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Reconfiguration of functional brain networks and metabolic cost converge during task performance.

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.

SUBMITTER: Hahn A

PROVIDER: S-EPMC7176400 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Reconfiguration of functional brain networks and metabolic cost converge during task performance.

Hahn Andreas A Breakspear Michael M Rischka Lucas L Wadsak Wolfgang W Godbersen Godber M GM Pichler Verena V Michenthaler Paul P Vanicek Thomas T Hacker Marcus M Kasper Siegfried S Lanzenberger Rupert R Cocchi Luca L

eLife 20200421

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 functiona ...[more]

PMID: 32314956

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Project description:Natural vision engages a wide range of higher-level regions that integrate visual information over the large-scale brain network. How interareal connectivity reconfigures during the processing of ongoing natural visual scenes and how these dynamic functional changes relate to the underlaying anatomical links between regions is not well understood. Here, we hypothesized that macaque visual brain regions are poly-functional sharing the capacity to change their configuration state depending on the nature of visual input. To address this hypothesis, we reconstructed networks from in-vivo diffusion-weighted imaging (DWI) and functional magnetic resonance imaging (fMRI) data obtained in four alert macaque monkeys viewing naturalistic movie scenes. At first, we characterized network properties and found greater interhemispheric density and greater inter-subject variability in free-viewing networks as compared to structural networks. From the structural connectivity, we then captured modules on which we identified hubs during free-viewing that formed a widespread visuo-saccadic network across frontal (FEF, 46v), parietal (LIP, Tpt), and occipitotemporal modules (MT, V4, TEm), and that excluded primary visual cortex. Inter-subject variability of well-connected hubs reflected subject-specific configurations that largely recruited occipito-parietal and frontal modules. Across the cerebral hemispheres, free-viewing networks showed higher correlations among long-distance brain regions as compared to structural networks. From these findings, we hypothesized that long-distance interareal connectivity could reconfigure depending on the ongoing changes in visual scenes. Testing this hypothesis by applying temporally resolved functional connectivity we observed that many structurally defined areas (such as areas V4, MT/MST and LIP) were poly-functional as they were recruited as hub members of multiple network states that changed during the presentation of scenes containing objects, motion, faces, and actions. We suggest that functional flexibility in macaque macroscale brain networks is required for the efficient interareal communication during active natural vision. To further promote the use of naturalistic free-viewing paradigms and increase the development of macaque neuroimaging resources, we share our datasets in the PRIME-DE consortium.

Project description:Learning a new motor task is a complex cognitive and motor process. Especially early during motor learning, cognitive functions such as attentional engagement, are essential, e.g., to discover relevant visual stimuli. Drawing participant's attention towards task-relevant stimuli-e.g., with task instructions using visual cues or explicit written information-is a common practice to support cognitive engagement during training and, hence, accelerate motor learning. However, there is little scientific evidence about how visually cued or written task instructions affect attentional brain networks during motor learning. In this experiment, we trained 36 healthy participants in a virtual motor task: surfing waves by steering a boat with a joystick. We measured the participants' motor performance and observed attentional brain networks using alpha-band electroencephalographic (EEG) activity before and after training. Participants received one of the following task instructions during training: (1) No explicit task instructions and letting participants surf freely (implicit training; IMP); (2) Task instructions provided through explicit visual cues (explicit-implicit training; E-IMP); or (3) through explicit written commands (explicit training; E). We found that providing task instructions during training (E and E-IMP) resulted in less post-training motor variability-linked to enhanced performance-compared to training without instructions (IMP). After training, participants trained with visual cues (E-IMP) enhanced the alpha-band strength over parieto-occipital and frontal brain areas at wave onset. In contrast, participants who trained with explicit commands (E) showed decreased fronto-temporal alpha activity. Thus, providing task instructions in written (E) or using visual cues (E-IMP) leads to similar motor performance improvements by enhancing activation on different attentional networks. While training with visual cues (E-IMP) may be associated with visuo-attentional processes, verbal-analytical processes may be more prominent when written explicit commands are provided (E). Together, we suggest that training parameters such as task instructions, modulate the attentional networks observed during motor practice and may support participant's cognitive engagement, compared to training without instructions.

Dataset Information

Reconfiguration of functional brain networks and metabolic cost converge during task performance.

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Reconfiguration of functional brain networks and metabolic cost converge during task performance.

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