Intrinsic brain activity reorganization contributes to long-term compensation of higher-order hearing abilities in single-sided deafness

Abstract

Single-sided deafness (SSD) is an extreme case of partial hearing deprivation and results in a significant decline in higher-order hearing abilities, including sound localization and speech-in-noise recognition. Clinical studies have reported that patients with SSD recover from these higher-order hearing abilities to some extent over time. Neuroimaging studies have observed extensive brain functional plasticity in patients with SSD. However, studies investigating the role of plasticity in functional compensation, particularly those investigating the relationship between intrinsic brain activity alterations and higher-order hearing abilities, are still limited. In this study, we used resting-state functional MRI to investigate intrinsic brain activity, measured by the amplitude of low-frequency fluctuation (ALFF), in 19 patients with left SSD, 17 patients with right SSD, and 21 normal hearing controls (NHs). All patients with SSD had durations of deafness longer than 2 years. Decreased ALFF values in the bilateral precuneus (PCUN), lingual gyrus, and left middle frontal gyrus were observed in patients with SSD compared with the values of NHs. Longer durations of deafness were correlated with better hearing abilities, as well as higher ALFF values in the left inferior parietal lobule, the angular gyrus, the middle occipital gyrus, the bilateral PCUN, and the posterior cingulate gyrus. Moreover, we observed a generally consistent trend of correlation between ALFF values and higher-order hearing abilities in specific brain areas in patients with SSD. That is, better abilities were correlated with lower ALFF values in the frontal regions and higher ALFF values in the PCUN and surrounding parietal-occipital areas. Furthermore, mediation analysis revealed that the ALFF values in the PCUN were a significant mediator of the relationship between the duration of deafness and higher-order hearing abilities. Our study reveals significant plasticity of intrinsic brain activity in patients with SSD and suggests that reorganization of intrinsic brain activity may be one of the compensatory mechanisms that facilitate improvement in higher-order hearing abilities in these patients over time.