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Nested-spectral analysis reveals a disruption of behavioral-related dynamic functional balance in the aging brain

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Abstract

The relationship between the age-related reorganization of brain networks and individual behavior has attracted much attention. However, how age induces changes in neural activity at different frequencies in the brain to balance the demands of network integration and segregation, and how age-induced changes in network integration and segregation relate to behavior remain enigmatic. Here, a nested-spectral partition method was used to analyze behavioral-related dynamic functional balance in the aging brain with electroencephalogram signals collected from 56 healthy participants (age: 20–80 years) at rest. The nested-spectral partition approach measures hierarchical segregation and integration across multiple levels by detecting hierarchical modules in brain functional networks. Declines in general personality and general cognitive ability in older adults were captured by exploratory factor analysis. We showed that the brain network of elderly individuals contains more hierarchical modules to generate higher segregation, and it is closer to the functional balance state in the theta and alpha bands but away from this state in the gamma band. Meanwhile, the abnormal variability of functional balance in the elderly brain supports more flexible transitions between segregated and integrated states in the alpha band but reduces the transitions in the beta and gamma bands. Crucially, the degeneration of general personality and general cognitive ability is significantly associated with higher segregation and abnormal flexibility of the brain, especially in the theta, beta, and gamma bands. Our results provide deep insights from a spectral partitioning perspective into the brain dynamic mechanisms that are associated with age-related personality and cognitive degeneration.

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Funding

This work was supported by the National Natural Science Foundation of China (Grants No. 12132012, No. 11972275, No. 12272292, and No. 62071177).

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Authors and Affiliations

  1. State Key Laboratory for Strength and Vibration of Mechanical Structures, School of Aerospace Engineering, Xi’an Jiaotong University, Xi’an, 710049, China

    Yongchen Fan, Rong Wang, Lv Zhou & Ying Wu

  2. College of Science, Xi’an University of Science and Technology, Xi’an, 710049, China

    Rong Wang

  3. National Demonstration Center for Experimental Mechanics Education, Xi’an Jiaotong University, Xi’an, 710049, China

    Lv Zhou & Ying Wu

  4. Department of Psychology and Cognition and Human Behavior Key Laboratory of Hunan Province, Hunan Normal University, Changsha, 410081, China

    Pan Lin

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Conceptualization was contributed by YF; Methodology was contributed by YF and RW; Data curation was contributed by YF; Formal analysis was contributed by YF; Funding acquisition was contributed by RW, Pan Lin and YW; Investigation was contributed by YF, RW and LZ; Software was contributed by YF; Supervision was contributed by RW and YW; Visualization was contributed by YF; Writing—original draft, was contributed by YF; Writing—review & editing, was contributed by YF, RW, PL and YW.

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Fan, Y., Wang, R., Zhou, L. et al. Nested-spectral analysis reveals a disruption of behavioral-related dynamic functional balance in the aging brain. Nonlinear Dyn 111, 9537–9553 (2023). https://doi.org/10.1007/s11071-023-08328-7

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