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

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.

Cognition and Cognitive Reserve in Cochlear Implant Recipients

“…The close interaction between hearing loss and cognitive functions has gained attention of researchers recently ( Panza et al, 2019 ; Powell et al, 2021 ). On the one hand, neurocognitive functions have an impact on speech understanding, especially in challenging acoustic situations ( Rönnberg et al, 2013 ; Völter et al, 2020a , b ); on the other hand, several studies have pointed out the negative impact of hearing loss on cognition, both on a behavioral as well as on a neuroanatomic level ( Deal et al, 2015 ; Armstrong et al, 2020 ; Manno et al, 2021 ; Ren et al, 2021 ; Völter et al, 2021a ). A longitudinal study conducted by Lin in 2011 demonstrated that the risk of dementia within 11.9 years was elevated by 1.89 times in people with mild-hearing impairment, 3-fold in people with moderate hearing impairment, and by 4.94 times in people with severe hearing impairment ( Lin et al, 2011 ).…”

Aberrant brain functional network strength related to cognitive impairment in age-related hearing loss

“…(2) slice timing; (3) realignment for head motion correction; (4) segmentation; (5) normalization to a standard template; (6) regressing six motion parameters, six temporal derivatives, and 12 corresponding squared items using the Friston-24 parameter; (7) smoothing with 8-mm full width at halfmaximum Gaussian kernel; and (8) detrending and filtering (0.01-0.08). Subjects with a translational or rotational head motion of >2.0 mm or 2.0 • in any direction were excluded.…”

“…In terms of the global brain, cortical thinning and reduced gray matter volume have been found in ARHL subjects ( 5 , 6 ). Ren et al also found that abnormal spontaneous neural activity was frequency dependent and correlated with cognition by exploring all frequency bands of oscillation ( 7 ). Some studies have shown that the functional reorganization of the auditory cortex ( 8 ), cingulo-opercular network ( 9 ), motor ( 10 ), visual ( 11 ), and attention networks ( 12 ) in ARHL could be responsible for cognitive and neural functioning and, in turn, affect auditory processing.…”

Disrupted Topological Organization of Resting-State Functional Brain Networks in Age-Related Hearing Loss

“…Although impaired inner ear function is the main cause of ARHL, it is increasingly recognized that ARHL is also related to structural and functional changes in the central auditory pathway and other areas of the central nervous system (Kazee et al, 1995 ; Spongr et al, 1997 ; Salvi et al, 2002 ; Ouda et al, 2015 ). With the further application of functional magnetic resonance imaging (fMRI) which was based on blood oxygen level dependent (BOLD) in central nervous system abnormalities of ARHL, some studies have found that hearing loss devoted to the disrupted functional networks such as limbic network (SCLN), default mode network (DMN), executive control network (ECN), attention network (AN), and visual network (VN) (Chen et al, 2018 , 2020 ; Xing et al, 2020 , 2021a , b ; Ren et al, 2021 ). In addition, experiments have found abnormal structural and functional visual centers similar to the auditory center in ARHL (Schulte et al, 2020 ; Wei et al, 2021 ), proving that the dysfunction caused by hearing loss involves the whole brain (Benetti et al, 2021 ).…”

“…Recent studies using magnetic resonance spectroscopy (MRS) have shown decreased neurotransmitters such as gamma-aminobutyric acid (GABA) in ARHL related to age and speech in noise, indicating that the reduction of neurotransmitters in the auditory system is related to functional impairment (Gao et al, 2015 ; Dobri and Ross, 2021 ). Many fMRI studies and animal experiments have linked the decline of cognition with functional abnormalities in ARHL, as well as dementia and depression (Chen et al, 2020 ; Choi et al, 2021 ; Ren et al, 2021 ; Shen et al, 2021 ). However, the causal relationship between the degeneration of peripheral auditory system, such as inner ear structure, and the declined function of central auditory system and cognitive function in patients has not been clear (Rutherford et al, 2018 ; Bowl and Dawson, 2019 ; Ralli et al, 2019 ).…”