Temporal sequences of brain activity at rest are constrained by white matter structure and modulated by cognitive demands

TL;DR

This study reveals how white matter structure constrains and modulates the temporal sequences of brain activity during rest and cognitive tasks, linking structural connectivity to dynamic brain function and age-related changes.

Contribution

It demonstrates that white matter architecture influences brain activity trajectories and their modulation by cognitive demands, integrating diffusion imaging, network control theory, and age-related analyses.

Findings

White matter structure constrains brain activity trajectories at rest.

Cognitive load modulates the sequences of brain activity during tasks.

Age-related differences are observed in brain state dynamics.

Abstract

A diverse white matter network and finely tuned neuronal membrane properties allow the brain to transition seamlessly between cognitive states. However, it remains unclear how static structural connections guide the temporal progression of large-scale brain activity patterns in different cognitive states. Here, we analyze the brain's trajectories through a high-dimensional activity space at the level of single time point activity patterns from functional magnetic resonance imaging data acquired during passive visual fixation (rest) and an n-back working memory task. We find that specific state space trajectories, which represent temporal sequences of brain activity, are modulated by cognitive load and related to task performance. Using diffusion-weighted imaging acquired from the same subjects, we use tools from network control theory to show that linear spread of activity along white matter connections constrains the brain's state space trajectories at rest. Additionally, accounting for stimulus-driven visual inputs explains the different trajectories taken during the n-back task. We also used models of network rewiring to show that these findings are the result of non-trivial geometric and topological properties of white matter architecture. Finally, we examine associations between age and time-resolved brain state dynamics, revealing new insights into functional changes in the default mode and executive control networks. Overall, these results elucidate the structural underpinnings of cognitively and developmentally relevant spatiotemporal brain dynamics.