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Unifying Brain Geometry and Connectivity

Deco, Gustavo (UPF)

Engineering Sciences

Explaining how brain structure gives rise to emerging dynamics is a central goal in neuroscience. We present an anatomical constraint showing that rare long-range (LR) connections are essential for capturing both spontaneous and task-evoked functional organization. This framework unifies cortical geometry and local connectivity via the exponential distance rule (EDR), while explicitly incorporating LR exceptions identified in the structural connectome. Using this enriched structural description, we demonstrate that task-evoked activity lies on a low-dimensional manifold composed of a small set of modes, suggesting that efficient information processing relies on a compact dynamical repertoire.While cortical geometry and EDR-based local connectivity explain much of large-scale functional structure, they miss the computational importance of rare LR projections. These connections, though few, markedly enhance information integration and are not predictable from cortical folding alone. We show that harmonic modes combining EDR with LR connectivity (EDR+LR) provide a markedly superior basis for reconstructing functional dynamics - including LR functional connectivity and task-evoked responses - compared to geometry - or EDR-only models. Overall, our results reveal that rare LR connections crucially shape a low-dimensional manifold of fundamental modes that efficiently captures the complexity of human brain activity.

Figure: EDR+LR uses fewest harmonic modes to reconstruct task activity. (A) For each of the four graph representations (Top panel) the reconstruction of seven representative task - activation maps is shown in terms of normalized mse distance (distance normalized by the max of each task). As can be seen, lower frequency modes contribute disproportionately more toward the reconstruction distance as it can be seen by the elbow around 20 modes (Lower panel). (B) This can also be seen in the reconstruction mse distance for all 47 HCP tasks for the EDR+LR, EDR binary, and EDR continuous, each benchmarked against the geometrical modes for the first 20 modes, where the Top panel shows hues of blue with better performance of the EDR modes while red hues mean better performance of the geometric modes. The Lower panel shows the average across the 47 HCP tasks. (C) As an example, for the motor task target (Far Left), we compare the overall correlational contributions of the number of modes (using 20, 15, 10, and 5 modes) when using EDR+LR and geometry as the underlying representations. As can be seen, the reconstruction with EDR+LR converges more quickly for lower modes than geometry.


REFERENCE

Vohryzek J, Sanz-Perl Y, Kringelbach ML & Deco G 2025, 'Human brain dynamics are shaped by rare long- range connections over and above cortical geometry', Proceedings of the national academy of sciences of the united states of america, 122 - 1 - e2415102122.