Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study
Covert speech (CS) refers to speaking internally to oneself without producing any sound or movement. CS is involved in multiple cognitive functions and disorders. Reconstructing CS content by brain-computer interface (BCI) is also an emerging technique. However, it is still controversial whether CS...
| Main Authors: | , , , , , , , , , , , , , |
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| Other Authors: | |
| Format: | Journal Article |
| Language: | English |
| Published: |
2024
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| Subjects: | |
| Online Access: | https://hdl.handle.net/10356/178883 |
| _version_ | 1826126036044087296 |
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| author | Zhang, Wei Jiang, Muyun Teo, Colin Kok Ann Bhuvanakantham, Raghavan Fong, Lai Guan Sim, Jeremy Wei Khang Guo, Zhiwei Foo, Vince Chuan Huat Chua, Jonathan Rong Hui Padmanabhan, Parasuraman Leong, Victoria Lu, Jia Gulyás, Balázs Guan, Cuntai |
| author2 | School of Computer Science and Engineering |
| author_facet | School of Computer Science and Engineering Zhang, Wei Jiang, Muyun Teo, Colin Kok Ann Bhuvanakantham, Raghavan Fong, Lai Guan Sim, Jeremy Wei Khang Guo, Zhiwei Foo, Vince Chuan Huat Chua, Jonathan Rong Hui Padmanabhan, Parasuraman Leong, Victoria Lu, Jia Gulyás, Balázs Guan, Cuntai |
| author_sort | Zhang, Wei |
| collection | NTU |
| description | Covert speech (CS) refers to speaking internally to oneself without producing any sound or movement. CS is involved in multiple cognitive functions and disorders. Reconstructing CS content by brain-computer interface (BCI) is also an emerging technique. However, it is still controversial whether CS is a truncated neural process of overt speech (OS) or involves independent patterns. Here, we performed a word-speaking experiment with simultaneous EEG-fMRI. It involved 32 participants, who generated words both overtly and covertly. By integrating spatial constraints from fMRI into EEG source localization, we precisely estimated the spatiotemporal dynamics of neural activity. During CS, EEG source activity was localized in three regions: the left precentral gyrus, the left supplementary motor area, and the left putamen. Although OS involved more brain regions with stronger activations, CS was characterized by an earlier event-locked activation in the left putamen (peak at 262 ms versus 1170 ms). The left putamen was also identified as the only hub node within the functional connectivity (FC) networks of both OS and CS, while showing weaker FC strength towards speech-related regions in the dominant hemisphere during CS. Path analysis revealed significant multivariate associations, indicating an indirect association between the earlier activation in the left putamen and CS, which was mediated by reduced FC towards speech-related regions. These findings revealed the specific spatiotemporal dynamics of CS, offering insights into CS mechanisms that are potentially relevant for future treatment of self-regulation deficits, speech disorders, and development of BCI speech applications. |
| first_indexed | 2024-10-01T06:46:10Z |
| format | Journal Article |
| id | ntu-10356/178883 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T06:46:10Z |
| publishDate | 2024 |
| record_format | dspace |
| spelling | ntu-10356/1788832024-07-12T15:36:15Z Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study Zhang, Wei Jiang, Muyun Teo, Colin Kok Ann Bhuvanakantham, Raghavan Fong, Lai Guan Sim, Jeremy Wei Khang Guo, Zhiwei Foo, Vince Chuan Huat Chua, Jonathan Rong Hui Padmanabhan, Parasuraman Leong, Victoria Lu, Jia Gulyás, Balázs Guan, Cuntai School of Computer Science and Engineering Lee Kong Chian School of Medicine (LKCMedicine) Interdisciplinary Graduate School (IGS) School of Social Sciences National University Health System DSO National Laboratories, Singapore Yong Loo Lin School of Medicine, NUS Cognitive Neuroimaging Centre Medicine, Health and Life Sciences Covert speech Functional connectivity Covert speech (CS) refers to speaking internally to oneself without producing any sound or movement. CS is involved in multiple cognitive functions and disorders. Reconstructing CS content by brain-computer interface (BCI) is also an emerging technique. However, it is still controversial whether CS is a truncated neural process of overt speech (OS) or involves independent patterns. Here, we performed a word-speaking experiment with simultaneous EEG-fMRI. It involved 32 participants, who generated words both overtly and covertly. By integrating spatial constraints from fMRI into EEG source localization, we precisely estimated the spatiotemporal dynamics of neural activity. During CS, EEG source activity was localized in three regions: the left precentral gyrus, the left supplementary motor area, and the left putamen. Although OS involved more brain regions with stronger activations, CS was characterized by an earlier event-locked activation in the left putamen (peak at 262 ms versus 1170 ms). The left putamen was also identified as the only hub node within the functional connectivity (FC) networks of both OS and CS, while showing weaker FC strength towards speech-related regions in the dominant hemisphere during CS. Path analysis revealed significant multivariate associations, indicating an indirect association between the earlier activation in the left putamen and CS, which was mediated by reduced FC towards speech-related regions. These findings revealed the specific spatiotemporal dynamics of CS, offering insights into CS mechanisms that are potentially relevant for future treatment of self-regulation deficits, speech disorders, and development of BCI speech applications. Agency for Science, Technology and Research (A*STAR) Nanyang Technological University Published version W.Z. and V.L. are supported by the RIE2025 Human Potential Programme Prenatal/Early Childhood Grant (H22P0M0002), administered by A*STAR. This work was supported by funding from the Cognitive Neuroimaging Centre, NTU Shared Research Facility (D821/CoNiC), Ageing Research Institute for Society and Education (ARISE/2017/16) and DSO National Laboratories (DSOCL21193). 2024-07-10T01:54:27Z 2024-07-10T01:54:27Z 2024 Journal Article Zhang, W., Jiang, M., Teo, C. K. A., Bhuvanakantham, R., Fong, L. G., Sim, J. W. K., Guo, Z., Foo, V. C. H., Chua, J. R. H., Padmanabhan, P., Leong, V., Lu, J., Gulyás, B. & Guan, C. (2024). Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study. NeuroImage, 293, 120629-. https://dx.doi.org/10.1016/j.neuroimage.2024.120629 1053-8119 https://hdl.handle.net/10356/178883 10.1016/j.neuroimage.2024.120629 38697588 2-s2.0-85192008759 293 120629 en H22P0M0002 D821/CoNiC ARISE/2017/16 DSOCL21193 NeuroImage © 2024 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). application/pdf |
| spellingShingle | Medicine, Health and Life Sciences Covert speech Functional connectivity Zhang, Wei Jiang, Muyun Teo, Colin Kok Ann Bhuvanakantham, Raghavan Fong, Lai Guan Sim, Jeremy Wei Khang Guo, Zhiwei Foo, Vince Chuan Huat Chua, Jonathan Rong Hui Padmanabhan, Parasuraman Leong, Victoria Lu, Jia Gulyás, Balázs Guan, Cuntai Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study |
| title | Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study |
| title_full | Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study |
| title_fullStr | Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study |
| title_full_unstemmed | Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study |
| title_short | Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: a simultaneous EEG-fMRI study |
| title_sort | revealing the spatiotemporal brain dynamics of covert speech compared with overt speech a simultaneous eeg fmri study |
| topic | Medicine, Health and Life Sciences Covert speech Functional connectivity |
| url | https://hdl.handle.net/10356/178883 |
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