The impact of aging on human brain network target controllability

• Published in: Brain Structure and Function 2022-12, Vol.227 (9), p.3001-3015
• Main Authors: Bassignana, Giulia, Lacidogna, Giordano, Bartolomeo, Paolo, Colliot, Olivier, De Vico Fallani, Fabrizio
• Format: Article
• Language: English
• Subjects: Age; Aging; Biomedical and Life Sciences; Biomedicine; Brain; Cell Biology; Cognitive science; Dementia disorders; Life span; Mathematics; Neurology; Neuroscience; Neurosciences; Original Article; Sensorimotor system; Stroke
• ISSN: 1863-2653; 1863-2661; 0340-2061
• DOI: 10.1007/s00429-022-02584-w

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.