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.

Moments of inattention to our surroundings may be essential to optimal cognitive functioning. Here, we investigated the hypothesis that humans spontaneously switch between two opposing attentional states during wakefulness—one in which we attend to the external environment (an “online” state) and one in which we disengage from the sensory environment to focus our attention internally (an “offline” state). We created a data-driven model of this proposed alternation between “online” and “offline” attentional states in humans, on a seconds-level timescale. Participants ( n = 34) completed a sustained attention to response task while undergoing simultaneous high-density EEG and pupillometry recording and intermittently reporting on their subjective experience. “Online” and “offline” attentional states were initially defined using a cluster analysis applied to multimodal measures of (1) EEG spectral power, (2) pupil diameter, (3) RT, and (4) self-reported subjective experience. We then developed a classifier that labeled trials as belonging to the online or offline cluster with >95% accuracy, without requiring subjective experience data. This allowed us to classify all 5-sec trials in this manner, despite the fact that subjective experience was probed on only a small minority of trials. We report evidence of statistically discriminable “online” and “offline” states matching the hypothesized characteristics. Furthermore, the offline state strongly predicted memory retention for one of two verbal learning tasks encoded immediately prior. Together, these observations suggest that seconds-timescale alternation between online and offline states is a fundamental feature of wakefulness and that this may serve a memory processing function.