The network is more important than the node: stereo-EEG evidence of neurocognitive networks in epilepsy

Nicholas W. G. Murray, Anthony C. Kneebone, Petra L. Graham, Chong H. Wong, Greg Savage, Lisa Gillinder, Michael W. K. Fong
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Abstract

Neuropsychological assessment forms an integral part of the presurgical evaluation for patients with medically refractory focal epilepsy. Our understanding of cognitive impairment in epilepsy is based on seminal lesional studies that have demonstrated important structure-function relationships within the brain. However, a growing body of literature demonstrating heterogeneity in the cognitive profiles of patients with focal epilepsy (e.g., temporal lobe epilepsy; TLE) has led researchers to speculate that cognition may be impacted by regions outside the seizure onset zone, such as those involved in the interictal or “irritative” network.Neuropsychological data from 48 patients who underwent stereoelectroencephalography (SEEG) monitoring between 2012 and 2023 were reviewed. Patients were categorized based on the site of seizure onset, as well as their irritative network, to determine the impact of wider network activity on cognition. Neuropsychological data were compared with normative standards (i.e., z = 0), and between groups.There were very few distinguishing cognitive features between patients when categorized based purely on the seizure onset zone (i.e., frontal lobe vs. temporal lobe epilepsy). In contrast, patients with localized irritative networks (i.e., frontal or temporal interictal epileptiform discharges [IEDs]) demonstrated more circumscribed profiles of impairment compared with those demonstrating wider irritative networks (i.e., frontotemporal IEDs). Furthermore, the directionality of propagation within the irritative network was found to influence the manifestations of cognitive impairment.The findings suggest that neuropsychological assessment is sensitive to network activity beyond the site of seizure onset. As such, an overly focal interpretation may not accurately reflect the distribution of the underlying pathology. This has important implications for presurgical work-up in epilepsy, as well as subsequent surgical outcomes.
网络比节点更重要:癫痫患者神经认知网络的立体电子脑电图证据
神经心理学评估是药物难治性局灶性癫痫患者术前评估不可或缺的一部分。我们对癫痫认知障碍的认识基于开创性的病变研究,这些研究证明了大脑内部重要的结构与功能关系。然而,越来越多的文献显示,局灶性癫痫(如颞叶癫痫)患者的认知特征具有异质性,这让研究人员推测,认知可能会受到发作起始区以外区域的影响,例如那些参与发作间期或 "刺激性 "网络的区域。根据发作开始的部位及其刺激性网络对患者进行分类,以确定更广泛的网络活动对认知的影响。神经心理学数据与常模标准(即 z = 0)进行了比较,并在组间进行了比较。相比之下,具有局部刺激性网络(即额叶或颞叶发作间期癫痫样放电 [IEDs])的患者与具有较广泛刺激性网络(即额颞叶 IEDs)的患者相比,表现出更多的障碍特征。研究结果表明,神经心理学评估对癫痫发作部位以外的网络活动非常敏感。因此,过于聚焦的解释可能无法准确反映潜在病理的分布。这对癫痫的术前检查和后续手术结果都有重要影响。
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