Published July 3, 2023 | Version v1
Journal article Open

Large-scale neural dynamics in a shared low-dimensional state space reflect cognitive and attentional dynamics

  • 1. University of Chicago
  • 2. Sungkyunkwan University

Description

Cognition and attention arise from the adaptive coordination of neural systems in response to external and internal demands. The low-dimensional latent subspace that underlies large-scale neural dynamics and the relationships of these dynamics to cognitive and attentional states, however, are unknown. We conducted functional magnetic resonance imaging as human participants performed attention tasks, watched comedy sitcom episodes and an educational documentary, and rested. Whole-brain dynamics traversed a common set of latent states that spanned canonical gradients of functional brain organization, with global desynchronization among functional networks modulating state transitions. Neural state dynamics were synchronized across people during engaging movie watching and aligned to narrative event structures. Neural state dynamics reflected attention fluctuations such that different states indicated engaged attention in task and naturalistic contexts, whereas a common state indicated attention lapses in both contexts. Together, these results demonstrate that traversals along large-scale gradients of human brain organization reflect cognitive and attentional dynamics.

Data availability

Raw fMRI data from the SitcOm, Nature documentary, Gradual-onset continuous performance task (SONG) dataset are available on OpenNeuro; https://openneuro.org/datasets/ds004592/versions/1.0.1. Behavioral data, processed fMRI output, and main analysis scripts are published on Github (copy archived at Song, 2023).

The following data sets were generated:
Song H Shim WM Rosenberg MD (2023) OpenNeuro SONG dataset. https://doi.org/10.18112/openneuro.ds004592.v1.0.1

The following previously published data sets were used:
Nastase SA Liu Y Hillman H Zadbood A Hasenfratz L Keshavarzian N Chen J Honey CJ Yeshurun Y Regev M Nguyen M Chang CHC Baldassano C Lositsky O Simony E Chow MA Leong YC Brooks PP Micciche E Choe G Goldstein A Vanderwal T Halchenko YO Norman KA Hasson U (2020) OpenNeuro Narratives: fMRI data for evaluating models of naturalistic language comprehension. https://doi.org/10.18112/openneuro.ds002345.v1.1.4
Chen J Leong YC Honey CJ Yong CH Norman KA Hasson U (2018) OpenNeuro Sherlock. https://doi.org/10.18112/openneuro.ds001132.v1.0.0
Margulies DS Ghosh SS Goulas A Falkiewicz M Huntenburg JM Langs G Bezgin G Eickhoff SB Castellanos FX Petrides M Jefferies E Smallwood J (2016) NeuroVault ID 1598. Situating the default-mode network along a principal gradient of macroscale cortical organization. https://identifiers.org/neurovault.collection:1598

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Additional details

Identifiers

DOI
10.7554/eLife.85487
Other
oai:uchicago.tind.io:7714

Funding

Institute for Basic Science
IBS R015-D1
National Research Foundation of Korea
NRF-2019M3E5D2A01060299
National Research Foundation of Korea
NRF-2019R1A2C1085566
National Science Foundation
BCS-2043740

UChicago Information

Division(s)
Social Sciences Division
Department(s)
Psychology
Center(s) or Institute(s)
Neuroscience Institute