Disrupted directed connectivity along the cingulate cortex determines vigilance after sleep deprivation

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2013-10, Vol.79, p.213-222
• Main Authors: Piantoni, Giovanni, Cheung, Bing Leung P., Van Veen, Barry D., Romeijn, Nico, Riedner, Brady A., Tononi, Giulio, Van Der Werf, Ysbrand D., Van Someren, Eus J.W.
• Format: Article
• Language: English
• Subjects: Adult; Arousal; Biological and medical sciences; Brain; Brain Mapping; Cingulate cortex; Disorders of higher nervous function. Focal brain diseases. Central vestibular syndrome and deafness. Brain stem syndromes; EEG; Effective connectivity; Electroencephalography; Female; Fundamental and applied biological sciences. Psychology; Gyrus Cinguli - physiopathology; Humans; Male; Medical research; Medical sciences; Nerve Net - physiopathology; Nervous system (semeiology, syndromes); Neural Pathways - physiopathology; Neurology; Neuronal Plasticity; Noise; Resting state; Sleep deprivation; Sleep Deprivation - physiopathology; Sleep. Vigilance; Studies; Vertebrates: nervous system and sense organs; Vigilance
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2013.04.103

The cingulate cortex is regarded as the backbone of structural and functional connectivity of the brain. While its functional connectivity has been intensively studied, little is known about its effective connectivity, its modulation by behavioral states, and its involvement in cognitive performance. Given the previously reported effects on cingulate functional connectivity, we investigated how eye-closure and sleep deprivation changed cingulate effective connectivity, estimated from resting-state high-density electroencephalography (EEG) using a novel method to calculate Granger Causality directly in source space. Effective connectivity along the cingulate cortex was dominant in the forward direction. Eyes-open connectivity in the forward direction was greater compared to eyes-closed, in well-rested participants. The difference between eyes-open and eyes-closed connectivity was attenuated and no longer significant after sleep deprivation. Individual variability in the forward connectivity after sleep deprivation predicted subsequent task performance, such that those subjects who showed a greater increase in forward connectivity between the eyes-open and the eyes-closed periods also performed better on a sustained attention task. Effective connectivity in the opposite, backward, direction was not affected by whether the eyes were open or closed or by sleep deprivation. These findings indicate that the effective connectivity from posterior to anterior cingulate regions is enhanced when a well-rested subject has his eyes open compared to when they are closed. Sleep deprivation impairs this directed information flow, proportional to its deleterious effect on vigilance. Therefore, sleep may play a role in the maintenance of waking effective connectivity. •Effective connectivity on the cingulate cortex was calculated from EEG resting state.•Forward effective connectivity is higher than backward connectivity.•Eyes-open forward connectivity is higher than during the eyes-closed period.•This enhancement disappears and is no longer significant after sleep deprivation.•Forward connectivity after sleep deprivation correlates with the vigilance level.