Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss

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

doi:10.3389/fnagi.2021.772136

Intrinsic Brain Activity of Inferior Temporal Region Increased in Prodromal Alzheimer's Disease With Hearing Loss

Front Aging Neurosci. 2022 Jan 28:13:772136. doi: 10.3389/fnagi.2021.772136. eCollection 2021.

Authors

Luwei Hong¹, Qingze Zeng¹, Kaicheng Li¹, Xiao Luo¹, Xiaopei Xu¹, Xiaocao Liu¹, Zheyu Li², Yanv Fu², Yanbo Wang², Tianyi Zhang³, Yanxing Chen², Zhirong Liu², Peiyu Huang¹, Minming Zhang¹

Affiliations

¹ Department of Radiology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China.
² Department of Neurology, The 2nd Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China.
³ Department of Neurology, Tongde Hospital of Zhejiang Province, Hangzhou, China.

Abstract

Background and objective: Hearing 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.

Methods: We 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).

Results: The 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.

Conclusion: HL 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.

Keywords: Alzheimer's disease; fractional amplitude of low-frequency fluctuation; hearing loss; mild cognitive impairment; resting-state functional MRI.