Alterations of structural and functional connectivity in profound sensorineural hearing loss infants within an early sensitive period: A combined DTI and fMRI study

Abstract

Due to heightened level of neuroplasticity, there is a sensitive period (2-4 years after birth) that exists for optimal central auditory development. Using diffusion tensor imaging combined with resting-state functional connectivity (rsFC) analysis, this study directly investigates the structural connectivity alterations of the whole brain white matter (WM) and the functional reorganization of the auditory network in infants with sensorineural hearing loss (SNHL) during the early sensitive period. 46 bilateral profound SNHL infants prior to cochlear implantation (mean age, 17.59 months) and 33 healthy controls (mean age, 18.55 months) were included in the analysis. Compared with controls, SNHL infants showed widespread WM alterations, including bilateral superior longitudinal fasciculus, inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, right corticospinal tract, posterior thalamic radiation and left uncinate fasciculus. Moreover, SNHL infants demonstrated increased rsFC between left/right primary auditory cortex seeds and right insula and superior temporal gyrus. In conclusion, this study suggests that SNHL in the early sensitive period is associated with diffuse WM alterations that mainly affect the auditory and language pathways. Furthermore, increased rsFC in areas mainly associated with auditory and language networks may potentially reflect reorganization and compensatory activation in response to auditory deprivation during the early sensitive period.

Keywords: Diffusion tensor imaging; Functional connectivity; Resting-state functional magnetic resonance imaging; Sensitive period; Sensorineural hearing loss.

Fig. 1

Whole-brain group-comparison results for FA values obtained by TBSS analysis (p < 0.05, FWE corrected). The background image is the mean FA and the FA skeleton (green). Blue voxels represent regions in which FA was significantly decreased in the SNHL group relative to the HC group. FA = fractional anisotropy, TBSS = tract–based spatial statistics, FWE = Family Wise Error, SNHL = sensorineural hearing loss, HC = healthy control (All images are in radiologic orientation).

Fig. 2

Intra-group functional connectivity maps in the SNHL group and HC group. A: Axial visualization, B: Surface visualization. In both groups, the left/right A1 showed similar positive functional connectivity to brain regions (color coded) of bilateral superior temporal gyrus, middle temporal gyrus, insula, inferior frontal gyrus, angular, inferior parietal lobule and Rolandic operculum, most of which are considered to be part of the auditory network, salience network and default mode network. All images were shown with FDR correction of p < 0.05. The colored bar indicates the corresponding t values. SNHL = sensorineural hearing loss, HC = healthy control, A1 = primary auditory cortex, FDR = false discovery rate. (All images are in radiologic orientation)

Fig. 3

Inter-group functional connectivity analyses results. A: Axial visualization; B: Surface visualization. Compared with HC group, SNHL group showed significant increased functional connectivity in the right insula and STG when the left A1 was used as the seed region. In addition, increased functional connectivity was found in the right insula and STG when the right A1 was used as the seed region. No region of decreased functional connectivity was found in SNHL group compared with HC group. All images were shown with FDR correction of p < 0.05. The colored bar indicates the corresponding t values. SNHL = sensorineural hearing loss, HC = healthy control, A1 = primary auditory cortex, STG = superior temporal gyrus, FDR = false discovery rate. (All images are in radiologic orientation).