Compression of functional gradients from rest to naturalistic processing: modulation effect of age
Poster No:
755
Submission Type:
Abstract Submission
Authors:
Shuer Ye1, Jasper Mostert1, Robin Pedersen2, Xiaqing Lan1, Lei Zhao3, Alireza Salami2, Maryam Ziaei1
Institutions:
1Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology, Trondheim, Norway, 2Umeå Center for Functional Brain Imaging (UFBI), Umeå University, Umeå, Sweden, 3Chinese Academy of Sciences, Beijing, China
First Author:
Shuer Ye
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Co-Author(s):
Jasper Mostert
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Xiaqing Lan
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Maryam Ziaei
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology
Trondheim, Norway
Introduction:
Elucidating how the brain integrates informative real-world stimuli to emerge abstract cognition is essential for understanding the extensive functional diversity of the human brain and the neural basis of human behavior (Chang et al., 2021; Zhang et al., 2021). Recent studies have demonstrated that encoding sensory input into higher-order complex cognition relies on the hierarchical functional organization of the cortex (Bernhardt et al., 2022; Huntenburg et al., 2018; Margulies et al., 2016). While the functional hierarchy of resting-state functional gradients is well-established, how these gradients are modulated by ecological naturalistic stimuli remains unclear. The gradient pattern has been shown to be sensitive to age, with changes occurring during developmental periods but also throughout the aging process(Bethlehem et al., 2020; Xia et al., 2022). However, the impact of aging on this hierarchical architecture, especially those during naturalistic processing, and its link to cognition remains elusive.
Methods:
Utilizing resting-state and movie fMRI data from two large datasets, CAM-CAN (N= 402) and DyNAMiC (N=156) (Nordin et al., 2022; Taylor, 2017), this study conducted a comprehensive comparison of brain organization between rest and movie-watching. Specifically, diffusion embedding was applied to extract the main gradients of rest and movie-watching, and we examined the gradient alteration between rest and movie-watching at regional, network, and global levels. We further explored the mediation effects of network integration and segregation, as well as the modulation effect of age, on the relationship between brain state and global gradient properties, including gradient range and variance. Lastly, we investigate the relationship between gradient characteristics and cognitive functions between age groups.
Results:
We identified a robust compression pattern in functional gradients during the transition from rest to movie-watching (Fig.1) which was significantly intensified in older age (Fig.2) and mediated by individual differences in functional integration and segregation of brain networks. Moreover, a greater global gradient range and variance, particularly during movie-watching gradients, were consistently associated with better cognitive ability such as memory function and perception speed.
·Figure 1. Regional, global, and network-level gradient differences between resting state and movie watching.
·Figure 2. The modulation effect of age on the state-driven gradient alterations.
Conclusions:
This study is the first to directly compare resting and movie-watching state from the macroscale brain organization while delineating age-related alterations in functional hierarchy. We found that gradients become more compressed when shifting from passive rest to active naturalistic movie watching, likely due to enhanced functional integration and reduced functional segregation of brain networks in response to external stimuli. Additionally, gradient compression was modulated by age and contributed to better cognitive performance. These findings enhance our understanding of the functional hierarchy across different brain states and provide valuable insights into the neural basis of cognitive aging. This knowledge could inform the development of interventions to maintain hierarchical processing, potentially mitigating age-related cognitive decline.
Higher Cognitive Functions:
Higher Cognitive Functions Other 1
Lifespan Development:
Aging 2
Modeling and Analysis Methods:
fMRI Connectivity and Network Modeling
Keywords:
Aging
FUNCTIONAL MRI
1|2Indicates the priority used for review
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Bethlehem, R. A. I., Paquola, C., Seidlitz, J., Ronan, L., Bernhardt, B., Consortium, C.-C., & Tsvetanov, K. A. (2020). Dispersion of functional gradients across the adult lifespan. NeuroImage, 222, 117299.
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Huntenburg, J. M., Bazin, P.-L., & Margulies, D. S. (2018). Large-Scale Gradients in Human Cortical Organization. Trends in Cognitive Sciences, 22(1), 21–31.
Margulies, D. S., Ghosh, S. S., Goulas, A., Falkiewicz, M., Huntenburg, J. M., Langs, G., Bezgin, G., Eickhoff, S. B., Castellanos, F. X., Petrides, M., Jefferies, E., & Smallwood, J. (2016). Situating the default-mode network along a principal gradient of macroscale cortical organization. Proceedings of the National Academy of Sciences, 113(44), 12574–12579.
Nordin, K., Gorbach, T., Pedersen, R., Panes Lundmark, V., Johansson, J., Andersson, M., McNulty, C., Riklund, K., Wåhlin, A., Papenberg, G., Kalpouzos, G., Bäckman, L., & Salami, A. (2022). DyNAMiC: A prospective longitudinal study of dopamine and brain connectomes: A new window into cognitive aging. Journal of Neuroscience Research, 100(6), 1296–1320.
Taylor, J. R. (2017). The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) data repository: Structural and functional MRI, MEG, and cognitive data from a cross-sectional adult lifespan sample. NeuroImage, 144, 262–269.
Xia, Y., Xia, M., Liu, J., Liao, X., Lei, T., Liang, X., Zhao, T., Shi, Z., Sun, L., Chen, X., Men, W., Wang, Y., Pan, Z., Luo, J., Peng, S., Chen, M., Hao, L., Tan, S., Gao, J.-H., … He, Y. (2022). Development of functional connectome gradients during childhood and adolescence. Science Bulletin, 67(10), 1049–1061.
Zhang, Y., Kim, J.-H., Brang, D., & Liu, Z. (2021). Naturalistic stimuli: A paradigm for multiscale functional characterization of the human brain. Current Opinion in Biomedical Engineering, 19, 100298.