Brain network dynamics in the wake-sleep transition reorganize according to task engagement.

Abstract

Alertness fluctuations and cognitive processing comprise overlapping brain circuits that include frontoparietal, thalamocortical, and sensory pathways. It is unclear how these brain circuits can simultaneously support such disparate but foundational human processes. To develop an integrated framework of consciousness and cognition, it is important to understand how fluctuations in alertness and cognitive processing interact in their shared circuits. In this electroencephalography (EEG)-functional magnetic resonance imaging (fMRI) study, we assessed individuals who fluctuated between alert and drowsy states while engaged in either an active or passive auditory task. We hypothesized that during periods of low alertness, individuals who actively maintain task engagement would recruit additional frontoparietal and sensory processing networks, while thalamocortical dynamics that typically change during sleep onset would remain unaffected. We found that when alertness decreased, passively listening to auditory tones led to increased synchronization primarily in the parietal lobe, whereas actively performing an auditory task resulted in increased long-range frontoparietal synchronization. During decreasing alertness, passive listening (but not active task engagement) was associated with widespread increased synchronization between the thalamus and cortex. In contrast, active task engagement (but not passive listening) led to increased synchronization between the auditory cortex and the rest of the brain. These results suggest the brain's capacity for flexible functional reorganization when alertness levels decline but cognitive processes persist. The brain patterns that support transitions of consciousness at sleep onset also reflect ongoing cognitive task demands.