Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss
Background and ObjectiveHearing loss (HL) is one of the modifiable risk factors for Alzheimer's disease (AD). However, the underlying mechanism behind HL in AD remains elusive. A possible mechanism is cognitive load hypothesis, which postulates that over-processing of degraded auditory signals...
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| Format: | Article |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Aging Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnagi.2021.772136/full |
| _version_ | 1830379687632699392 |
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| author | Luwei Hong Qingze Zeng Kaicheng Li Xiao Luo Xiaopei Xu Xiaocao Liu Zheyu Li Yanv Fu Yanbo Wang Tianyi Zhang Yanxing Chen Zhirong Liu Peiyu Huang Minming Zhang |
| author_facet | Luwei Hong Qingze Zeng Kaicheng Li Xiao Luo Xiaopei Xu Xiaocao Liu Zheyu Li Yanv Fu Yanbo Wang Tianyi Zhang Yanxing Chen Zhirong Liu Peiyu Huang Minming Zhang |
| author_sort | Luwei Hong |
| collection | DOAJ |
| description | Background and ObjectiveHearing loss (HL) is one of the modifiable risk factors for Alzheimer's disease (AD). However, the underlying mechanism behind HL in AD remains elusive. A possible mechanism is cognitive load hypothesis, which postulates that over-processing of degraded auditory signals in the auditory cortex leads to deficits in other cognitive functions. Given mild cognitive impairment (MCI) is a prodromal stage of AD, untangling the association between HL and MCI might provide insights for potential mechanism behind HL.MethodsWe included 85 cognitively normal (CN) subjects with no hearing loss (NHL), 24 CN with HL, 103 mild cognitive impairment (MCI) patients with NHL, and 23 MCI with HL from the ADNI database. All subjects underwent resting-state functional MRI and neuropsychological scale assessments. Fractional amplitude of low-frequency fluctuation (fALFF) was used to reflect spontaneous brain activity. The mixed-effects analysis was applied to explore the interactive effects between HL and cognitive status (GRF corrected, voxel p-value <0.005, cluster p-value < 0.05, two-tailed). Then, the FDG data was included to further reflect the regional neuronal abnormalities. Finally, Pearson correlation analysis was performed between imaging metrics and cognitive scores to explore the clinical significance (Bonferroni corrected, p < 0.05).ResultsThe interactive effects primarily located in the left superior temporal gyrus (STG) and bilateral inferior temporal gyrus (ITG). Post-hoc analysis showed that NC with HL had lower fALFF in bilateral ITG compared to NC with NHL. NC with HL had higher fALFF in the left STG and decreased fALFF in bilateral ITG compared to MCI with HL. In addition, NC with HL had lower fALFF in the right ITG compared to MCI with NHL. Correlation analysis revealed that fALFF was associated with MMSE and ADNI-VS, while SUVR was associated with MMSE, MoCA, ADNI-EF and ADNI-Lan.ConclusionHL showed different effects on NC and MCI stages. NC had increased spontaneous brain activity in auditory cortex while decreased activity in the ITG. Such pattern altered with disease stage changing and manifested as decreased activity in auditory cortex along with increased activity in ITG in MCI. This suggested that the cognitive load hypothesis may be the underlying mechanism behind HL. |
| first_indexed | 2024-12-20T09:15:36Z |
| format | Article |
| id | doaj.art-582eaba3e0674cd7bc60a529124adfd2 |
| institution | Directory Open Access Journal |
| issn | 1663-4365 |
| language | English |
| last_indexed | 2024-12-20T09:15:36Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Aging Neuroscience |
| spelling | doaj.art-582eaba3e0674cd7bc60a529124adfd22022-12-21T19:45:26ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652022-01-011310.3389/fnagi.2021.772136772136Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing LossLuwei Hong0Qingze Zeng1Kaicheng Li2Xiao Luo3Xiaopei Xu4Xiaocao Liu5Zheyu Li6Yanv Fu7Yanbo Wang8Tianyi Zhang9Yanxing Chen10Zhirong Liu11Peiyu Huang12Minming Zhang13Department of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, Tongde Hospital of Zhejiang Province, Hangzhou, ChinaDepartment of Neurology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, ChinaBackground and ObjectiveHearing loss (HL) is one of the modifiable risk factors for Alzheimer's disease (AD). However, the underlying mechanism behind HL in AD remains elusive. A possible mechanism is cognitive load hypothesis, which postulates that over-processing of degraded auditory signals in the auditory cortex leads to deficits in other cognitive functions. Given mild cognitive impairment (MCI) is a prodromal stage of AD, untangling the association between HL and MCI might provide insights for potential mechanism behind HL.MethodsWe included 85 cognitively normal (CN) subjects with no hearing loss (NHL), 24 CN with HL, 103 mild cognitive impairment (MCI) patients with NHL, and 23 MCI with HL from the ADNI database. All subjects underwent resting-state functional MRI and neuropsychological scale assessments. Fractional amplitude of low-frequency fluctuation (fALFF) was used to reflect spontaneous brain activity. The mixed-effects analysis was applied to explore the interactive effects between HL and cognitive status (GRF corrected, voxel p-value <0.005, cluster p-value < 0.05, two-tailed). Then, the FDG data was included to further reflect the regional neuronal abnormalities. Finally, Pearson correlation analysis was performed between imaging metrics and cognitive scores to explore the clinical significance (Bonferroni corrected, p < 0.05).ResultsThe interactive effects primarily located in the left superior temporal gyrus (STG) and bilateral inferior temporal gyrus (ITG). Post-hoc analysis showed that NC with HL had lower fALFF in bilateral ITG compared to NC with NHL. NC with HL had higher fALFF in the left STG and decreased fALFF in bilateral ITG compared to MCI with HL. In addition, NC with HL had lower fALFF in the right ITG compared to MCI with NHL. Correlation analysis revealed that fALFF was associated with MMSE and ADNI-VS, while SUVR was associated with MMSE, MoCA, ADNI-EF and ADNI-Lan.ConclusionHL showed different effects on NC and MCI stages. NC had increased spontaneous brain activity in auditory cortex while decreased activity in the ITG. Such pattern altered with disease stage changing and manifested as decreased activity in auditory cortex along with increased activity in ITG in MCI. This suggested that the cognitive load hypothesis may be the underlying mechanism behind HL.https://www.frontiersin.org/articles/10.3389/fnagi.2021.772136/fullhearing lossAlzheimer's diseasemild cognitive impairmentresting-state functional MRIfractional amplitude of low-frequency fluctuation |
| spellingShingle | Luwei Hong Qingze Zeng Kaicheng Li Xiao Luo Xiaopei Xu Xiaocao Liu Zheyu Li Yanv Fu Yanbo Wang Tianyi Zhang Yanxing Chen Zhirong Liu Peiyu Huang Minming Zhang Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss Frontiers in Aging Neuroscience hearing loss Alzheimer's disease mild cognitive impairment resting-state functional MRI fractional amplitude of low-frequency fluctuation |
| title | Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss |
| title_full | Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss |
| title_fullStr | Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss |
| title_full_unstemmed | Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss |
| title_short | Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss |
| title_sort | intrinsic brain activity of inferior temporal region increased in prodromal alzheimer s disease with hearing loss |
| topic | hearing loss Alzheimer's disease mild cognitive impairment resting-state functional MRI fractional amplitude of low-frequency fluctuation |
| url | https://www.frontiersin.org/articles/10.3389/fnagi.2021.772136/full |
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