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What happens “when one door is half closed, another does not open yet” for the unilateral sudden sensorineural hearing loss patients
Yuting Li1, Yuxuan Shang1, Zhuhong Chen1, Jingting Sun1, and Xiaochen Wei2
1Tangdu Hospital, Fourth Military Medical University, Xi'an, China, 2GE Healthcare, MR Research China, Beijing, Beijing, China

Synopsis

Featured alterations in dynamic brain functions, neurovascular coupling, or brain structure occurs at early-, intermediate- or late-stage of unilateral sudden sensorineural hearing loss (SSNHL) “when one door is half closed, another does not open yet”, respectively, and may serve as the neuroimaging markers for SSNHL.

Introduction

A partial cross-modal plasticity establishes after long time single sided deafness, i.e., “when one door is half closed, another opens to some extent”. Our object is to explore the whether there is cross-modal plasticity and what happens in the human brain of patients along with the disease development of unilateral sudden sensorineural hearing loss (SSNHL) “when one door is half closed, another does not open yet”

Methods

SSNHL patients were enrolled according to hearing loss at least 30 dB in three sequential frequencies in the standard pure-tone audiogram (PTA) in less than 3 days and were divided into three subgroups (early-, intermediate- or late- stage). Then, we used functional magnetic resonance imaging (fMRI), three-dimensional arterial spin labeling (3D-ASL) and three-dimensional brain volume (3D-BRAVO) magnetic resonance (MR) scanning to explore alteration of different periods in SSNHL.

Results

38 SSNHL patients and 44 health controls were enrolled. We first identified low number of transitions (NT) between varied dynamic functional network connectivity (dFNC) states (Fig. 1) and decreased connectivity between the right superior temporal gyrus (STG) and right Precuneus gyrus/ right Postcentral gyrus occurs at the early-stage SSNHL (Fig. 2). We then revealed the decreased neurovascular coupling (NVC) occurs restricted to the primary auditory cortex (left transverse temporal gyrus (TTG) and bilateral superior temporal gyrus (STG)) at the intermediate- and late-stage SSNHL (Fig. 3). These dFNC and NVC analyses advocated that cross-modal plasticity less likely occurred at the early- or intermediate-stage SSNHL. Furthermore, a significant volume decrease in right orbital part of the superior frontal gyrus (ORBsup) was observed only in the late-stage SSNHL cohort (Fig. 4A and 4B), suggesting a partial cross-modal plasticity in the emotional response occurred. Finally, only the volume of right ORBsup is robustly correlated with both disease stage and patient prognosis (Fig. 4C and 4D).

Conclusion

Our study supported the brain change occurred first within the AUD and gradually develop cross-modal plasticity along with the short-, intermediate- and late-stage SSNHL. These findings explain why short-stage SSNHL patients are with better therapeutic responses and hearing recovery. Our study shed light on potential of being translated to the clinic set to identify early-stage SSNHL patients and predict the prognosis of SSNHL patients.

Acknowledgements

The authors would like to thank Drs. Wu-Xun Cui, Si-Jie Xiu, from Department of Radiology of Tangdu Hospital, as well as Dr. Xiao-Cheng Wei from MR Research China of GE Healthcare for their outstanding technique support. Our gratitude also goes for Profs. Jin-Lian Li, Liang-Wei Chen and Jun-Ling Zhu from Department of Radiology of Tangdu Hospital for their constructive comments for this project.

References

1. Dewey RS, Hartley DE: Cortical cross-modal plasticity following deafness measured using functional near-infrared spectroscopy. Hear Res 2015, 325:55-63.

2. Qiao Y, Li X, Shen H, Zhang .X, Sun Y, Hao W, Guo B, Ni D, Gao Z, Guo H et al: Downward cross-modal plasticity in single-sided deafness. NeuroImage 2019, 197:608-617.

3. Benetti S, van Ackeren MJ, Rabini G, Zonca J, Foa V, Baruffaldi F, Rezk M, Pavani F, Rossion B, Collignon O: Functional selectivity for face processing in the temporal voice area of early deaf individuals. Proceedings of the National Academy of Sciences of the United States of America 2017, 114(31):E6437-E6446.

4. Benetti S, Zonca J, Ferrari A, Rezk M, Rabini G, Collignon O: Visual motion processing recruits regions selective for auditory motion in early deaf individuals. NeuroImage 2021, 230:117816.

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Figures

Temporal properties of dFNC of SSNHL and HC cohorts. (A) Fractional rates (FR), (B) Mean dwell time (MDT) and (C) Number of transitions (NT) were represented using violin plots. SSNHL patients had significantly higher (A) FR and (B) MDT in State 3 and (c) lower NT. Horizontal lines showed group medians and interquartile ranges. The p-value was marked on the figure, * p <0.05 (FDR corrected).

Group differences of right STG-whole-brain dFNC in State 3. (A) The right STG were identified with GICA and used in SBN analysis. (B) In State 3, SSNHL patients had lower dFNC between the right STG and right Postcentral gyrus / right Precuneus. Color map of the t value was shown. (C) We performed two sample t-test, one-way ANOVA and post-hoc t-test to report two-tail p-value. Statistical maps were thresholded at p < 0.001 at voxel level and p < 0.01 at the cluster level. ** represented significant difference at p < 0.01.

Whole-brain NVC analysis. (A) Brain regions with significant NVC alterations. Color map indicated the NVC value. (B) ALFF- CBF correlation (representing NVC) of three different brain regions between the SSNHL and HC cohorts. The solid lines represented the median of the group. (C) Comparison of NVC between subgroups of SSNHL and HC in three different regions. * p < 0.05, ** p < 0.01 (Bonferroni corrected).

Brain volume changes between SSNHL subgroups. (A) One-way ANOVA revealed significant differences of GM in right ORBsup between the four groups (red region). (B) Comparation of GM volume between HC and SSNHL subgroups revealed that there was obvious difference between HC and late-stage SSNHL patients, * p <0.05. (C) The GM volume in right ORBsup had negative correlation with the onset time of SSNHL. (D) The GM volume in right ORBsup was positively correlated with the improvement rate of PTA. The red lines represented mean volume in right ORBsup of HC.

Proc. Intl. Soc. Mag. Reson. Med. 30 (2022)
3799
DOI: https://doi.org/10.58530/2022/3799