Spontaneous Entry into an Offline State during Wakefulness: A Mechanism 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.