Share:
Share this content in WeChat
X
[Chinese] [PDF] 190 31
Clinical Article
The relationship between the abnormality of functional gradient and anxiety-depression disorders in patients with bilateral sudden sensorineural hearing loss
ZHU Haixue  LI Biao  FANG Zihuai  FENG Yuan  YIN Xindao  XU Xiaomin 

DOI:10.12015/issn.1674-8034.2025.08.001.


[Abstract] Objective Sudden sensorineural hearing loss is one of the otologic emergency diseases which often induces anxiety-depression like emotional impairments. But how sudden sensorineural hearing loss promotes the occurrence of emotional abnormalities is unclear. This study used brain functional gradient technique to explore the relationship between sudden sensorineural hearing loss and emotional impairments.Materials and Methods We evaluated hearing, multi-dimensional neural scales, and resting-state brain function gradients in 44 patients with sudden sensorineural hearing loss and 40 healthy controls. Functional connectivity gradients were used to identify alterations in cortical connectivity gradients induced by sudden bilateral sensorineural hearing loss. Statistical parametric mapping 12 (SPM12) was used to process functional magnetic resonance imaging (fMRI) data, and Pearson's correlation was used to calculate the correlation between fMRI data and anxiety-depression like emotional impairments based on statistical package for the social sciences 22.0 (SPSS 22.0) software.Results Patients with sudden sensorineural hearing loss and healthy controls were well matched for age, gender and education level. The mean hearing thresholds of both ears in patients were significantly higher than healthy controls. The scores of anxiety and depression scales were significantly higher in patients with sudden sensorineural hearing loss. The results showed no significant difference in the primary gradient between the two groups. At the network level, patients with sudden sensorineural hearing loss showed no significant difference in the primary gradient. However, at the nodal level, increased gradient was observed in the left precuneus, while decreased gradients were observed in the left, right calcarine fissure and surrounding cortex, right parahippocampal gyrus and left medial superior frontal gyrus (P < 0.001). Moreover, there was a negative correlation between anxiety and the gradient of calcarine fissure and surrounding cortex in patients with sudden sensorineural hearing loss (r = -0.413, P = 0.005).Conclusions The functional gradient changes of brain regions in patients with sudden sensorineural hearing loss may help to clarify the neuropathological basis of emotional impairments in patients with sudden sensorineural hearing loss.
[Keywords] sudden sensorineural hearing loss;neural imaging;magnetic resonance imaging;functional gradient;anxiety;depression

ZHU Haixue1   LI Biao2   FANG Zihuai3   FENG Yuan3   YIN Xindao3   XU Xiaomin3*  

1 Department of Radiology, Taikang Xianlin Drum Tower Hospital, Afiliated Hospital of Medical School, Nanjing University, Nanjing 210046, China

2 Department of Otolaryngology, Nanjing First Hospital, Nanjing Medical University, Nanjing 210006, China

3 Department of Radiology, Nanjing First Hospital, Nanjing Medical University, Nanjing 210006, China

Corresponding author: XU X M, E-mail: xmxu15@163.com

Conflicts of interest   None.

Received  2025-02-24
Accepted  2025-08-08
DOI: 10.12015/issn.1674-8034.2025.08.001
DOI:10.12015/issn.1674-8034.2025.08.001.

