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. Applyin...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2025-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/99997 |
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| author | Lanfang Liu Jiahao Jiang Hehui Li Guosheng Ding |
| author_facet | Lanfang Liu Jiahao Jiang Hehui Li Guosheng Ding |
| author_sort | Lanfang Liu |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-bc6effc50da04de19dace1a446c63664 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-bc6effc50da04de19dace1a446c636642025-01-21T13:48:35ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.99997Tripartite organization of brain state dynamics underlying spoken narrative comprehensionLanfang Liu0https://orcid.org/0000-0002-1448-9009Jiahao Jiang1https://orcid.org/0000-0001-6335-391XHehui Li2https://orcid.org/0000-0002-7315-3396Guosheng Ding3https://orcid.org/0000-0002-0065-6398Department of Psychology, School of Arts and Sciences, Beijing Normal University at Zhuhai, Zhuhai, China; Faculty of Psychology, Beijing Normal University, Beijing, ChinaState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University & IDG/McGovern Institute for Brain Research, Beijing, ChinaCenter for Brain Disorders and Cognitive Sciences, School of Psychology, Shenzhen University, Shenzhen, ChinaState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University & IDG/McGovern Institute for Brain Research, Beijing, ChinaSpeech 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.https://elifesciences.org/articles/99997speech comprehensionbrain dynamicsHMM |
| spellingShingle | Lanfang Liu Jiahao Jiang Hehui Li Guosheng Ding Tripartite organization of brain state dynamics underlying spoken narrative comprehension eLife speech comprehension brain dynamics HMM |
| title | Tripartite organization of brain state dynamics underlying spoken narrative comprehension |
| title_full | Tripartite organization of brain state dynamics underlying spoken narrative comprehension |
| title_fullStr | Tripartite organization of brain state dynamics underlying spoken narrative comprehension |
| title_full_unstemmed | Tripartite organization of brain state dynamics underlying spoken narrative comprehension |
| title_short | Tripartite organization of brain state dynamics underlying spoken narrative comprehension |
| title_sort | tripartite organization of brain state dynamics underlying spoken narrative comprehension |
| topic | speech comprehension brain dynamics HMM |
| url | https://elifesciences.org/articles/99997 |
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