Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: A simultaneous EEG-fMRI study

• Published in: NEUROIMAGE Vol. 293; p. 120629
• Main Authors: Zhang, Wei, Jiang, Muyun, Teo, Kok Ann Colin, Bhuvanakantham, Raghavan, Fong, LaiGuan, Sim, Wei Khang Jeremy, Guo, Zhiwei, Foo, Chuan Huat Vince, Chua, Rong Hui Jonathan, Padmanabhan, Parasuraman, Leong, Victoria, Lu, Jia, Gulyás, Balázs, Guan, Cuntai
• Format: Journal Article Publication
• Language: English
• Published: United States Elsevier Inc 01.06.2024; Elsevier Limited; Elsevier
• Subjects: Aphasia; Biochips; Brain; Brain mapping; Cognitive ability; Computer applications; Covert speech; EEG; Electroencephalography; Experiments; Functional connectivity; Functional magnetic resonance imaging; Implants; Left putamen; Localization; Magnetic resonance imaging; Medical imaging; Neural networks; Neuroimaging; Overt speech; Precentral gyrus; Putamen; Scanners; Simultaneous EEG-fMRI; Speaking; Speech; Speech disorders; Supplementary motor area; Tomography; Covert speech; Functional connectivity; Left putamen; Overt speech; Simultaneous EEG-fMRI
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2024.120629

•Utilized simultaneous EEG-fMRI to compare the precise spatiotemporal brain dynamics between covert speech (CS) and overt speech (OS).•Identified earlier event-locked EEG activation in the left putamen for CS compared with OS.•Identified inhibited functional connectivity between the left putamen and speech-related regions in the dominant hemisphere for CS compared with OS.•Verified significant effect pathways from the spatiotemporal brain dynamics towards CS using path analysis. 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.