Modular co-organization of functional connectivity and scale-free dynamics in the human brain
Scale-free neuronal dynamics and interareal correlations are emergent characteristics of spontaneous brain activity. How such dynamics and the anatomical patterns of neuronal connectivity are mutually related in brain networks has, however, remained unclear. We addressed this relationship by quantif...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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The MIT Press
2017-06-01
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| Series: | Network Neuroscience |
| Subjects: | |
| Online Access: | https://www.mitpressjournals.org/doi/pdf/10.1162/NETN_a_00008 |
| _version_ | 1828812035282960384 |
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| author | Alexander Zhigalov Gabriele Arnulfo Lino Nobili Satu Palva J. Matias Palva |
| author_facet | Alexander Zhigalov Gabriele Arnulfo Lino Nobili Satu Palva J. Matias Palva |
| author_sort | Alexander Zhigalov |
| collection | DOAJ |
| description | Scale-free neuronal dynamics and interareal correlations are emergent characteristics of spontaneous brain activity. How such dynamics and the anatomical patterns of neuronal connectivity are mutually related in brain networks has, however, remained unclear. We addressed this relationship by quantifying the network colocalization of scale-free neuronal activity—both neuronal avalanches and long-range temporal correlations (LRTCs)—and functional connectivity (FC) by means of intracranial and noninvasive human resting-state electrophysiological recordings. We found frequency-specific colocalization of scale-free dynamics and FC so that the interareal couplings of LRTCs and the propagation of neuronal avalanches were most pronounced in the predominant pathways of FC. Several control analyses and the frequency specificity of network colocalization showed that the results were not trivial by-products of either brain dynamics or our analysis approach. Crucially, scale-free neuronal dynamics and connectivity also had colocalized modular structures at multiple levels of network organization, suggesting that modules of FC would be endowed with partially independent dynamic states. These findings thus suggest that FC and scale-free dynamics—hence, putatively, neuronal criticality as well—coemerge in a hierarchically modular structure in which the modules are characterized by dense connectivity, avalanche propagation, and shared dynamic states. The framework of criticality has been suggested to explain the scale-free dynamics of neuronal activity in complex interaction networks. However, the in vivo relationship between scale-free dynamics and functional connectivity (FC) has remained unclear. We used human intracranial and noninvasive electrophysiological measurements to map scale-free dynamics and connectivity. We found that the propagation of fast activity avalanches and the interareal coupling of slow, long-range temporal correlations—two key forms of scale-free neuronal dynamics—were nontrivially colocalized with the strongest functional connections. Most importantly, scale-free dynamics and FC exhibited similar modular network structures. FC and scale-free dynamics, and possibly also neuronal criticality, appear to co-emerge in a modular architecture in which the modules are characterized internally by shared dynamic states, avalanche propagation, and dense functional connectivity. |
| first_indexed | 2024-12-12T09:36:24Z |
| format | Article |
| id | doaj.art-e8a8f57b01ff457ca3459c27f943c9e1 |
| institution | Directory Open Access Journal |
| issn | 2472-1751 |
| language | English |
| last_indexed | 2024-12-12T09:36:24Z |
| publishDate | 2017-06-01 |
| publisher | The MIT Press |
| record_format | Article |
| series | Network Neuroscience |
| spelling | doaj.art-e8a8f57b01ff457ca3459c27f943c9e12022-12-22T00:28:42ZengThe MIT PressNetwork Neuroscience2472-17512017-06-011214316510.1162/NETN_a_00008NETN_a_00008Modular co-organization of functional connectivity and scale-free dynamics in the human brainAlexander Zhigalov0Gabriele Arnulfo1Lino Nobili2Satu Palva3J. Matias Palva4Neuroscience Center, University of Helsinki, FinlandNeuroscience Center, University of Helsinki, FinlandClaudio Munari Epilepsy Surgery Centre, Niguarda Hospital, ItalyNeuroscience Center, University of Helsinki, FinlandNeuroscience Center, University of Helsinki, FinlandScale-free neuronal dynamics and interareal correlations are emergent characteristics of spontaneous brain activity. How such dynamics and the anatomical patterns of neuronal connectivity are mutually related in brain networks has, however, remained unclear. We addressed this relationship by quantifying the network colocalization of scale-free neuronal activity—both neuronal avalanches and long-range temporal correlations (LRTCs)—and functional connectivity (FC) by means of intracranial and noninvasive human resting-state electrophysiological recordings. We found frequency-specific colocalization of scale-free dynamics and FC so that the interareal couplings of LRTCs and the propagation of neuronal avalanches were most pronounced in the predominant pathways of FC. Several control analyses and the frequency specificity of network colocalization showed that the results were not trivial by-products of either brain dynamics or our analysis approach. Crucially, scale-free neuronal dynamics and connectivity also had colocalized modular structures at multiple levels of network organization, suggesting that modules of FC would be endowed with partially independent dynamic states. These findings thus suggest that FC and scale-free dynamics—hence, putatively, neuronal criticality as well—coemerge in a hierarchically modular structure in which the modules are characterized by dense connectivity, avalanche propagation, and shared dynamic states. The framework of criticality has been suggested to explain the scale-free dynamics of neuronal activity in complex interaction networks. However, the in vivo relationship between scale-free dynamics and functional connectivity (FC) has remained unclear. We used human intracranial and noninvasive electrophysiological measurements to map scale-free dynamics and connectivity. We found that the propagation of fast activity avalanches and the interareal coupling of slow, long-range temporal correlations—two key forms of scale-free neuronal dynamics—were nontrivially colocalized with the strongest functional connections. Most importantly, scale-free dynamics and FC exhibited similar modular network structures. FC and scale-free dynamics, and possibly also neuronal criticality, appear to co-emerge in a modular architecture in which the modules are characterized internally by shared dynamic states, avalanche propagation, and dense functional connectivity.https://www.mitpressjournals.org/doi/pdf/10.1162/NETN_a_00008Scale-free dynamicsFunctional connectomeModular networksNeuronal avalanchesLong-range temporal correlations |
| spellingShingle | Alexander Zhigalov Gabriele Arnulfo Lino Nobili Satu Palva J. Matias Palva Modular co-organization of functional connectivity and scale-free dynamics in the human brain Network Neuroscience Scale-free dynamics Functional connectome Modular networks Neuronal avalanches Long-range temporal correlations |
| title | Modular co-organization of functional connectivity and scale-free dynamics in the human brain |
| title_full | Modular co-organization of functional connectivity and scale-free dynamics in the human brain |
| title_fullStr | Modular co-organization of functional connectivity and scale-free dynamics in the human brain |
| title_full_unstemmed | Modular co-organization of functional connectivity and scale-free dynamics in the human brain |
| title_short | Modular co-organization of functional connectivity and scale-free dynamics in the human brain |
| title_sort | modular co organization of functional connectivity and scale free dynamics in the human brain |
| topic | Scale-free dynamics Functional connectome Modular networks Neuronal avalanches Long-range temporal correlations |
| url | https://www.mitpressjournals.org/doi/pdf/10.1162/NETN_a_00008 |
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