Brain network dynamics in transitions of consciousness reorganize according to task engagement

Abstract

SUMMARYSubstantial changes in behavior, physiology, and brain function occur when alertness decreases1– 5. These changes in brain function involve increased synchronization between cortical areas6,7as well as alterations in sensory processing pathways and networks connecting the thalamus and cortex5,8–11. Cognitive tasks engage overlapping functional networks with sensory pathways facilitating information processing12,13, and thalamocortical and corticocortical networks supporting task performance14,15. Frontoparietal circuits play a crucial role in cognitive tasks16and states of decreased consciousness17. To develop an integrated framework of consciousness and cognition, it is important to understand how fluctuations in alertness and cognitive processing interact in these shared circuits18. Our hypothesis is 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. Our findings demonstrated that as alertness decreased, passively listening to auditory tones led to increased synchronization 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 reveal the functional mechanisms of the brain’s flexible reorganization during transitions of consciousness when individuals are actively engaged in cognitive processes.