Abstract
Understanding how few distributed areas can steer large-scale brain activity is a fundamental question that has practical implications, which range from inducing specific patterns of behavior to counteracting disease. Recent endeavors based on network controllability provided fresh insights into the potential ability of single regions to influence whole brain dynamics through the underlying structural connectome. However, controlling the entire brain activity is often unfeasible and might not always be necessary. The question whether single areas can control specific target subsystems remains crucial, albeit still poorly explored. Furthermore, the structure of the brain network exhibits progressive changes across the lifespan, but little is known about the possible consequences in the controllability properties. To address these questions, we adopted a novel target controllability approach that quantifies the centrality of brain nodes in controlling specific target anatomo-functional systems. We then studied such target control centrality in human connectomes obtained from healthy individuals aged from 5 to 85. Main results showed that the sensorimotor system has a high influencing capacity, but it is difficult for other areas to influence it. Furthermore, we reported that target control centrality varies with age and that temporal-parietal regions, whose cortical thinning is crucial in dementia-related diseases, exhibit lower values in older people. By simulating targeted attacks, such as those occurring in focal stroke, we showed that the ipsilesional hemisphere is the most affected one regardless of the damaged area. Notably, such degradation in target control centrality was more evident in younger people, thus supporting early-vulnerability hypotheses after stroke.
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Data availability statement
All the experimental data used in this work are fully accessible from the NKI-Rockland database (Nooner et al. 2012).
References
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Acknowledgements
Authors would like to acknowledge Thibault Rolland (fr.linkedin.com/in/thibault-rolland-40b57419a) for the realization of Picture 1. The content is solely the responsibility of the authors and does not necessarily represent the official views of any of the funding agencies.
Funding
The research leading to these results has received funding from the French government under management of Agence Nationale de la Recherche as part of the “Investissements d’avenir” program, reference ANR-19-P3IA-0001 (PRAIRIE 3IA Institute) and reference ANR-10-IAIHU-06 (Agence Nationale de la Recherche-10-IA Institut Hospitalo-Universitaire-6), and from the Inria Project Lab Program (project Neuromarkers), the European Research Council (ERC) under the European Unions Horizon 2020 research and innovation programme (Grant Agreement no. 864729).
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Bassignana, G., Lacidogna, G., Bartolomeo, P. et al. The impact of aging on human brain network target controllability. Brain Struct Funct 227, 3001–3015 (2022). https://doi.org/10.1007/s00429-022-02584-w
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DOI: https://doi.org/10.1007/s00429-022-02584-w