Long-Range White-Matter Pathways Enable Efficient Spontaneous Neural Activity Propagation in the Human Brain.

Area of Science:

• Neuroscience
• Connectomics
• Brain Imaging

Background:

• Efficient brain-wide communication relies on rapid neural signal propagation over long distances.
• Understanding the factors influencing propagation timing is crucial for deciphering brain function and dysfunction.
• Existing models often overlook the interplay between anatomical structure, functional organization, and signal dynamics.

Purpose of the Study:

• To investigate how spatial geometry, functional networks, and white-matter microstructure jointly influence neural propagation timing.
• To determine if propagation rules for epileptiform activity (interictal epileptiform discharges - IEDs) mirror those of physiological activity.
• To identify microstructural mechanisms enabling fast, long-range brain communication.

Main Methods:

• Utilized stereo-electroencephalography (stereo-EEG) and diffusion spectrum imaging (DSI) in 47 epilepsy patients.
• Quantified inter-regional propagation delays using event-based IED traveling waves and continuous lagged-correlation analysis.
• Analyzed the relationship between propagation timing, anatomical distance, structural connectivity, functional connectivity, and white-matter microstructural properties (quantitative anisotropy - QA).

Main Results:

• Neural propagation, both epileptiform and physiological, follows structured routing patterns, deviating from random spread.
• Propagation delays saturate at longer distances, indicating that geometry alone does not explain fast long-range transmission.
• Shorter delays correlate with stronger structural and functional connectivity, with faster within-network than between-network propagation.
• Higher quantitative anisotropy (QA) in white-matter tracts is associated with faster apparent propagation velocity, revealing a microstructural basis for efficient communication.

Conclusions:

• Brain-wide communication timing is constrained by architecture, integrating macroscale connectome organization with neural dynamics.
• Shared propagation rules govern both pathological (IEDs) and physiological brain activity, emphasizing the brain's efficient communication principles.
• White-matter microstructure, particularly QA, plays a critical role in facilitating rapid long-range neural signal transmission.