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Abstract 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.
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Effect of cognitive load on time spent offline during wakefulness
Abstract Humans continuously alternate between online attention to the current environment and offline attention to internally generated thought and imagery. This may be a fundamental feature of the waking brain, but remains poorly understood. Here, we took a data-driven approach to defining online and offline states of wakefulness, using machine learning methods applied to measures of sensory responsiveness, subjective report, electroencephalogram (EEG), and pupil diameter. We tested the effect of cognitive load on the structure and prevalence of online and offline states, hypothesizing that time spent offline would increase as cognitive load of an ongoing task decreased. We also expected that alternation between online and offline states would persist even in the absence of a cognitive task. As in prior studies, we arrived at a three-state model comprised of one online state and two offline states. As predicted, when cognitive load was high, more time was spent online. Also as predicted, the same three states were present even when participants were not performing a task. These observations confirm our method is successful at isolating seconds-long periods of offline time. Varying cognitive load may be a useful way to manipulate time spent in at least one of these offline states in future experimental studies.
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- PAR ID:
- 10489021
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Cerebral Cortex
- Volume:
- 34
- Issue:
- 2
- ISSN:
- 1047-3211
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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