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Abnormal functional connectivity and degree centrality in anterior cingulate cortex in patients with long-term sensorineural hearing loss

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Abstract

Wide-ranging functional remodeling is involved in sensorineural hearing loss (SNHL), which has been demonstrated to have accumulated risk of cognitive and emotional dysfunction. Anterior cingulate cortex (ACC) has close connections with the auditory area and plays a vital role in regulating the cognitive, emotional and auditory processing. However, the functional reorganization of the ACC and its associations with potential cognitive and emotional impairments involved in SNHL have never been explored. Thirty-five patients with long-term bilateral SNHL and thirty-five well-matched healthy controls were recruited for this study. We analyzed resting-state functional MRI data and neuropsychological test scores from these participants. Functional connectivity of the ACC subdivisions, voxel-wise degree centrality (DC) and intra−/internetwork connectivity were computed to evaluate the functional changes related to cognitive, emotional and multiple sensory functions. ANCOVA and post hoc analyses were conducted to identify differences between normal controls and patients for each measure. Widespread alterations of functional coupling with the subdivisions of the ACC were observed in regions involved in cognitive, emotional and multiple sensory processing, particularly within the cingulo-opercular network (CON), default mode network (DMN) and auditory network (AN) in the SNHL patients. Outstandingly increased DC was found in the ACC. Network analyses showed significant intra- and inter-network hypo-synchronization in the SNHL patients. Importantly, the functional alterations were associated with the anxiety states and the processing speed. The functional reorganization in the ACC and the disturbance of intrinsic multiple network functional connectivity among the CON, DMN, and AN were found in the SNHL patient, which might shed more lights on potential substrates underlying the cognitive and emotional impairments related to the SNHL.

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (NOs. 81520108015 and 81230034), the Fundamental Research Funds for the Central Universities (NO. 2242018 k30004) and the National Key Basic Research Program of China (NOs. 2013CB733800 and 2013CB733803). Y. Luan conducted the experiments, recruited the participants, analyzed the data, and wrote the paper; C. Wang helped with the integration of the data; Y. Jiao, T. Tang and C. Lu helped with the analyses of the data. J. Zhang helped the data collection. R. Salvi provided suggestions and guidance in the discussion. G.J. Teng directed this study, designed the research and gave key advice.

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Authors and Affiliations

  1. Jiangsu Key Laboratory of Molecular and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School of Southeast University, Nanjing, 210009, China

    Ying Luan, Congxiao Wang, Yun Jiao, Tianyu Tang, Jian Zhang, Chunqiang Lu & Gao-Jun Teng

  2. Center for Hearing and Deafness, University at Buffalo, State University of New York, Buffalo, NY, 14214, USA

    Richard Salvi

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  1. Ying Luan
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Correspondence to Gao-Jun Teng.

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All the authors have approved the manuscript. There are no potential conflicts of interest to declare. All the participants provided written informed consent before the experiment in the current study, which was approved by the Research Ethics Committee of the Affiliated Zhongda Hospital of Southeast University.

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This research was approved by the Ethics Committee of the Affiliated Zhongda Hospital of Southeast University, and all the participants provided written informed consent before the experiment. All the procedures were conducted in accordance with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

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Luan, Y., Wang, C., Jiao, Y. et al. Abnormal functional connectivity and degree centrality in anterior cingulate cortex in patients with long-term sensorineural hearing loss. Brain Imaging and Behavior 14, 682–695 (2020). https://doi.org/10.1007/s11682-018-0004-0

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