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Time-resolved directional organization of brain networks: distinct strength and temporal signatures from neurophysiology to disease

Nan XuiD, Xiaodi ZhangiD, Wen-Ju PaniD, Jeremy L. SmithiD, Eric H. SchumacheriD, Jason W. AlleniD, Vince D. CalhouniD, Shella Dawn KeilholziD

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Abstract

Brain function depends on time-resolved directional organization: influence is continuously redistributed across regions, shaping who drives whom, when, and for how long. Yet dynamic neuroimaging has largely emphasized undirected fluctuations in functional connectivity, limiting biological interpretation of asymmetric interactions. Here we show that directed influence can be resolved into two biologically distinct signatures: strength, reflecting the efficacy of influence, and duration, reflecting its temporal extent. To test this principle, we developed sliding-window prediction correlation (SWpC), a framework for estimating these signatures in fMRI and related signals. Across simultaneous rat local field potential (LFP)-fMRI and human motor-task fMRI, strength more closely tracks neural-BOLD coupling and task-evoked reconfiguration, whereas duration captures temporally extended BOLD patterns more susceptible to hemodynamic timing. In post-concussion vestibular dysfunction, altered strength-duration profiles define reproducible vestibular-multisensory states and improve patient-control discrimination. Together, these findings support a general principle of dynamic brain organization spanning neurophysiology, behavior, and disease.

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