Abstract

The ability to solve cognitive tasks depends upon adaptive changes in the organization of whole-brain functional networks. However, the link between task-induced network reconfigurations and their underlying energy demands is poorly understood. We address this by multimodal network analyses integrating functional and molecular neuroimaging acquired concurrently during a complex cognitive task. Task engagement elicited a marked increase in the association between glucose consumption and functional brain network reorganization. This convergence between metabolic and neural processes was specific to feedforward connections linking the visual and dorsal attention networks, in accordance with task requirements of visuo-spatial reasoning. Further increases in cognitive load above initial task engagement did not affect the relationship between metabolism and network reorganization but only modulated existing interactions. Our findings show how the upregulation of key computational mechanisms to support cognitive performance unveils the complex, interdependent changes in neural metabolism and neuro-vascular responses.

Highlights

  • Brain function relies on coordinated activity in local neural circuits, from which large-scale functional brain networks are composed (Park and Friston, 2013)

  • Simultaneous functional MRI (BOLD and ASL) and [18F]FDG positron emission tomography (PET) data were acquired while 22 healthy adult participants performed a cognitive task (Tetris)

  • metabolic connectivity mapping (MCM) evaluates the association between regional patterns of blood oxygen level dependent (BOLD)-derived functional connectivity and glucose metabolism

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Summary

Introduction

Brain function relies on coordinated activity in local neural circuits, from which large-scale functional brain networks are composed (Park and Friston, 2013). Recent work has assessed the dynamic changes in functional brain network architecture associated with cognitive task engagement. Results from these investigations have challenged the prior notion (Smith et al, 2009) that functional interactions at resting-state are relatively stable and sufficient to support goal-directed behavior (Cocchi et al, 2013). Solving tasks of increasing cognitive complexity has further been linked to complex changes in the functional interplay between cortical regions that otherwise comprise distinct networks at rest (Hearne et al, 2017). These findings are in line with the proposal that brain networks exhibit a flexible modular architecture, with highly interconnected hub regions changing their functional network assignment according to task demands (Cole et al, 2013)

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