Jordan, Denis
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Criticality creates a functional platform for network transitions between internal and external processing modes in the human brain
Continuous switching between internal and external modes in the brain appears important for generating models of the self and the world. However, how the brain transitions between these two modes remains unknown. We propose that a large synchronization fluctuation of brain networks, emerging only near criticality (i.e., a balanced state between order and disorder), spontaneously creates temporal windows with distinct preferences for integrating the network’s internal information or for processing external stimuli. Using a computational model, electroencephalography (EEG) analysis, and functional magnetic resonance imaging (fMRI) analysis during alterations of consciousness in humans, we report that synchronized and incoherent networks, respectively, bias toward internal and external information with specific network configurations. In the brain network model and EEG-based network, the network preferences are the most prominent at criticality and in conscious states associated with the bandwidth 4−12 Hz, with alternating functional network configurations. However, these network configurations are selectively disrupted in different states of consciousness such as general anesthesia, psychedelic states, minimally conscious states, and unresponsive wakefulness syndrome. The network preference for internal information integration is only significant in conscious states and psychedelic states, but not in other unconscious states, suggesting the importance of internal information integration in maintaining consciousness. The fMRI co-activation pattern analysis shows that functional networks that are sensitive to external stimuli–such as default mode, dorsal attentional, and frontoparietal networks–are activated in incoherent states, while insensitive networks, such as global activation and deactivation networks, are dominated in highly synchronized states. We suggest that criticality produces a functional platform for the brain’s capability for continuous switching between two modes, which is crucial for the emergence of consciousness.
Criticality creates a functional platform for network transitions between internal and external processing modes in the human brain
Continuous switching between internal and external modes in the brain appears important for generating models of the self and the world. However, how the brain transitions between these two modes remains unknown. We propose that a large synchronization fluctuation of brain networks, emerging only near criticality (i.e., a balanced state between order and disorder), spontaneously creates temporal windows with distinct preferences for integrating the network’s internal information or for processing external stimuli. Using a computational model, electroencephalography (EEG) analysis, and functional magnetic resonance imaging (fMRI) analysis during alterations of consciousness in humans, we report that synchronized and incoherent networks, respectively, bias toward internal and external information with specific network configurations. In the brain network model and EEG-based network, the network preferences are the most prominent at criticality and in conscious states associated with the bandwidth 4−12 Hz, with alternating functional network configurations. However, these network configurations are selectively disrupted in different states of consciousness such as general anesthesia, psychedelic states, minimally conscious states, and unresponsive wakefulness syndrome. The network preference for internal information integration is only significant in conscious states and psychedelic states, but not in other unconscious states, suggesting the importance of internal information integration in maintaining consciousness. The fMRI co-activation pattern analysis shows that functional networks that are sensitive to external stimuli–such as default mode, dorsal attentional, and frontoparietal networks–are activated in incoherent states, while insensitive networks, such as global activation and deactivation networks, are dominated in highly synchronized states. We suggest that criticality produces a functional platform for the brain’s capability for continuous switching between two modes, which is crucial for the emergence of consciousness.
Relationship of critical dynamics, functional connectivity, and states of consciousness in large-scale human brain networks
Recent modeling and empirical studies support the hypothesis that large-scale brain networks function near a critical state. Similar functional connectivity patterns derived from resting state empirical data and brain network models at criticality provide further support. However, despite the strong implication of a relationship, there has been no principled explanation of how criticality shapes the characteristic functional connectivity in large-scale brain networks. Here, we hypothesized that the network science concept of partial phase locking is the underlying mechanism of optimal functional connectivity in the resting state. We further hypothesized that the characteristic connectivity of the critical state provides a theoretical boundary to quantify how far pharmacologically or pathologically perturbed brain connectivity deviates from its critical state, which could enable the differentiation of various states of consciousness with a theory-based metric. To test the hypothesis, we used a neuroanatomically informed brain network model with the resulting source signals projected to electroencephalogram (EEG)-like sensor signals with a forward model. Phase lag entropy (PLE), a measure of phase relation diversity, was estimated and the topography of PLE was analyzed. To measure the distance from criticality, the PLE topography at a critical state was compared with those of the EEG data from baseline consciousness, isoflurane anesthesia, ketamine anesthesia, vegetative state/unresponsive wakefulness syndrome, and minimally conscious state. We demonstrate that the partial phase locking at criticality shapes the functional connectivity and asymmetric anterior-posterior PLE topography, with low (high) PLE for high (low) degree nodes. The topographical similarity and the strength of PLE differentiates various pharmacologic and pathologic states of consciousness. Moreover, this model-based EEG network analysis provides a novel metric to quantify how far a pharmacologically or pathologically perturbed brain network is away from critical state, rather than merely determining whether it is in a critical or non-critical state.