Scalp and hippocampal sleep correlates of memory function in drug-resistant temporal lobe epilepsy.

IF 5.3 2区 医学 Q1 CLINICAL NEUROLOGY
Sleep Pub Date : 2024-02-08 DOI:10.1093/sleep/zsad228
Véronique Latreille, Tamir Avigdor, John Thomas, Joelle Crane, Viviane Sziklas, Marilyn Jones-Gotman, Birgit Frauscher
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Abstract

Seminal animal studies demonstrated the role of sleep oscillations such as cortical slow waves, thalamocortical spindles, and hippocampal ripples in memory consolidation. In humans, whether ripples are involved in sleep-related memory processes is less clear. Here, we explored the interactions between sleep oscillations (measured as traits) and general episodic memory abilities in 26 adults with drug-resistant temporal lobe epilepsy who performed scalp-intracranial electroencephalographic recordings and neuropsychological testing, including two analogous hippocampal-dependent verbal and nonverbal memory tasks. We explored the relationships between hemispheric scalp (spindles, slow waves) and hippocampal physiological and pathological oscillations (spindles, slow waves, ripples, and epileptic spikes) and material-specific memory function. To differentiate physiological from pathological ripples, we used multiple unbiased data-driven clustering approaches. At the individual level, we found material-specific cerebral lateralization effects (left-verbal memory, right-nonverbal memory) for all scalp spindles (rs > 0.51, ps < 0.01) and fast spindles (rs > 0.61, ps < 0.002). Hippocampal epileptic spikes and short pathological ripples, but not physiological oscillations, were negatively (rs > -0.59, ps < 0.01) associated with verbal learning and retention scores, with left lateralizing and antero-posterior effects. However, data-driven clustering failed to separate the ripple events into defined clusters. Correlation analyses with the resulting clusters revealed no meaningful or significant associations with the memory scores. Our results corroborate the role of scalp spindles in memory processes in patients with drug-resistant temporal lobe epilepsy. Yet, physiological and pathological ripples were not separable when using data-driven clustering, and thus our findings do not provide support for a role of sleep ripples as trait-like characteristics of general memory abilities in epilepsy.

耐药性颞叶癫痫患者头皮和海马睡眠与记忆功能的相关性。
开创性的动物实验证明了睡眠振荡(如皮层慢波、丘脑棘波和海马波纹)在记忆巩固中的作用。在人类中,波纹是否参与了与睡眠相关的记忆过程还不太清楚。在这里,我们对26名患有耐药性颞叶癫痫的成年人进行了头皮-颅内脑电图记录和神经心理学测试,包括两项类似的依赖海马的言语和非言语记忆任务,探讨了睡眠振荡(以性状测量)与一般外显记忆能力之间的相互作用。我们探讨了半球头皮(棘波、慢波)和海马生理性和病理性振荡(棘波、慢波、波纹和癫痫尖峰)与特定材料记忆功能之间的关系。为了区分生理性和病理性波纹,我们使用了多种无偏的数据驱动聚类方法。在个体水平上,我们发现所有头皮棘波(rs > 0.51,ps < 0.01)和快速棘波(rs > 0.61,ps < 0.002)具有特定材料的大脑侧化效应(左侧言语记忆,右侧非言语记忆)。海马癫痫棘波和短病理波纹(而非生理振荡)与言语学习和保持得分呈负相关(rs > -0.59,ps <0.01),并具有左侧化和前-后效应。然而,数据驱动的聚类未能将波纹事件分离成确定的群组。对由此产生的聚类进行的相关性分析表明,这些聚类与记忆得分之间没有任何有意义或显著的关联。我们的研究结果证实了头皮棘波在耐药性颞叶癫痫患者记忆过程中的作用。然而,在使用数据驱动聚类时,生理波纹和病理波纹无法分离,因此我们的研究结果并不支持睡眠波纹作为癫痫患者一般记忆能力的特征。
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来源期刊
Sleep
Sleep 医学-临床神经学
CiteScore
10.10
自引率
10.70%
发文量
1134
审稿时长
3 months
期刊介绍: SLEEP® publishes findings from studies conducted at any level of analysis, including: Genes Molecules Cells Physiology Neural systems and circuits Behavior and cognition Self-report SLEEP® publishes articles that use a wide variety of scientific approaches and address a broad range of topics. These may include, but are not limited to: Basic and neuroscience studies of sleep and circadian mechanisms In vitro and animal models of sleep, circadian rhythms, and human disorders Pre-clinical human investigations, including the measurement and manipulation of sleep and circadian rhythms Studies in clinical or population samples. These may address factors influencing sleep and circadian rhythms (e.g., development and aging, and social and environmental influences) and relationships between sleep, circadian rhythms, health, and disease Clinical trials, epidemiology studies, implementation, and dissemination research.
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