Tripartite organization of brain state dynamics underlying spoken narrative comprehension

Speech comprehension involves the dynamic interplay of multiple cognitive processes, from basic sound perception, to linguistic encoding, and finally to complex semantic-conceptual interpretations. How the brain handles the diverse streams of information processing remains poorly understood. Applying Hidden Markov Modeling to fMRI data obtained during spoken narrative comprehension, we reveal that the whole brain networks predominantly oscillate within a tripartite latent state space. These states are, respectively, characterized by high activities in the sensory-motor (State #1), bilateral temporal (State #2), and default mode networks (DMN; State #3) regions, with State #2 acting as a transitional hub. The three states are selectively modulated by the acoustic, word-level semantic, and clause-level semantic properties of the narrative. Moreover, the alignment with both the best performer and the group-mean in brain state expression can predict participants' narrative comprehension scores measured from the post-scan recall. These results are reproducible with different brain network atlas and generalizable to two datasets consisting of young and older adults. Our study suggests that the brain underlies narrative comprehension by switching through a tripartite state space, with each state probably dedicated to a specific component of language faculty, and effective narrative comprehension relies on engaging those states in a timely manner.

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Publication Details

Journal
eLife
Published
2024-10-08
DOI
https://doi.org/10.7554/elife.99997
Citations
2
Primary Topic
Cognitive Science and Mapping
Type
article
Field-Weighted Citation Impact
0.69

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article

Tripartite organization of brain state dynamics underlying spoken narrative comprehension

Lanfang Liu, Hehui Li, Guosheng Ding, Jiahao Jiang
2 citations
eLife
Cognitive Science and Mapping
0.69
article

Tripartite organization of brain state dynamics underlying spoken narrative comprehension

Lanfang Liu, Hehui Li, Guosheng Ding, Jiahao Jiang
article en
2 citations

Abstract

Speech comprehension involves the dynamic interplay of multiple cognitive processes, from basic sound perception, to linguistic encoding, and finally to complex semantic-conceptual interpretations. How the brain handles the diverse streams of information processing remains poorly understood. Applying Hidden Markov Modeling to fMRI data obtained during spoken narrative comprehension, we reveal that the whole brain networks predominantly oscillate within a tripartite latent state space. These states are, respectively, characterized by high activities in the sensory-motor (State #1), bilateral temporal (State #2), and default mode networks (DMN; State #3) regions, with State #2 acting as a transitional hub. The three states are selectively modulated by the acoustic, word-level semantic, and clause-level semantic properties of the narrative. Moreover, the alignment with both the best performer and the group-mean in brain state expression can predict participants' narrative comprehension scores measured from the post-scan recall. These results are reproducible with different brain network atlas and generalizable to two datasets consisting of young and older adults. Our study suggests that the brain underlies narrative comprehension by switching through a tripartite state space, with each state probably dedicated to a specific component of language faculty, and effective narrative comprehension relies on engaging those states in a timely manner.

eLifeVol. 13
McGovern Institute for Brain Research (US), Shenzhen University (CN), Beijing Normal University (CN), Shenzhen Institute of Neuroscience (CN)
National Natural Science Foundation of China, Basic and Applied Basic Research Foundation of Guangdong Province
Quality Education
Openalex Percentile: Top 24%
Cognitive Science and Mapping
0.69
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