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Functional connectivity analysis of fMRI data collected from human subjects with chronic tinnitus and varying levels of tinnitus-related distress.

ABSTRACT: The data presented here are functional connectivity analyses based on fMRI scans from a clinical sample of the chronic tinnitus population (n = 75). All data were obtained during an experiment in which subjects listened to auditory stimuli via headphones while undergoing fMRI scanning. The stimuli consisted of tones and bandpass noise presented at different frequencies. Stimulus frequency was the experimental factor, which was set (1) at each subject's tinnitus percept frequency (TF) and (2) at an unrelated control frequency (CF) at least one octave away from the TF stimuli. All subjects were presented with stimuli at these two frequencies. We refer the reader to our original research article "Functional brain changes in auditory phantom perception evoked by different stimulus frequencies" (Hullfish et al., 2018) for further discussion. Here, we present data specifically from group-level analyses where the subjects were divided according to their level of tinnitus-related distress. The high-distress (HD) group comprised 43 subjects with Tinnitus Questionnaire (TQ) scores greater than or equal to 47, out of a possible 82 points. The low-distress (LD) group comprised the remaining 32 subjects with TQ score less than 47. The data presented include contrasts of functional connectivity elicited by TF and CF stimuli in each group as well as contrasts between the two groups.

SUBMITTER: Hullfish J

PROVIDER: S-EPMC6216076 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Functional connectivity analysis of fMRI data collected from human subjects with chronic tinnitus and varying levels of tinnitus-related distress.

Hullfish Jeffrey J Abenes Ian I Kovacs Silvia S Sunaert Stefan S De Ridder Dirk D Vanneste Sven S

Data in brief 20181019

The data presented here are functional connectivity analyses based on fMRI scans from a clinical sample of the chronic tinnitus population (<i>n</i> = 75). All data were obtained during an experiment in which subjects listened to auditory stimuli via headphones while undergoing fMRI scanning. The stimuli consisted of tones and bandpass noise presented at different frequencies. Stimulus frequency was the experimental factor, which was set (1) at each subject's tinnitus percept frequency (TF) and ...[more]

PMID: 30417040

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Project description:The exact neurophysiological basis of chronic tinnitus, which affects 10-15% of the population, remains unknown and is controversial at many levels. It is an open question whether phantom sound perception results from increased central neural gain or not, a crucial question for any future therapeutic intervention strategies for tinnitus. We performed a comprehensive study of mild hearing-impaired participants with and without tinnitus, excluding participants with co-occurrences of hyperacusis. A right-hemisphere correlation between tinnitus loudness and auditory perceptual difficulty was observed in the tinnitus group, independent of differences in hearing thresholds. This correlation was linked to reduced and delayed sound-induced suprathreshold auditory brain responses (ABR wave V) in the tinnitus group, suggesting subsided rather than exaggerated central neural responsiveness. When anatomically predefined auditory regions of interest were analysed for altered sound-evoked BOLD fMRI activity, it became evident that subcortical and cortical auditory regions and regions involved in sound detection (posterior insula, hippocampus), responded with reduced BOLD activity in the tinnitus group, emphasizing reduced, rather than increased, central neural gain. Regarding previous findings of evoked BOLD activity being linked to positive connectivities at rest, we additionally analysed r-fcMRI responses in anatomically predefined auditory regions and regions associated with sound detection. A profound reduction in positive interhemispheric connections of homologous auditory brain regions and a decline in the positive connectivities between lower auditory brainstem regions and regions involved in sound detection (hippocampus, posterior insula) were observed in the tinnitus group. The finding went hand-in-hand with the emotional (amygdala, anterior insula) and temporofrontal/stress-regulating regions (prefrontal cortex, inferior frontal gyrus) that were no longer positively connected with auditory cortex regions in the tinnitus group but were instead positively connected to lower-level auditory brainstem regions. Delayed sound processing, reduced sound-evoked BOLD fMRI activity and altered r-fcMRI in the auditory midbrain correlated in the tinnitus group and showed right hemisphere dominance as did tinnitus loudness and perceptual difficulty. The findings suggest that reduced central neural gain in the auditory stream may lead to phantom perception through a failure to energize attentional/stress-regulating networks for contextualization of auditory-specific information. Reduced auditory-specific information flow in tinnitus has until now escaped detection in humans, as low-level auditory brain regions were previously omitted from neuroimaging studies.Trial registrationGerman Clinical Trials Register DRKS0006332.

Project description:The phantom sound of tinnitus is believed to be triggered by aberrant neural activity in the central auditory pathway, but since this debilitating condition is often associated with emotional distress and anxiety, these comorbidities likely arise from maladaptive functional connections to limbic structures such as the amygdala and hippocampus. To test this hypothesis, resting-state functional magnetic resonance imaging (fMRI) was used to identify aberrant effective connectivity of the amygdala and hippocampus in tinnitus patients and to determine the relationship with tinnitus characteristics. Chronic tinnitus patients (n = 26) and age-, sex-, and education-matched healthy controls (n = 23) were included. Both groups were comparable for hearing level. Granger causality analysis utilizing the amygdala and hippocampus as seed regions were used to investigate the directional connectivity and the relationship with tinnitus duration or distress. Relative to healthy controls, tinnitus patients demonstrated abnormal directional connectivity of the amygdala and hippocampus, including primary and association auditory cortex, and other non-auditory areas. Importantly, scores on the Tinnitus Handicap Questionnaires were positively correlated with increased connectivity from the left amygdala to left superior temporal gyrus (r = 0.570, P = 0.005), and from the right amygdala to right superior temporal gyrus (r = 0.487, P = 0.018). Moreover, enhanced effective connectivity from the right hippocampus to left transverse temporal gyrus was correlated with tinnitus duration (r = 0.452, P = 0.030). The results showed that tinnitus distress strongly correlates with enhanced effective connectivity that is directed from the amygdala to the auditory cortex. The longer the phantom sensation, the more likely acute tinnitus becomes permanently encoded by memory traces in the hippocampus. Hum Brain Mapp 38:2384-2397, 2017. © 2017 Wiley Periodicals, Inc.

Dataset Information

Functional connectivity analysis of fMRI data collected from human subjects with chronic tinnitus and varying levels of tinnitus-related distress.

Publications

Functional connectivity analysis of fMRI data collected from human subjects with chronic tinnitus and varying levels of tinnitus-related distress.

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