[1]
XIE W, KARPETA N, TONG B, et al. Comorbidities and laboratory changes of sudden sensorineural hearing loss: a review[J/OL]. Front Neurol, 2023, 14: 1142459 [2025-02-23]. https://pmc.ncbi.nlm.nih.gov/articles/PMC10151530. DOI: 10.3389/fneur.2023.1142459.
[2]
CHEN Y H, YOUNG Y H. Bilateral simultaneous sudden sensorineural hearing loss[J]. J Neurol Sci, 2016, 362: 139-143. DOI: 10.1016/j.jns.2016.01.029.
[3]
CHO Y, KIM J, OH S J, et al. Clinical features and prognosis of severe-to-profound sudden sensorineural hearing loss[J/OL]. Am J Otolaryngol, 2022, 43(3): 103455 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/35398740. DOI: 10.1016/j.amjoto.2022.103455.
[4]
CHEN Y C, LIU Y H, KANG B H, et al. Hyperbaric oxygen therapy improves the effects of systemic steroid therapy for sudden sensorineural hearing loss[J/OL]. Heliyon, 2025, 11(2): e42025 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/35398740. DOI: 10.1016/j.heliyon.2025.e42025.
[5]
TOMAZ A, PERON K A, SUZUKI F A B, et al. Standard and Extend High-Frequency Audiometry in Sudden Sensorineural Hearing Loss: Impacts on Tinnitus and Mental Health[J/OL]. Otol Neurotol, 2024, 45(5): e366-e375 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/38511269. DOI: 10.1097/MAO.0000000000004168.
[6]
SLADE K, PLACK C J, NUTTALL H E. The Effects of Age-Related Hearing Loss on the Brain and Cognitive Function[J]. Trends Neurosci, 2020, 43(10): 810-821. DOI: 10.1016/j.tins.2020.07.005.
[7]
THIEBAUT DE SCHOTTEN M, FORKEL S J. The emergent properties of the connected brain[J]. Science, 2022, 378(6619): 505-510. DOI: 10.1126/science.abq2591.
[8]
LI Y T, BAI K, LI G Z, et al. Functional to structural plasticity in unilateral sudden sensorineural hearing loss: neuroimaging evidence[J/OL]. Neuroimage, 2023, 283: 120437 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/37924896. DOI: 10.1016/j.neuroimage.2023.120437.
[9]
LI J, ZOU Y, KONG X, et al. Exploring functional connectivity alterations in sudden sensorineural hearing loss: A multilevel analysis[J/OL]. Brain Res, 2024, 1824: 148677 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/37924896. DOI: 10.1016/j.brainres.2023.148677.
[10]
HUNTENBURG J M, BAZIN P L, GOULAS A, et al. A Systematic Relationship Between Functional Connectivity and Intracortical Myelin in the Human Cerebral Cortex[J]. Cereb Cortex, 2017, 27(2): 981-997. DOI: 10.1093/cercor/bhx030.
[11]
BURT J B, DEMIRTAS M, ECKNER W J, et al. Hierarchy of transcriptomic specialization across human cortex captured by structural neuroimaging topography[J]. Nat Neurosci, 2018, 21(9): 1251-1259. DOI: 10.1038/s41593-018-0195-0.
[12]
MARGULIES D S, GHOSH S S, GOULAS A, et al. Situating the default-mode network along a principal gradient of macroscale cortical organization[J]. Proc Natl Acad Sci U S A, 2016, 113(44): 12574-12579. DOI: 10.1073/pnas.1608282113.
[13]
Chinese Journal of Otorhinolaryngology-Head and Neck Surgery Editorial Board, Chinese Medical Association Otorhinolaryngology-Head and Neck Surgery Branch. Guidelines for the Diagnosis and Treatment of Sudden Deafness (2015)[J]. Chinese Journal of Otorhinolaryngology Head and Neck Surgery, 2015, 50(6): 443-447. DOI: 10.3760/cma.j.issn.1673-0860.2015.06.002.
[14]
ESTEBAN O, MARKIEWICZ C J, BLAIR R W, et al. fMRIPrep: a robust preprocessing pipeline for functional MRI[J]. Nat Methods, 2019, 16(1): 111-116. DOI: 10.1038/s41592-018-0235-4.
[15]
