Altered regional and circuit resting-state activity associated with unilateral hearing loss

Abstract

The deprivation of sensory input after hearing damage results in functional reorganization of the brain including cross-modal plasticity in the sensory cortex and changes in cognitive processing. However, it remains unclear whether partial deprivation from unilateral auditory loss (UHL) would similarly affect the neural circuitry of cognitive processes in addition to the functional organization of sensory cortex. Here, we used resting-state functional magnetic resonance imaging to investigate intrinsic activity in 34 participants with UHL from acoustic neuroma in comparison with 22 matched normal controls. In sensory regions, we found decreased regional homogeneity (ReHo) in the bilateral calcarine cortices in UHL. However, there was an increase of ReHo in the right anterior insular cortex (rAI), the key node of cognitive control network (CCN) and multimodal sensory integration, as well as in the left parahippocampal cortex (lPHC), a key node in the default mode network (DMN). Moreover, seed-based resting-state functional connectivity analysis showed an enhanced relationship between rAI and several key regions of the DMN. Meanwhile, lPHC showed more negative relationship with components in the CCN and greater positive relationship in the DMN. Such reorganizations of functional connectivity within the DMN and between the DMN and CCN were confirmed by a graph theory analysis. These results suggest that unilateral sensory input damage not only alters the activity of the sensory areas but also reshapes the regional and circuit functional organization of the cognitive control network.

Figure 1. Group difference in ReHo revealed by ANCOVA.

Significant differences, location and ReHo values of each group in right anterior insular cortex (rAI) (A), left parahippocampal cortex (lPHC) (B), left calcarine cortex (C) and right calcarine cortex (D). The bar and error bar represent the mean value and SD, respectively, of the ReHo values in the region. * p<0.05, corrected. UHL, unilateral hearing loss, NC, normal controls.

Figure 2. Group difference in resting state functional connectivity with rAI (the seed region) revealed by ANCOVA.

The significant differences were shown in right medial prefrontal cortex (rMPFC) (A), right postcentral gyrus (rPCG) (B) and pregenual anterior cingulate cortex (pACC) (C). The bar and error bar represent the mean value and SD, respectively, of the functional connectivity values in the region. * p<0.05, corrected.

Figure 3. Group difference in resting state functional connectivity with lPHC (seed region) revealed by ANCOVA.

The significant differences are shown in (A) right insula, (B) supplementary motor area (SMA), (C) right angular gyrus (rAG), (D) left cuneus and (E) right precuneus. The bar and error bar represent the mean value and SD, respectively, of the functional connectivity values in the region. * p<0.05, corrected.