The information content of brain states is explained by structural constraints on state energetics

TL;DR

This study links brain structural constraints to the information content of brain states, showing how these constraints influence state transitions and their energetic costs during different cognitive tasks.

Contribution

It introduces a numerical measure of information content based on activation rarity and demonstrates how structural wiring constrains state transitions and their energetic costs.

Findings

Information content varies with cognitive tasks.

High information states are more costly to reach but are efficiently accessible.

Brain's structural network reduces transition costs compared to random models.

Abstract

Signal propagation along the structural connectome of the brain induces changes in the patterns of activity. These activity patterns define global brain states and contain information in accordance with their expected probability of occurrence. The structural connectome, in conjunction with the dynamics, determines the set of possible brain states and constrains the transition between accessible states. Yet, precisely how these structural constraints on state-transitions relate to their information content remains unexplored. To address this gap in knowledge, we defined the information content as a function of the activation distribution, where statistically rare values of activation correspond to high information content. With this numerical definition in hand, we studied the spatiotemporal distribution of information content in fMRI data from the Human Connectome Project during different tasks, and report four key findings. First, information content strongly depends on the cognitive task. Second, while information content shows similarities to other measures of brain activity, it is distinct from both Neurosynth maps and task contrast maps generated by a general linear model applied to the fMRI data. Third, the brain's structural wiring constrains the cost to control its state, where the cost to transition into high information content states is larger than that to transition into low information content states. Finally, all state transitions - especially those to high information content states - are less costly than expected from random network null models, thereby indicating the brain's marked efficiency. Taken together, our findings establish an explanatory link between the information contained in a brain state and the energetic cost of attaining that state, thereby laying important groundwork for our understanding of large-scale cognitive computations.