4.7 Article

Avalanche criticality in individuals, fluid intelligence, and working memory

Journal

HUMAN BRAIN MAPPING
Volume 43, Issue 8, Pages 2534-2553

Publisher

WILEY
DOI: 10.1002/hbm.25802

Keywords

avalanche criticality; fluid intelligence; large-scale brain network; phase transition; resting-state fMRI; working memory

Funding

  1. Fundamental Research Funds for the Central Universities [lzujbky-2021-62]
  2. National Natural Science Foundation of China [12047501]
  3. 111 Project [B18015]
  4. National Key R&D Program of China [2018YFC1312904, 2019YFA0709502]
  5. Shanghai Municipal Science and Technology Major Project [2018SHZDZX01]
  6. Shanghai Center for Brain Science and Brain-Inspired Technology
  7. ZJLab

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This study investigates the relationship between human cognitive performance and scale-free brain dynamics. The results show that individual scale-free avalanche activity is significantly associated with maximal synchronization entropy of brain activity. Participants with higher fluid intelligence and working memory scores have neural dynamics closer to criticality.
The critical brain hypothesis suggests that efficient neural computation can be achieved through critical brain dynamics. However, the relationship between human cognitive performance and scale-free brain dynamics remains unclear. In this study, we investigated the whole-brain avalanche activity and its individual variability in the human resting-state functional magnetic resonance imaging (fMRI) data. We showed that though the group-level analysis was inaccurate because of individual variability, the subject wise scale-free avalanche activity was significantly associated with maximal synchronization entropy of their brain activity. Meanwhile, the complexity of functional connectivity, as well as structure-function coupling, is maximized in subjects with maximal synchronization entropy. We also observed order-disorder phase transitions in resting-state brain dynamics and found that there were longer times spent in the subcritical regime. These results imply that large-scale brain dynamics favor the slightly subcritical regime of phase transition. Finally, we showed evidence that the neural dynamics of human participants with higher fluid intelligence and working memory scores are closer to criticality. We identified brain regions whose critical dynamics showed significant positive correlations with fluid intelligence performance and found that these regions were located in the prefrontal cortex and inferior parietal cortex, which were believed to be important nodes of brain networks underlying human intelligence. Our results reveal the possible role that avalanche criticality plays in cognitive performance and provide a simple method to identify the critical point and map cortical states on a spectrum of neural dynamics, ranging from subcriticality to supercriticality.

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