Axmacher Nikolai, Elger Christian E, Fell Juergen
Department of Epileptology, University of Bonn, Sigmund-Freud-Str. 25, D-53105 Bonn, Germany.
Brain. 2008 Jul;131(Pt 7):1806-17. doi: 10.1093/brain/awn103. Epub 2008 May 24.
High-frequency oscillations (ripples) have been described in the hippocampus and rhinal cortex of both animals and human subjects and have been linked to replay and consolidation of previously acquired information. More specifically, studies in rodents suggested that ripples are generated in the hippocampus and are then transferred into the rhinal cortex, and that they occur predominantly during negative half waves of neocortical slow oscillations. Recordings in human epilepsy patients used either microelectrodes or foramen ovale electrodes; it is thus unclear whether macroelectrodes, which are routinely used for pre-surgical investigations, allow the recording of ripples as well. Furthermore, no direct link between ripples and behavioural performance has yet been established. Here, we recorded intracranial electroencephalogram with macroelectrodes from the hippocampus and rhinal cortex contralateral to the seizure onset zone in 11 epilepsy patients during a memory consolidation task while they were having an afternoon 'nap', i.e. a sleep period of approximately 1 h duration. We found that ripples could reliably be detected both in the hippocampus and in the rhinal cortex and had a similar frequency composition to events recorded previously with microelectrodes in humans. Results from cross-correlation analysis revealed that hippocampal events were closely locked to rhinal events and were consistent with findings on transmission of ripples from the hippocampus into the rhinal cortex. Furthermore, hippocampal ripples were significantly locked to the phase of hippocampal delta band activity, which might provide a mechanism for the reported phase-locking to neocortical slow oscillations. Ripples occurred with the highest incidence during periods when subjects lay awake during the nap time. Finally, we found that the number of rhinal, but not hippocampal, ripples was correlated with the number of successfully recalled items (post-nap) learned prior to sleep. These data confirm previous recordings in animals and humans, but move beyond them in several respects: they are the first recordings of ripples in humans during a cognitive task and suggest that ripples are indeed related to behavioural performance; furthermore, they propose a mechanism for phase-locking of ripples to neocortical slow waves via phase coupling to hippocampal delta activity; finally, they show that ripples can be recorded reliably with standard macroelectrodes in the human brain.
高频振荡（涟漪波）已在动物和人类受试者的海马体及鼻周皮质中被描述，并且与先前获取信息的重演和巩固有关。更具体地说，对啮齿动物的研究表明，涟漪波在海马体中产生，然后传递到鼻周皮质，并且它们主要发生在新皮质慢振荡的负半波期间。对人类癫痫患者的记录使用了微电极或卵圆孔电极；因此，尚不清楚常规用于术前检查的宏观电极是否也能记录涟漪波。此外，涟漪波与行为表现之间尚未建立直接联系。在此，我们在11名癫痫患者进行记忆巩固任务且处于下午“小憩”（即持续约1小时的睡眠期）时，使用宏观电极从癫痫发作起始区对侧的海马体和鼻周皮质记录了颅内脑电图。我们发现，在海马体和鼻周皮质中都能可靠地检测到涟漪波，并且其频率组成与先前在人类中使用微电极记录的事件相似。互相关分析结果显示，海马体事件与鼻周事件紧密相关，这与关于涟漪波从海马体传递到鼻周皮质的研究结果一致。此外，海马体涟漪波与海马体δ波段活动的相位显著相关，这可能为所报道的与新皮质慢振荡相位锁定提供一种机制。在小憩期间受试者清醒躺着的时候，涟漪波出现的频率最高。最后，我们发现，鼻周涟漪波的数量（而非海马体涟漪波的数量）与睡眠前学习的（午睡后）成功回忆项目的数量相关。这些数据证实了先前在动物和人类中的记录，但在几个方面超越了它们：它们是人类在认知任务期间首次记录到的涟漪波，并表明涟漪波确实与行为表现有关；此外，它们提出了一种通过与海马体δ活动的相位耦合使涟漪波与新皮质慢波相位锁定的机制；最后，它们表明在人类大脑中使用标准宏观电极能够可靠地记录涟漪波。
