Dynamics of Brain Lateralization and Genetic Underpinnings during Chinese Natural Speech Processing

2336 

Abstract Submission 

Ruohan Zhang¹, Shujie Geng², Xiaoqing Zheng², Wanwan Guo², Chun-Yi Lo³, Jiaying Zhang⁴, Xiao Chang², Xinran Wu⁵, Jie Zhang⁶, Miao Cao², Jianfeng Feng⁷

¹University of Warwick, Coventry, West Midlands, ²Fudan University, Shanghai, Shanghai, ³Chung Yuan Christian University, Taoyuan, Chinese Taipei, ⁴Beijing University of Posts and Telecommunications, Beijing, Beijing, ⁵Institute of Science and Technology for Brain-inspired Intelligence, Fudan University, Shanghai, Shanghai, ⁶Institute of Science and Technology for Brain-inspired Intelligence (ISTBI), Shanghai, Shanghai, ⁷Institute of Science and Technology for Brain inspired Intelligence, Shanghai, Shanghai

Ruohan Zhang  
University of Warwick
Coventry, West Midlands

Shujie Geng  
Fudan University
Shanghai, Shanghai

Xiaoqing Zheng  
Fudan University
Shanghai, Shanghai

Wanwan Guo  
Fudan University
Shanghai, Shanghai

Chun-Yi Zac Lo  
Chung Yuan Christian University
Taoyuan, Chinese Taipei

Jiaying Zhang  
Beijing University of Posts and Telecommunications
Beijing, Beijing

Xiao Chang  
Fudan University
Shanghai, Shanghai

Xinran Wu  
Institute of Science and Technology for Brain-inspired Intelligence, Fudan University
Shanghai, Shanghai

Jie Zhang  
Institute of Science and Technology for Brain-inspired Intelligence (ISTBI)
Shanghai, Shanghai

Miao Cao  
Fudan University
Shanghai, Shanghai

Jianfeng Feng  
Institute of Science and Technology for Brain inspired Intelligence
Shanghai, Shanghai

One notable aspect of language processing is brain lateralization, as the language system was traditionally assumed to be situated mainly in the left hemisphere, enhancing efficiency in multitask performance and reducing redundancy in neural organization. Nevertheless, lateralization has traditionally been treated as a static feature of the human brain. In a recent study, Wu et al. investigated dynamic lateralization in the brain in the resting state and its association with language functions and cognitive flexibility. This work suggests the potential of exploring dynamic lateralization across the whole brain during language processing. Furthermore, the impact of sex and contextual factors on dynamic lateralization patterns throughout the brain during language processing remains largely unknown.

We acquired fMRI data using an ultrahigh-field 7T Siemens Terra MR scanner with a cohort of 20 participants (with a mean age of 23.7 ± 1.8 years and 10 females for sex balance) while they performed a Chinese language natural listening task. During the task, all participants listened to two-hour narratives that replicated authentic language to simulate language processing in real-life situations. For the analyses, we employed a data-driven approach that combines a sliding window technique with the global signal-based laterality index to identify recurring whole-brain dynamic lateralization states. Then, we examined the spatial and temporal properties of the states as well as influences of sex and content. Next, we explored the genetic underpinnings of the observed dynamic lateralization states with publicly available postmortem brain-wide gene expression data. Finally, using resting-state fMRI data from the Human Connectome Project (HCP) cohort, we investigated whether the properties of the dynamic lateralization states observed during the Chinese natural listening task are related to inherent lateralization patterns.

We investigated whole-brain functional dynamic lateralization patterns during Chinese language processing and potential sex disparities using functional MRI data of 20 subjects listening to narrative stories in a 7T MRI scanner. Our findings revealed two distinct dynamic lateralization states, with areas of the language system consistently exhibiting left-lateralized and converse lateralization patterns for both association areas and primary sensorimotor areas. These two states, characterized by areas of higher-order systems exhibiting left- or right-lateralization, corresponded to the processing of rational and emotional contents. We observed pronounced inclinations towards the former state in males and the latter state in females, especially during the processing of rational content. Finally, genetic analysis revealed that the sex differences in lateralization states were potentially influenced by sex hormones.

Our study provides valuable insights into the dynamic nature of brain lateralization during Chinese language processing. The identification of two distinct lateralization states improves our understanding of interhemispheric coordination during language processing, emphasizing the dynamic shift in higher-order cognitive functions between left and right lateralization patterns. Furthermore, the associations of these lateralization states with sex differences and the processed content (emotional or rational content) offer insights into sex-specific patterns in language processing. Moreover, our genetic-level analyses suggest that the observed sex differences in language lateralization may be influenced by sex hormones. Future research should focus on replicating and expanding our findings utilizing larger and more diverse sample populations, exploring different age groups, and investigating the functional significance of the observed dynamic lateralization states. This would advance our understanding of language processing mechanisms and their relevance in clinical and cognitive contexts.

Language Comprehension and Semantics

Language Other ²

Connectivity (eg. functional, effective, structural)

fMRI Connectivity and Network Modeling

BOLD fMRI ¹

FUNCTIONAL MRI

Language