Tinnitus-related dissociation between cortical and subcortical neural activity in humans with mild to moderate sensorineural hearing loss

Abstract

Tinnitus is a phantom sound percept that is strongly associated with peripheral hearing loss. However, only a fraction of hearing-impaired subjects develops tinnitus. This may be based on differences in the function of the brain between those subjects that develop tinnitus and those that do not. In this study, cortical and sub-cortical sound-evoked brain responses in 34 hearing-impaired chronic tinnitus patients and 19 hearing level-matched controls were studied using 3-T functional magnetic resonance imaging (fMRI). Auditory stimuli were presented to either the left or the right ear at levels of 30-90 dB SPL. We extracted neural activation as a function of sound intensity in eight auditory regions (left and right auditory cortices, medial geniculate bodies, inferior colliculi and cochlear nuclei), the cerebellum and a cinguloparietal task-positive region. The activation correlated positively with the stimulus intensity, and negatively with the hearing threshold. We found no differences between both groups in terms of the magnitude and lateralization of the sound-evoked responses, except for the left medial geniculate body and right cochlear nucleus where activation levels were elevated in the tinnitus subjects. We observed significantly reduced functional connectivity between the inferior colliculi and the auditory cortices in tinnitus patients compared to controls. Our results indicate a failure of thalamic gating in the development of tinnitus.

Impairments of thalamic resting-state functional connectivity in patients with chronic tinnitus

“…Our results are consistent with recent auditory stimulusbased fMRI findings in which reduced functional connectivity was observed between the thalamus (MGB) and the cortex of tinnitus patients [14,15]. Our findings may be considered in the context of model of Rauschecker et al in which the projections of the nucleus accumbens feed back to the thalamic reticular nucleus, which in turn selectively inhibits sections of the thalamus and auditory cortex corresponding to the tinnitus pitch.…”

“…The thalamus, which regulates the flow of sensory information to and from the auditory cortex, is thought to play an important role in the perception of tinnitus [9,14]. Consistent with this view, we observed that the thalamus showed decreased functional connectivity with the primary and associative auditory cortex, specifically the STG (Brodmann's area 42) and MTG (Brodmann's area 21).…”

“…Tinnitus was associated with decreased ALFF activity bilaterally in the thalamus function [4]. Other sound-evoked fMRI showed that tinnitus was associated with reduced functional connectivity between thalamus and cortex [13][14][15].…”

Evidence for differential modulation of primary and nonprimary auditory cortex by forward masking in tinnitus

“…One widely cited neural synchrony model of tinnitus has attributed oscillatory activity in the TFR to hyperpolarization of thalamic nuclei consequent on deafferentation of auditory pathways (Llin as et al, 2005;Kalappa et al, 2014). Hyperpolarization could explain reduced sound-evoked functional connectivity between auditory cortical and subcortical structures which has been reported in tinnitus sufferers compared to controls (Boyen et al, 2014;Lanting et al, 2014).…”

Pump Up the Volume: Could Excessive Neural Gain Explain Tinnitus and Hyperacusis?

“…This suggests that some pathologies are more likely to be associated with tinnitus than others; for example, 74-91% of otosclerosis patients report tinnitus [Ayache et al, 2003;Sobrinho et al, 2004]. Alternatively, perception of tinnitus has been hypothesized to be due to a failure of the 'thalamic gate' [Boyen et al, 2014;Rauschecker et al, 2010].…”