Abstract
Consciousness is an emergent property of the complex brain network. In order to understand how consciousness is constructed, neural interactions within this network must be elucidated. Previous studies have shown that specific neural interactions between the thalamus and frontoparietal cortices; frontal and parietal cortices; and parietal and temporal cortices are correlated with levels of consciousness. However, due to technical limitations, the network underlying consciousness has not been investigated in terms of large-scale interactions with high temporal and spectral resolution. In this study, we recorded neural activity with dense electrocorticogram (ECoG) arrays and used the spectral Granger causality to generate a more comprehensive network that relates to consciousness in monkeys. We found that neural interactions were significantly different between conscious and unconscious states in all combinations of cortical region pairs. Furthermore, the difference in neural interactions between conscious and unconscious states could be represented in 4 frequency-specific large-scale networks with unique interaction patterns: 2 networks were related to consciousness and showed peaks in alpha and beta bands, while the other 2 networks were related to unconsciousness and showed peaks in theta and gamma bands. Moreover, networks in the unconscious state were shared amongst 3 different unconscious conditions, which were induced either by ketamine and medetomidine, propofol, or sleep. Our results provide a novel picture that the difference between conscious and unconscious states is characterized by a switch in frequency-specific modes of large-scale communications across the entire cortex, rather than the cessation of interactions between specific cortical regions.
Highlights
As humans, we experience stable consciousness while we are awake but lose this conscious state during sleep
We found that neural interactions between cortical regions that fell into a specific spectral domain drastically changed between conscious and unconscious states, indicating that the unique frequencyspecific modes of large-scale region interactions over the entire cortex might be the fingerprint of conscious versus unconscious states
To extract/construct the sustained network of neural interactions from the recorded neural data, we pooled the ECoG data with a 120-sec time length (200 ms × 600) from the data set collected on different experimental days, and calculated a single model of spectral Granger causality for all of individual pairs of bipolar signals (See Figure 1B and methods)
Summary
We experience stable consciousness while we are awake but lose this conscious state during sleep. One intriguing hypothesis aimed to explain the neural mechanism underlying consciousness and unconsciousness, is that neural integration within the brain generates the conscious state, while the loss of the integration is responsible for producing the unconscious state [1,2,3,4] This “integration theory” has been evaluated by quantifying neural interactions in the brain, and previous studies have confirmed the reduction of neural interaction occurring under the unconscious state by using various measurements ranging from functional imaging [5,6,7] to electroencephalography (EEG) [8,9,10,11]. Compared to bottom-up interactions, top-down interactions from the frontal to the parietal cortices [9,11,12] were more correlated with the conscious state
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