Frequency-specific alternations in the amplitude of low-frequency fluctuations in chronic tinnitus.

Jian Wang,Yu-Chen Chen,Gao-Jun Teng,Jian Zhang,Wenqing Xia,Zhenyu Xiong,Vijaya P. K. Muthaiah,Bin Luo,Richard Salvi

doi:10.3389/fncir.2015.00067

Abstract

Tinnitus, a phantom ringing, buzzing, or hissing sensation with potentially debilitating consequences, is thought to arise from aberrant spontaneous neural activity at one or more sites within the central nervous system; however, the location and specific features of these oscillations are poorly understood with respect to specific tinnitus features. Recent resting-state functional magnetic resonance imaging (fMRI) studies suggest that aberrant fluctuations in spontaneous low-frequency oscillations (LFO) of the blood oxygen level-dependent (BOLD) signal may be an important factor in chronic tinnitus; however, the role that frequency-specific components of LFO play in subjective tinnitus remains unclear. A total of 39 chronic tinnitus patients and 41 well-matched healthy controls participated in the resting-state fMRI scans. The LFO amplitudes were investigated using the amplitude of low-frequency fluctuation (ALFF) and fractional ALFF (fALFF) in two different frequency bands (slow-4: 0.027–0.073 Hz and slow-5: 0.01–0.027 Hz). We observed significant differences between tinnitus patients and normal controls in ALFF/fALFF in the two bands (slow-4 and slow-5) in several brain regions including the superior frontal gyrus (SFG), inferior frontal gyrus, middle temporal gyrus, angular gyrus, supramarginal gyrus, and middle occipital gyrus. Across the entire subject pool, significant differences in ALFF/fALFF between the two bands were found in the midbrain, basal ganglia, hippocampus and cerebellum (Slow 4 > Slow 5), and in the middle frontal gyrus, supramarginal gyrus, posterior cingulate cortex, and precuneus (Slow 5 > Slow 4). We also observed significant interaction between frequency bands and patient groups in the orbitofrontal gyrus. Furthermore, tinnitus distress was positively correlated with the magnitude of ALFF in right SFG and the magnitude of fALFF slow-4 band in left SFG, whereas tinnitus duration was positively correlated with the magnitude of ALFF in right SFG and the magnitude of fALFF slow-5 band in left SFG. Resting-state fMRI provides an unbiased method for identifying aberrant spontaneous LFO occurring throughout the central nervous system. Chronic tinnitus patients have widespread abnormalities in ALFF and fALFF slow-4 and slow-5 band which are correlated with tinnitus distress and duration. These results provide new insights on the neuropathophysiology of chronic tinnitus; therapies capable of reversing these aberrant patterns may reduce tinnitus distress.

Highlights

Chronic subjective tinnitus is a common hearing disorder often described as a buzzing, sizzling or ringing sensation that occurs in the absence of an objective sound
The results showed that there were no significant changes in gray matter (GM) and white matter (WM) volumes between the two groups (p > 0.05)
Brain regions showing a significantly larger amplitude of low-frequency fluctuation (ALFF) in tinnitus patients compared to healthy controls (TIN > HC, red colors) were seen in right superior frontal gyrus (SFG), right middle temporal gyrus (MTG), right angular gyrus (AG), and left inferior frontal gyrus (IFG)

Summary

INTRODUCTION

Chronic subjective tinnitus is a common hearing disorder often described as a buzzing, sizzling or ringing sensation that occurs in the absence of an objective sound. Abnormal resting-state functional networks have been found in tinnitus, such as the auditory network (Burton et al, 2012; Kim et al, 2012; Maudoux et al, 2012a; Schmidt et al, 2013), default mode network (DMN; Schmidt et al, 2013; Chen et al, 2015a,b), dorsal attention network (DAN; Burton et al, 2012; Schmidt et al, 2013), ventral attention network (VAN; Burton et al, 2012) These findings are based on investigations of LFO from the perspective of temporal synchrony or interregional cooperation, but fail to consider the amplitude of alternations in local or regional neuronal activity. We hypothesized that (1) aberrant LFO amplitudes in tinnitus may depend on the specific frequency bands, especially the slow-4 and slow-5 bands that were mainly associated with neuronal oscillations, and that (2) these frequency specific abnormalities would be correlated with unique tinnitus characteristics such as tinnitus duration or distress

MATERIALS AND METHODS

RESULTS

Correlation Analysis Results

CONCLUSION