Brain Frequency-Specific Changes in the Spontaneous Neural Activity Are Associated With Cognitive Impairment in Patients With Presbycusis

Fuxin Ren; Wen Ma; Wei Zong; Ning Li; Xiao Li; Fuyan Li; Lili Wu; Honghao Li; Muwei Li; Fei Gao

doi:10.3389/fnagi.2021.649874

Brain Frequency-Specific Changes in the Spontaneous Neural Activity Are Associated With Cognitive Impairment in Patients With Presbycusis

Front Aging Neurosci. 2021 Jul 14:13:649874. doi: 10.3389/fnagi.2021.649874. eCollection 2021.

Authors

Fuxin Ren^{1

2}, Wen Ma³, Wei Zong^{1

2}, Ning Li^{1

2}, Xiao Li^{1

2}, Fuyan Li^{1

2}, Lili Wu⁴, Honghao Li⁵, Muwei Li⁶, Fei Gao^{1

2}

Affiliations

¹ Department of Radiology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, China.
² Department of Radiology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, China.
³ Department of Otolaryngology, The Central Hospital of Jinan City, Cheeloo College of Medicine, Shandong University, Jinan, China.
⁴ CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
⁵ Department of Neurology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, China.
⁶ Vanderbilt University Institute of Imaging Science, Nashville, TN, United States.

Abstract

Presbycusis (PC) is characterized by preferential hearing loss at high frequencies and difficulty in speech recognition in noisy environments. Previous studies have linked PC to cognitive impairment, accelerated cognitive decline and incident Alzheimer's disease. However, the neural mechanisms of cognitive impairment in patients with PC remain unclear. Although resting-state functional magnetic resonance imaging (rs-fMRI) studies have explored low-frequency oscillation (LFO) connectivity or amplitude of PC-related neural activity, it remains unclear whether the abnormalities occur within all frequency bands or within specific frequency bands. Fifty-one PC patients and fifty-one well-matched normal hearing controls participated in this study. The LFO amplitudes were investigated using the amplitude of low-frequency fluctuation (ALFF) at different frequency bands (slow-4 and slow-5). PC patients showed abnormal LFO amplitudes in the Heschl's gyrus, dorsolateral prefrontal cortex (dlPFC), frontal eye field and key nodes of the speech network exclusively in slow-4, which suggested that abnormal spontaneous neural activity in PC was frequency dependent. Our findings also revealed that stronger functional connectivity between the dlPFC and the posterodorsal stream of auditory processing, as well as lower functional coupling between the PCC and key nodes of the DMN, which were associated with cognitive impairments in PC patients. Our study might underlie the cross-modal plasticity and higher-order cognitive participation of the auditory cortex after partial hearing deprivation. Our findings indicate that frequency-specific analysis of ALFF could provide valuable insights into functional alterations in the auditory cortex and non-auditory regions involved in cognitive impairment associated with PC.

Keywords: cognitive impairment; frequency band; functional connectivity; low-frequency fluctuation; presbycusis.