Structure-informed functional connectivity driven by identifiable and state-specific control regions

Abstract

Describing how the brain anatomical wiring contributes to the emergence of coordinated neural activity underlying complex behavior remains challenging. Indeed, patterns of remote coactivations that adjust with the ongoing task-demand do not systematically match direct, static anatomical links. Here, we propose that observed coactivation patterns, known as functional connectivity (FC), can be explained by a controllable linear diffusion dynamics defined on the brain architecture. Our model, termed structure-informed FC, is based on the hypothesis that different sets of brain regions controlling the information flow on the anatomical wiring produce state-specific functional patterns. We thus introduce a principled framework for the identification of potential control centers in the brain. We find that well-defined, sparse, and robust sets of control regions, partially overlapping across several tasks and resting state, produce FC patterns comparable to empirical ones. Our findings suggest that controllability is a fundamental feature allowing the brain to reach different states.

Author Summary

Understanding how brain anatomy promotes particular patterns of coactivations among neural regions is a key challenge in neuroscience. This challenge can be addressed using network science and systems theory. Here, we propose that coactivations result from the diffusion of information through the network of anatomical links connecting brain regions, with certain regions controlling the dynamics. We translate this hypothesis into a model called structure-informed functional connectivity, and we introduce a framework for identifying control regions based on empirical data. We find that our model produces coactivation patterns comparable to empirical ones, and that distinct sets of control regions are associated with different functional states. These findings suggest that controllability is an important feature allowing the brain to reach different states.