Neuroanatomical changes due to hearing loss and chronic tinnitus: A combined VBM and DTI study

Abstract

Subjective tinnitus is the perception of sound in the absence of an external source. Tinnitus is often accompanied by hearing loss but not everyone with hearing loss experiences tinnitus. We examined neuroanatomical alterations associated with hearing loss and tinnitus in three groups of subjects: those with hearing loss with tinnitus, those with hearing loss without tinnitus and normal hearing controls without tinnitus. To examine changes in gray matter we used structural MRI scans and voxel-based morphometry (VBM) and to identify changes in white matter tract orientation we used diffusion tensor imaging (DTI). A major finding of our study was that there were both gray and white matter changes in the vicinity of the auditory cortex for subjects with hearing loss alone relative to those with tinnitus and those with normal hearing. We did not find significant changes in gray or white matter in subjects with tinnitus and hearing loss compared to normal hearing controls. VBM analysis revealed that individuals with hearing loss without tinnitus had gray matter decreases in anterior cingulate and superior and medial frontal gyri relative to those with hearing loss and tinnitus. Region-of-interest analysis revealed additional decreases in superior temporal gyrus for the hearing loss group compared to the tinnitus group. Investigating effects of hearing loss alone, we found gray matter decreases in superior and medial frontal gyri in participants with hearing loss compared to normal hearing controls. DTI analysis showed decreases in fractional anisotropy values in the right superior and inferior longitudinal fasciculi, corticospnial tract, inferior fronto-occipital tract, superior occipital fasciculus, and anterior thalamic radiation for the hearing loss group relative to normal hearing controls. In attempting to dissociate the effect of tinnitus from hearing loss, we observed that hearing loss rather than tinnitus had the greatest influence on gray and white matter alterations.

Differential tinnitus-related neuroplastic alterations of cortical thickness and surface area

“…Naturally, a neuroanatomical examination that considers only gray matter traits is not complete. We agree that changes in white matter architecture can also be conceived as neuroplastic biomarkers of the tinnitus network [26,83,28]. As outlined by Adjamian and co-authors [33] these studies report both local increases and decreases of white matter fiber tracts in TI.…”

“…Accordingly, [66, p. 1141] concluded that "GM volume, which is a composite of 2 other traits (surface area and thickness), might not be the best choice". Even though recent clinical studies [27,28,31,13,35] continue to use VBM to identify apparent tinnitus-related group differences, we suggest that surface-based morphometry should be used in complement with VBM because it allows for the computation of three distinct parameters, namely CV, CSA, and CT. Thus, SBM minimizes the risk of underestimating or ignoring existing relationships between CT or CSA and behavior.…”

“…The number of studies that scrutinized the neuroanatomical changes in the brain structure of TI is smaller, but for the time being, the results are notably inconsistent and 50 heterogeneous [26,27,28,29,30,31,32] (for a review, see [33]). The range of brain regions that appear to undergo structural changes either as a function or as a catalyst of chronic noise perception includes the supratemporal, the lateral (pre-)frontal cortex, medial frontal, cingulate, temporal, subcallosal and parietal cortex as well as a number of subcortical nuclei.…”

“…In particular, bilateral 55 peri-auditory regions in the superior temporal lobe [26,27,28] and subcortical areas that are considered as part of the (anatomically ill-defined) limbic system [29,34] often show anatomical changes. However, to date, neither the direction of tinnitus-related changes (increase or decrease of neuroanatomical gray matter (GM)) is clear, nor is it clarified whether the changes in the neural architecture 60 of distinct regions occur independently or are related.…”

“…Furthermore, evidence for confined "structural abnormalities specifically related to tinnitus is sparse" [33, p. 119], and this fact makes it difficult to test specific anatomical hypotheses. The results obtained from studies that used the standard VBM approach [27,28,29,30,32,1,35] 70 are difficult to reconcile due to their heterogeneity. Thus the question arises whether the inconsistency of available results may be related to methodological limitations of VBM measurements [33].…”