PAQUOLA C, DE WAEL R VOS, WAGSTYL K, et al. Microstructural and functional gradients are increasingly dissociated in transmodal cortices[J/OL]. PLoS Biol, 2019, 17(5): e3000284 [2025-02-23]. https://pmc.ncbi.nlm.nih.gov/articles/PMC6544318. DOI: 10.1371/journal.pbio.3000284.
[16]
YEO B T T, KRIENEN F M, SEPULCRE J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity[J]. J Neurophysiol, 2011, 106(3): 1125-1165. DOI: 10.1152/jn.00338.2011.
[17]
TONG Z, ZHANG J, XING C, et al. Reorganization of the cortical connectome functional gradient in age-related hearing loss[J/OL]. Neuroimage, 2023, 284: 120475 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/38013009. DOI: 10.1016/j.neuroimage.2023.120475.
[18]
LI B, XU X M, WU Y Q, et al. The relationship between changes in functional connectivity gradients and cognitive-emotional disorders in sudden sensorineural hearing loss[J/OL]. Brain Commun, 2024, 6(5): fcae317 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/39318785. DOI: 10.1093/braincomms/fcae317.
[19]
DADARIO N B, SUGHRUE M E. The functional role of the precuneus[J]. Brain, 2023, 146(9): 3598-3607. DOI: 10.1093/brain/awad181.
[20]
ROSEMANN S, RAUSCHECKER J P. Neuroanatomical alterations in middle frontal gyrus and the precuneus related to tinnitus and tinnitus distress[J/OL]. Hear Res, 2022, 424: 108595 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/35963187. DOI: 10.1016/j.heares.2022.108595.
[21]
REN F, MA W, LI M, et al. Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study[J/OL]. Front Neurosci, 2018, 12: 744 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/30405333. DOI: 10.3389/fnins.2018.00744.
[22]
WANG H F, ZHANG W, ROLLS E T, et al. Hearing impairment is associated with cognitive decline, brain atrophy and tau pathology[J/OL]. EBioMedicine, 2022, 86: 104336 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/36356475. DOI: 10.1016/j.ebiom.2022.104336.
[23]
CHEN J W, HU B, QIN P, et al. Altered Brain Activity and Functional Connectivity in Unilateral Sudden Sensorineural Hearing Loss[J/OL]. Neural Plast, 2020, 2020: 9460364 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/33029130. DOI: 10.1155/2020/9460364.
[24]
LEE S Y, CHOI B Y, KOO J W, et al. Cortical Oscillatory Signatures Reveal the Prerequisites for Tinnitus Perception: A Comparison of Subjects With Sudden Sensorineural Hearing Loss With and Without Tinnitus[J/OL]. Front Neurosci, 2020, 14: 596647 [2025-02-23]. https://pmc.ncbi.nlm.nih.gov/articles/PMC7731637. DOI: 10.3389/fnins.2020.596647.
[25]
LIU Y, ZHANG J, JIANG Z, et al. Organization of corticocortical and thalamocortical top-down inputs in the primary visual cortex[J/OL]. Nat Commun, 2024, 15(1): 4495 [2025-02-23]. https://pmc.ncbi.nlm.nih.gov/articles/PMC11130321. DOI: 10.1038/s41467-024-48924-8.
[26]
LIU X, SHI L, LI E, et al. Associations of hearing loss and structural changes in specific cortical regions: a Mendelian randomization study[J/OL]. Cereb Cortex, 2024, 34(3): bhae084 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/38494888. DOI: 10.1093/cercor/bhae084.
[27]
SONG J, WANG Y, OUYANG F, et al. Differences in brain functional connectivity between tinnitus with or without hearing loss[J]. Neuroreport, 2024, 35(11): 712-720. DOI: 10.1097/WNR.0000000000002057.
[28]
YIN Y, LYU X, ZHOU J, et al. Cerebral cortex functional reorganization in preschool children with congenital sensorineural hearing loss: a resting-state fMRI study[J/OL]. Front Neurol, 2024, 15: 1423956 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/38988601. DOI: 10.3389/fneur.2024.1423956.
