Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss
BackgroundPatients with age-related hearing loss (ARHL) often struggle with tracking and locating sound sources, but the neural signature associated with these impairments remains unclear.Materials and methodsUsing a passive listening task with stimuli from five different horizontal directions in fu...
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| Format: | Article |
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Frontiers Media S.A.
2024-03-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2024.1353413/full |
| _version_ | 1797258644876689408 |
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| author | Junzhi Wu Shuai Nie Chunlin Li Xing Wang Ye Peng Jiaqi Shang Linan Diao Hongping Ding Qian Si Songjian Wang Songjian Wang Renjie Tong Yutang Li Liwei Sun Juan Zhang |
| author_facet | Junzhi Wu Shuai Nie Chunlin Li Xing Wang Ye Peng Jiaqi Shang Linan Diao Hongping Ding Qian Si Songjian Wang Songjian Wang Renjie Tong Yutang Li Liwei Sun Juan Zhang |
| author_sort | Junzhi Wu |
| collection | DOAJ |
| description | BackgroundPatients with age-related hearing loss (ARHL) often struggle with tracking and locating sound sources, but the neural signature associated with these impairments remains unclear.Materials and methodsUsing a passive listening task with stimuli from five different horizontal directions in functional magnetic resonance imaging, we defined functional regions of interest (ROIs) of the auditory “where” pathway based on the data of previous literatures and young normal hearing listeners (n = 20). Then, we investigated associations of the demographic, cognitive, and behavioral features of sound localization with task-based activation and connectivity of the ROIs in ARHL patients (n = 22).ResultsWe found that the increased high-level region activation, such as the premotor cortex and inferior parietal lobule, was associated with increased localization accuracy and cognitive function. Moreover, increased connectivity between the left planum temporale and left superior frontal gyrus was associated with increased localization accuracy in ARHL. Increased connectivity between right primary auditory cortex and right middle temporal gyrus, right premotor cortex and left anterior cingulate cortex, and right planum temporale and left lingual gyrus in ARHL was associated with decreased localization accuracy. Among the ARHL patients, the task-dependent brain activation and connectivity of certain ROIs were associated with education, hearing loss duration, and cognitive function.ConclusionConsistent with the sensory deprivation hypothesis, in ARHL, sound source identification, which requires advanced processing in the high-level cortex, is impaired, whereas the right–left discrimination, which relies on the primary sensory cortex, is compensated with a tendency to recruit more resources concerning cognition and attention to the auditory sensory cortex. Overall, this study expanded our understanding of the neural mechanisms contributing to sound localization deficits associated with ARHL and may serve as a potential imaging biomarker for investigating and predicting anomalous sound localization. |
| first_indexed | 2024-04-24T22:56:49Z |
| format | Article |
| id | doaj.art-2de68300e4ff4f7084bb1546bd01bb45 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-24T22:56:49Z |
| publishDate | 2024-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-2de68300e4ff4f7084bb1546bd01bb452024-03-18T04:37:12ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2024-03-011810.3389/fnins.2024.13534131353413Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing lossJunzhi Wu0Shuai Nie1Chunlin Li2Xing Wang3Ye Peng4Jiaqi Shang5Linan Diao6Hongping Ding7Qian Si8Songjian Wang9Songjian Wang10Renjie Tong11Yutang Li12Liwei Sun13Juan Zhang14Department of Otorhinolaryngology Head and Neck Surgery, Beijing Chaoyang Hospital, Capital Medical University, Beijing, ChinaDepartment of Otorhinolaryngology Head and Neck Surgery, Beijing Chaoyang Hospital, Capital Medical University, Beijing, ChinaSchool of Biomedical Engineering, Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Capital Medical University, Beijing, ChinaDepartment of Otorhinolaryngology Head and Neck Surgery, Beijing Chaoyang Hospital, Capital Medical University, Beijing, ChinaDepartment of Otorhinolaryngology Head and Neck Surgery, Beijing Chaoyang Hospital, Capital Medical University, Beijing, ChinaCenter of Clinical Hearing, Shandong Second Provincial General Hospital, Jinan, Shandong, ChinaDepartment of Otorhinolaryngology Head and Neck Surgery, Beijing Chaoyang Hospital, Capital Medical University, Beijing, ChinaCollege of Special Education, Binzhou Medical University, Yantai, Shandong, ChinaSchool of Cyber Science and Technology, Beihang University, Beijing, ChinaKey Laboratory of Otolaryngology, Head and Neck Surgery, Ministry of Education, Beijing Institute of Otolaryngology, Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaSchool of Biomedical Engineering, Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Capital Medical University, Beijing, ChinaSchool of Biomedical Engineering, Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Capital Medical University, Beijing, ChinaSchool of Biomedical Engineering, Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Capital Medical University, Beijing, ChinaDepartment of Otorhinolaryngology Head and Neck Surgery, Beijing Chaoyang Hospital, Capital Medical University, Beijing, ChinaBackgroundPatients with age-related hearing loss (ARHL) often struggle with tracking and locating sound sources, but the neural signature associated with these impairments remains unclear.Materials and methodsUsing a passive listening task with stimuli from five different horizontal directions in functional magnetic resonance imaging, we defined functional regions of interest (ROIs) of the auditory “where” pathway based on the data of previous literatures and young normal hearing listeners (n = 20). Then, we investigated associations of the demographic, cognitive, and behavioral features of sound localization with task-based activation and connectivity of the ROIs in ARHL patients (n = 22).ResultsWe found that the increased high-level region activation, such as the premotor cortex and inferior parietal lobule, was associated with increased localization accuracy and cognitive function. Moreover, increased connectivity between the left planum temporale and left superior frontal gyrus was associated with increased localization accuracy in ARHL. Increased connectivity between right primary auditory cortex and right middle temporal gyrus, right premotor cortex and left anterior cingulate cortex, and right planum temporale and left lingual gyrus in ARHL was associated with decreased localization accuracy. Among the ARHL patients, the task-dependent brain activation and connectivity of certain ROIs were associated with education, hearing loss duration, and cognitive function.ConclusionConsistent with the sensory deprivation hypothesis, in ARHL, sound source identification, which requires advanced processing in the high-level cortex, is impaired, whereas the right–left discrimination, which relies on the primary sensory cortex, is compensated with a tendency to recruit more resources concerning cognition and attention to the auditory sensory cortex. Overall, this study expanded our understanding of the neural mechanisms contributing to sound localization deficits associated with ARHL and may serve as a potential imaging biomarker for investigating and predicting anomalous sound localization.https://www.frontiersin.org/articles/10.3389/fnins.2024.1353413/fullaginghearing losssound localizationfunctional magnetic resonance imagingfunctional connectivity |
| spellingShingle | Junzhi Wu Shuai Nie Chunlin Li Xing Wang Ye Peng Jiaqi Shang Linan Diao Hongping Ding Qian Si Songjian Wang Songjian Wang Renjie Tong Yutang Li Liwei Sun Juan Zhang Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss Frontiers in Neuroscience aging hearing loss sound localization functional magnetic resonance imaging functional connectivity |
| title | Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss |
| title_full | Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss |
| title_fullStr | Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss |
| title_full_unstemmed | Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss |
| title_short | Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss |
| title_sort | sound localization related activation and functional connectivity of dorsal auditory pathway in relation to demographic cognitive and behavioral characteristics in age related hearing loss |
| topic | aging hearing loss sound localization functional magnetic resonance imaging functional connectivity |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2024.1353413/full |
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