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 ne...
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Frontiers Media S.A.
2021
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oai:doaj.org-article:318104445af34810bfca9c03e6b8073c2021-12-01T03:32:52ZCriticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain1662-513710.3389/fnsys.2021.657809https://doaj.org/article/318104445af34810bfca9c03e6b8073c2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fnsys.2021.657809/fullhttps://doaj.org/toc/1662-5137Continuous 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.Minkyung KimMinkyung KimHyoungkyu KimHyoungkyu KimZirui HuangZirui HuangGeorge A. MashourGeorge A. MashourGeorge A. MashourDenis JordanDenis JordanDenis JordanRüdiger IlgRüdiger IlgRüdiger IlgUnCheol LeeUnCheol LeeFrontiers Media S.A.articlecriticalityconsciousnessoscillator modelEEGfMRIbrain network transitionNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENFrontiers in Systems Neuroscience, Vol 15 (2021) |
| institution |
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| collection |
DOAJ |
| language |
EN |
| topic |
criticality consciousness oscillator model EEG fMRI brain network transition Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 |
| spellingShingle |
criticality consciousness oscillator model EEG fMRI brain network transition Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Minkyung Kim Minkyung Kim Hyoungkyu Kim Hyoungkyu Kim Zirui Huang Zirui Huang George A. Mashour George A. Mashour George A. Mashour Denis Jordan Denis Jordan Denis Jordan Rüdiger Ilg Rüdiger Ilg Rüdiger Ilg UnCheol Lee UnCheol Lee Criticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain |
| description |
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. |
| format |
article |
| author |
Minkyung Kim Minkyung Kim Hyoungkyu Kim Hyoungkyu Kim Zirui Huang Zirui Huang George A. Mashour George A. Mashour George A. Mashour Denis Jordan Denis Jordan Denis Jordan Rüdiger Ilg Rüdiger Ilg Rüdiger Ilg UnCheol Lee UnCheol Lee |
| author_facet |
Minkyung Kim Minkyung Kim Hyoungkyu Kim Hyoungkyu Kim Zirui Huang Zirui Huang George A. Mashour George A. Mashour George A. Mashour Denis Jordan Denis Jordan Denis Jordan Rüdiger Ilg Rüdiger Ilg Rüdiger Ilg UnCheol Lee UnCheol Lee |
| author_sort |
Minkyung Kim |
| title |
Criticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain |
| title_short |
Criticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain |
| title_full |
Criticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain |
| title_fullStr |
Criticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain |
| title_full_unstemmed |
Criticality Creates a Functional Platform for Network Transitions Between Internal and External Processing Modes in the Human Brain |
| title_sort |
criticality creates a functional platform for network transitions between internal and external processing modes in the human brain |
| publisher |
Frontiers Media S.A. |
| publishDate |
2021 |
| url |
https://doaj.org/article/318104445af34810bfca9c03e6b8073c |
| work_keys_str_mv |
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