[29]
ZHANG X, LAI H, LI Q, et al. Disrupted brain gray matter connectome in social anxiety disorder: a novel individualized structural covariance network analysis[J]. Cereb Cortex, 2023, 33(16): 9627-9638. DOI: 10.1093/cercor/bhad231.
[30]
ROY O, LEVASSEUR-MOREAU J, RENAULD E, et al. Whole-brain morphometry in Canadian soldiers with posttraumatic stress disorder[J]. Ann N Y Acad Sci, 2022, 1509(1): 37-49. DOI: 10.1111/nyas.14707.
[31]
BERGER J I, BILLIG A J, SEDLEY W, et al. What is the role of the hippocampus and parahippocampal gyrus in the persistence of tinnitus?[J/OL]. Hum Brain Mapp, 2024, 45(3): e26627 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/38376166. DOI: 10.1002/hbm.26627.
[32]
LI R, MIAO X, HAN B, LI J. Cortical thickness of the left parahippocampal cortex links central hearing and cognitive performance in aging[J]. Ann N Y Acad Sci, 2023, 1522(1): 117-125. DOI: 10.1111/nyas.14971.
[33]
PAN L, LI C, MENG L, et al. GDF1 ameliorates cognitive impairment induced by hearing loss[J]. Nat Aging, 2024, 4(4): 568-583. DOI: 10.1038/s43587-024-00592-5.
[34]
HU Y, BING D, LIU A, et al. A preliminary study of fMRI and the relationship with depression and anxiety in Meniere's patients[J/OL]. Am J Otolaryngol, 2025, 46(1): 104531 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/39667311. DOI: 10.1016/j.amjoto.2024.104531.
[35]
KIRSCHEN R M, LEAVER A M. Hearing Function Moderates Age-Related Differences in Brain Morphometry in the HCP Aging Cohort[J/OL]. Hum Brain Mapp, 2024, 45(16): e70074 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/39540247. DOI: 10.1002/hbm.70074.
[36]
LI B, XU X M, WU Y Q, et al. Disrupted Cross-Scale Network Associated With Cognitive-Emotional Disorders in Sudden Sensorineural Hearing Loss[J/OL]. CNS Neurosci Ther, 2025, 31(1): e70234 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/39868748. DOI: 10.1111/cns.70234.
[37]
LIU W Z, ZHANG W H, ZHENG Z H, et al. Identification of a prefrontal cortex-to-amygdala pathway for chronic stress-induced anxiety[J/OL]. Nat Commun, 2020, 11(1): 2221 [2025-02-23]. https://pmc.ncbi.nlm.nih.gov/articles/PMC7203160. DOI: 10.1038/s41467-020-15920-7.
[38]
HARE B D, DUMAN R S. Prefrontal cortex circuits in depression and anxiety: contribution of discrete neuronal populations and target regions[J]. Mol Psychiatry, 2020, 25(11): 2742-2758. DOI: 10.1038/s41380-020-0685-9.
[39]
WU B, CHEN Y, LONG X, et al. Altered single-subject gray matter structural networks in first-episode drug-naïve adolescent major depressive disorder[J/OL]. Psychiatry Res, 2023, 329: 115557 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/37890406. DOI: 10.1016/j.psychres.2023.115557.
[40]
KIM B H, PARK S Y, PARK C I, et al. Altered cortical thickness of the superior frontal gyrus and fusiform gyrus in individuals with subthreshold social anxiety[J/OL]. Sci Rep, 2023, 13(1): 21822 [2025-02-23]. https://pubmed.ncbi.nlm.nih.gov/38071248. DOI: 10.1038/s41598-023-49288-7.
[41]
KENWOOD M M, KALIN N H, BARBAS H. The prefrontal cortex, pathological anxiety, and anxiety disorders[J]. Neuropsychopharmacology, 2022, 47(1): 260-275. DOI: 10.1038/s41386-021-01109-z.

PREV Research progress of synthetic MRI in clinical diseases
NEXT MRI-based longitudinal assessment of hippocampal subregion volume changes during radiotherapy in nasopharyngeal carcinoma patients
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn