Higher-order connectomics of human brain function reveals local topological signatures of task decoding, individual identification, and behavior

• Published in: Nature communications Vol. 15; no. 1; pp. 10244 - 12
• Main Authors: Santoro, Andrea, Battiston, Federico, Lucas, Maxime, Petri, Giovanni, Amico, Enrico
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 26.11.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/378/116/1925; 631/378/116/2393; 639/705/1041; Adult; Behavior - physiology; Brain; Brain - diagnostic imaging; Brain - physiology; Brain architecture; Brain mapping; Brain Mapping - methods; Connectome; Data analysis; Decoding; Female; Fingerprinting; Functional magnetic resonance imaging; Functional morphology; Humanities and Social Sciences; Humans; Magnetic Resonance Imaging - methods; Male; multidisciplinary; Nerve Net - diagnostic imaging; Nerve Net - physiology; Science; Science (multidisciplinary); Subsystems; Time series; Young Adult
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-54472-y

Traditional models of human brain activity often represent it as a network of pairwise interactions between brain regions. Going beyond this limitation, recent approaches have been proposed to infer higher-order interactions from temporal brain signals involving three or more regions. However, to this day it remains unclear whether methods based on inferred higher-order interactions outperform traditional pairwise ones for the analysis of fMRI data. To address this question, we conducted a comprehensive analysis using fMRI time series of 100 unrelated subjects from the Human Connectome Project. We show that higher-order approaches greatly enhance our ability to decode dynamically between various tasks, to improve the individual identification of unimodal and transmodal functional subsystems, and to strengthen significantly the associations between brain activity and behavior. Overall, our approach sheds new light on the higher-order organization of fMRI time series, improving the characterization of dynamic group dependencies in rest and tasks, and revealing a vast space of unexplored structures within human functional brain data, which may remain hidden when using traditional pairwise approaches. Here, the authors perform a higher-order analysis of fMRI data, revealing that accounting for group interactions greatly enhances task decoding, brain fingerprinting, and brain-behavior associations compared to traditional methods, offering a new insight into brain dynamics.