Structurally-constrained relationships between cognitive states in the human brain.

Ann M Hermundstad,Arianne Johnson,Jean M Carlson,Scott T Grafton,Kevin S Brown,Amy Frithsen,Elissa M Aminoff,Danielle S Bassett,Christine M Tipper,Michael B Miller,Claus C Hilgetag

doi:10.1371/journal.pcbi.1003591

Abstract

The anatomical connectivity of the human brain supports diverse patterns of correlated neural activity that are thought to underlie cognitive function. In a manner sensitive to underlying structural brain architecture, we examine the extent to which such patterns of correlated activity systematically vary across cognitive states. Anatomical white matter connectivity is compared with functional correlations in neural activity measured via blood oxygen level dependent (BOLD) signals. Functional connectivity is separately measured at rest, during an attention task, and during a memory task. We assess these structural and functional measures within previously-identified resting-state functional networks, denoted task-positive and task-negative networks, that have been independently shown to be strongly anticorrelated at rest but also involve regions of the brain that routinely increase and decrease in activity during task-driven processes. We find that the density of anatomical connections within and between task-positive and task-negative networks is differentially related to strong, task-dependent correlations in neural activity. The space mapped out by the observed structure-function relationships is used to define a quantitative measure of separation between resting, attention, and memory states. We find that the degree of separation between states is related to both general measures of behavioral performance and relative differences in task-specific measures of attention versus memory performance. These findings suggest that the observed separation between cognitive states reflects underlying organizational principles of human brain structure and function.

Highlights

The brain is continually active, whether in a state of rest or during the performance of task-directed function
Human cognitive function is thought to be supported by patterns of correlated neural activity
While recent work has shown that such functional correlations are differentially supported by specific properties of anatomical brain connectivity, the extent to which brain anatomy shapes cognition is not understood

Summary

Introduction

The brain is continually active, whether in a state of rest or during the performance of task-directed function. Despite predictions that resting-state neural activity would be noisy and unconstrained, the human brain has been shown to exhibit patterns of correlated neural activity even in the absence of any task-directed function [1,2]. Signatures of task-related function have been identified in task-free states based on anticorrelations in spontaneous neural activity between default mode and task-related brain regions [7,8,9,10] Together, these sets of brain regions have widely been associated with two functional networks, denoted task-positive and task-negative, composed of regions known to become more (taskpositive) and less (task-negative) active during the task performance relative to their behavior at rest [7]. Correlations within these networks have been shown to support attention [11] and memory [12,13] processes, and disruptions to these networks have been implicated in neurological disorders [14,15,16,17]

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