Furman University, Greenville, SC.
J Cogn Neurosci. 2023 Oct 1;35(10):1617-1634. doi: 10.1162/jocn_a_02035.
Traditionally, neuroscience and psychology have studied the human brain during periods of "online" attention to the environment, while participants actively engage in processing sensory stimuli. However, emerging evidence shows that the waking brain also intermittently enters an "offline" state, during which sensory processing is inhibited and our attention shifts inward. In fact, humans may spend up to half of their waking hours offline [Wamsley, E. J., & Summer, T. Spontaneous entry into an "offline" state during wakefulness: A mechanism of memory consolidation? Journal of Cognitive Neuroscience, 32, 1714-1734, 2020; Killingsworth, M. A., & Gilbert, D. T. A wandering mind is an unhappy mind. Science, 330, 932, 2010]. The function of alternating between online and offline forms of wakefulness remains unknown. We hypothesized that rapidly switching between online and offline states enables the brain to alternate between the competing demands of encoding new information and consolidating already-encoded information. A total of 46 participants (34 female) trained on a memory task just before a 30-min retention interval, during which they completed a simple attention task while undergoing simultaneous high-density EEG and pupillometry recording. We used a data-driven method to parse this retention interval into a sequence of discrete online and offline states, with a 5-sec temporal resolution. We found evidence for three distinct states, one of which was an offline state with features well-suited to support memory consolidation, including increased EEG slow oscillation power, reduced attention to the external environment, and increased pupil diameter (a proxy for increased norepinephrine). Participants who spent more time in this offline state following encoding showed improved memory at delayed test. These observations are consistent with the hypothesis that even brief, seconds-long entry into an offline state may support the early stages of memory consolidation.
传统上，神经科学和心理学研究的是人类大脑在“在线”注意环境的时期，而参与者积极地参与处理感官刺激。然而，新出现的证据表明，清醒的大脑也会间歇性地进入“离线”状态，在此期间，感官处理受到抑制，我们的注意力转向内部。事实上，人类可能会在清醒状态下有一半的时间处于离线状态[Wamsley，E.J.，Summer，T. 自发性进入清醒的“离线”状态：记忆巩固的一种机制？认知神经科学杂志，32，1714-1734，2020；Killingsworth，M.A.，Gilbert，D.T. 心不在焉的人是不快乐的人。科学，330，932，2010]。在线和离线两种清醒状态之间交替的功能仍然未知。我们假设，在快速切换在线和离线状态之间，大脑可以在编码新信息和巩固已经编码的信息之间交替，以应对竞争需求。共有 46 名参与者（34 名女性）在记忆任务前接受了训练，然后进行了 30 分钟的保持间隔，在此期间，他们在进行高密度 EEG 和瞳孔测量记录的同时完成了一项简单的注意力任务。我们使用一种数据驱动的方法，以 5 秒的时间分辨率将这段保持间隔解析为一系列离散的在线和离线状态。我们发现了三个不同状态的证据，其中一个是具有支持记忆巩固特征的离线状态，包括增加 EEG 慢波功率、减少对外界环境的注意力以及增加瞳孔直径（去甲肾上腺素增加的指标）。在编码后，更多时间处于这种离线状态的参与者在延迟测试中表现出更好的记忆。这些观察结果与以下假设一致，即即使是短暂的、几秒钟长的离线状态进入也可能支持记忆巩固的早期阶段。
