Neuroanatomical Alterations in Tinnitus Assessed with Magnetic Resonance Imaging

Abstract

Previous studies of anatomical changes associated with tinnitus have provided inconsistent results, with some showing significant cortical and subcortical changes, while others have found effects due to hearing loss, but not tinnitus. In this study, we examined changes in brain anatomy associated with tinnitus using anatomical scans from 128 participants with tinnitus and hearing loss, tinnitus with clinically normal hearing, and non-tinnitus controls with clinically normal hearing. The groups were matched for hearing loss, age and gender. We employed voxel- and surface-based morphometry (SBM) to investigate gray and white matter volume and thickness within regions-of-interest (ROI) that were based on the results of previous studies. The largest overall effects were found for age, gender, and hearing loss. With regard to tinnitus, analysis of ROI revealed numerous small increases and decreases in gray matter and thickness between tinnitus and non-tinnitus controls, in both cortical and subcortical structures. For whole brain analysis, the main tinnitus-related significant clusters were found outside sensory auditory structures. These include a decrease in cortical thickness for the tinnitus group compared to controls in the left superior frontal gyrus (SFG), and a decrease in cortical volume with hearing loss in left Heschl's gyrus (HG). For masked analysis, we found a decrease in gray matter volume in the right Heschle's gyrus for the tinnitus group compared to the controls. We found no changes in the subcallosal region as reported in some previous studies. Overall, while some of the morphological differences observed in this study are similar to previously published findings, others are entirely different or even contradict previous results. We highlight other discrepancies among previous results and the increasing need for a more precise subtyping of the condition.

Keywords: auditory cortex; brain anatomy; surface-based morphometry; tinnitus; voxel-based morphometry.

Figure 1

The audiograms for each comparison group for the tinnitus participants (blue) and the controls (red) in (A) all subjects, (B) severe tinnitus and matched controls and (C) tinnitus with no hearing loss and matched controls.

Figure 2

The Rauschecker model brain regions [nucleus accumbens (NAc) and ventromedial prefrontal cortex (vmPFC)] that have been defined as a mask for further analysis.

Figure 3

The Mulhau masks that have previously shown anatomical changes relating to tinnitus.

Figure 4

The age of each subject plotted against their hearing threshold.

Figure 5

The areas showing that as age increases there is a significant increase in gray matter volume at the cerebrospinal fluid (CSF) boundaries for the regression group of all subjects using age as the regressor of interest.

Figure 6

Clusters showing a significant effect (p < 0.05 family wise error (FWE)-corrected) of tinnitus in the superior frontal gyrus (SFG; A) and of tinnitus severity in the pre-cuneus (B,C) in the whole-brain surface-based morphometry (SBM) analysis. Blue areas correspond to a negative effect (decrease in thickness for the tinnitus group vs. the control group and decrease in area and volume for increasing tinnitus severity).

Figure 7

Significant voxels (circled) found in the medial geniculate nucleus (MGN) for a reduction in white matter for tinnitus participants compared to controls for (A) regression group 1, all subjects and (B) regression group 2, severe tinnitus matched to controls.

Figure 8

Clusters showing a significant effect (p < 0.05 FWE-corrected) of tinnitus in left AC (A) right superior temporal sulcus (STS; B) right Heschl’s gyrus (HG) (C,D) and of tinnitus severity in right middle temporal gyrus (MTG) and PFC (E,F) in the masked SBM analysis. The yellow outlines depict the masks used to restrict the vertexwise analysis (auditory cortex, AC for A,B HG for C,D default mode network (DMN) for E; PFC for F). Blue areas correspond to a negative effect (decrease in thickness or volume for the tinnitus group vs. the control group) and the red areas to a positive effect (increasing thickness for increasing tinnitus severity).

Figure 9

Cluster showing a significant effect (p < 0.05 FWE-corrected) of tinnitus in left AC in the masked SBM analysis for the severe tinnitus grouping. The yellow outlines depict the AC masks used to restrict the vertexwise analysis. The blue area corresponds to a negative effect (decrease in thickness for the severe tinnitus group vs. matched controls).

Figure 10

Clusters showing a significant effect (p < 0.05 FWE-corrected) of tinnitus severity in right superior parietal gyrus (A) and right posterior cingulate cortex (B) in the whole-brain SBM analyses. Blue areas correspond to a negative effect (decrease in cortical area with increasing tinnitus severity).

Figure 11

Clusters showing a significant effect (p < 0.05 FWE-corrected) of tinnitus in left AC (A) and right rostromedial frontal cortex (B) of tinnitus severity in left HG (C,D) and left MTG (E) in the masked SBM analyses. The yellow outlines depict the masks used to restrict the vertexwise analysis (AC for A,C,D; PFC for B; DMN for E). Blue areas correspond to a negative effect (decrease in thickness for the normal-hearing tinnitus group vs. matched controls in (A,B) decrease in area and volume with increasing tinnitus severity in (C,D) and the red areas to a positive effect (increasing thickness for increasing tinnitus severity in (E).