scott, Sepeta Leigh, Horsfall Jessica, Bookheimer Susan Y, Shih Jerry J, Norman Marc A, Gooding Amanda, McDonald Carrie R
Ohio Health Rehabilitation Hospital, Columbus, Ohio, USA
Psychiatry, University of California San Diego, La Jolla, California, USA.
J Neurol Neurosurg Psychiatry. 2025 Apr 10;96(5):489-499. doi: 10.1136/jnnp-2024-333871.
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.
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.
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 =0.30).
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.
在存在神经损伤的情况下，语言和记忆网络如何共同重组有助于深入了解神经可塑性机制，并可为术前规划提供参考。由于（重新）组织通常是在单一认知模式内进行研究的，因此在癫痫发作后的（重新）组织过程中语言和记忆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）联合（重新）组织的速率和模式，以及（2）它们与术前和术后记忆功能的关联。
来自三个神经外科中心的癫痫患者（n = 162）接受了Wada测试。我们检查了语言与整体记忆和言语记忆之间的侧化模式（即一致性/不一致性）（n = 34），以及与临床特征和术前及术后记忆结果的关联。
在整体记忆和言语记忆中，语言与记忆侧化之间的总体一致性从最小到较弱（kappa = 0.28 - 0.44）。不一致主要出现在语言偏向左半球的个体中，其中分别有52%和32%的个体在整体记忆和言语记忆中表现出不一致。不一致在左半球癫痫和内侧颞叶硬化症中最为明显。相反，无论癫痫发作的侧别或记忆类型如何，语言偏向右半球始终预示着记忆也偏向右半球（95% - 100%）。虽然不一致与术前记忆功能无关，但不一致预示着在语言优势半球手术后记忆结果更好（p < 0.05；η = 0.30）。
当语言优势不典型时，记忆倾向于侧化。然而，当语言保持典型时，与记忆的一致性较弱，特别是对于左半球癫痫发作。语言的半球间转移可能会引发记忆的转移，这可能是为了维持内侧颞叶和新皮质语言网络之间的有效通信。相比之下，记忆似乎能够独立重组，不一致预示着术后记忆结果更好，而不会损害术前功能。我们的研究结果支持继续需要分别对语言和记忆侧化进行术前映射，特别是在典型语言优势和左半球癫痫发作的情况下。
