Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study

Abstract

Presbycusis (PC) is characterized by bilateral sensorineural hearing loss at high frequencies and speech-perception difficulties in noisy environments and has a strikingly detrimental impact on cognitive function. As the neural consequences of PC may involve the whole brain, we hypothesized that patients with PC would show structural alterations not only in the auditory cortex but also in the cortexes involved in cognitive function. The purpose of this study was to use surface-based morphometry (SBM) analysis to elucidate whole-brain structural differences between patients with PC and age-matched normal hearing controls. Three-dimensional T1-weighted MR images of 26 patients with mild PC and 26 age-, sex- and education-matched healthy controls (HCs) were acquired. All participants underwent a battery of neuropsychological tests. Our results revealed gray matter atrophy in several auditory cortical areas, nodes of the default mode network (DMN), including the bilateral precuneus and inferior parietal lobule, the right posterior cingulate cortex (PCC), and the right insula of patients with PC compared to that in the HCs. Our findings also revealed that hearing loss was associated with reduced gray matter volume in the right primary auditory cortex of patients with PC. Moreover, structural alterations in the nodes of the DMN were associated with cognitive impairments in PC patients. Additionally, this study provides evidence that a thicker right insula is associated with better speech perception in patients with PC. Based on these findings, we argue that the onset of PC seems to trigger its own cascade of conditions, including a need for increased cognitive resources during speech comprehension, which might lead to auditory and cognition-related cortical reorganization.

Reduced Suprathreshold Auditory Nerve Responses are Associated with Thinner Temporal Cortex and Slower Processing Speed in Presbycusis

“…Previous studies have related audiogram threshold loss with right temporal and cingulate cortex atrophy [9-12,40,41]. Here we extended these results, showing that in addition to audiogram threshold elevation, reduced suprathreshold amplitudes of auditory nerve responses are associated to a reduction of the thickness of bilateral middle and inferior temporal cortices, and right posterior cingulate cortex.…”

“…Presbycusis is also associated with executive dysfunction [8,9] and with brain atrophy in the temporal lobe [10,11]. Moreover, recent studies in presbycusis have shown cortical atrophy in regions beyond the auditory cortex, including the cingulate cortex and parietal regions [9,12].…”

Insula and Amygdala Atrophy Are Associated With Functional Impairment in Subjects With Presbycusis

“…After the whole-brain analysis, we selected regions of interest that have been consistently implicated in previous neuroimaging studies relating audition, cognition, and dementia (Li et al, 2017;Ren et al, 2018;Xu X.-M. et al, 2019). To define ROI's, we used the Desikan-Killiany atlas, a gyrus-based atlas (Desikan et al, 2006) that has been commonly employed to explore cortical morphometry (Fornito et al, 2013;Jalbrzikowski et al, 2013).…”

“…In addition to the behavioral changes that precede dementia, recent studies suggest that biomarkers of neurodegeneration such as brain atrophy in certain areas could predict cognitive decline and dementia (ten Kate et al, 2018). Likewise, subjects with presbycusis have gray matter atrophy in the temporal lobe (Lin et al, 2014), as well as in nodes of the default mode network (Ren et al, 2018), such as the insula and the cingulate cortex. In this sense, we recently found that subjects with presbycusis and cochlear dysfunction, as evidenced by the loss of otoacoustic emissions, have atrophy of the cingulate and temporal cortices, which were related to executive dysfunction and depressive symptoms (Belkhiria et al, 2019).…”

Interacting effects of frontal lobe neuroanatomy and working memory capacity to older listeners’ speech recognition in noise

“…Also cross-sectional work has shown that pure-tone hearing loss is related to neuroanatomical alterations of gray matter volume and thickness (Alfandari et al, 2018;Eckert et al, 2012;Rigters et al, 2018Rigters et al, , 2017Tuwaig et al, 2017;Rudner et al, 2019;Uchida et al, 2018;Ren et al, 2018;Armstrong et al, 2019;Neuschwander et al, 2019;Giroud et al, in prep., but see Profant et al, 2014).…”