Abstract
PurposeThe phantom sound of tinnitus is considered to be associated with abnormal functional coupling between the nucleus accumbens (NAc) and the prefrontal cortex, which may form a frontostriatal top-down gating system to evaluate and modulate sensory signals. Resting-state functional magnetic resonance imaging (fMRI) was used to recognize the aberrant directional connectivity of the NAc in chronic tinnitus and to ascertain the relationship between this connectivity and tinnitus characteristics.MethodsParticipants included chronic tinnitus patients (n = 50) and healthy controls (n = 55), matched for age, sex, education, and hearing thresholds. The hearing status of both groups was comparable. On the basis of the NAc as a seed region, a Granger causality analysis (GCA) study was conducted to investigate the directional connectivity and the relationship with tinnitus duration or distress.ResultsCompared with healthy controls, tinnitus patients exhibited abnormal directional connectivity between the NAc and the prefrontal cortex, principally the middle frontal gyrus (MFG), orbitofrontal cortex (OFC), and inferior frontal gyrus (IFG). Additionally, positive correlations between tinnitus handicap questionnaire (THQ) scores and increased directional connectivity from the right NAc to the left MFG (r = 0.357, p = 0.015) and from the right MFG to the left NAc (r = 0.626, p < 0.001) were observed. Furthermore, the enhanced directional connectivity from the right NAc to the right OFC was positively associated with the duration of tinnitus (r = 0.599, p < 0.001).ConclusionIn concurrence with expectations, tinnitus distress was correlated with enhanced directional connectivity between the NAc and the prefrontal cortex. The current study not only helps illuminate the neural basis of the frontostriatal gating control of tinnitus sensation but also contributes to deciphering the neuropathological features of tinnitus.
Highlights
Tinnitus is defined as a phantom auditory perception that may bother many patients to the extent that it changes their lives (Baguley et al, 2013; Bauer, 2018)
After VBM analysis, there were no significant differences in the comparisons of the whole-brain volumes (GM volume, white matter (WM) volume, and brain parenchyma volume) between chronic tinnitus patients and healthy controls (p > 0.05)
In this study, resting-state functional magnetic resonance imaging (fMRI) combined with Granger causality analysis (GCA) was used to investigate the directional connectivity between the nucleus accumbens (NAc) and all brain regions in chronic tinnitus patients compared with healthy controls
Summary
Tinnitus is defined as a phantom auditory perception that may bother many patients to the extent that it changes their lives (Baguley et al, 2013; Bauer, 2018). A series of anomalies in the auditory center were observed in tinnitus cases in prior research studies (Leaver et al, 2011, 2016a; Kim et al, 2012; Song et al, 2012, 2015; Vanneste and De Ridder, 2012; Adjamian et al, 2014; Husain and Schmidt, 2014; Chen et al, 2015, 2016; Hinkley et al, 2015; Gunbey et al, 2017; Schmidt et al, 2017; Hullfish et al, 2019), simultaneously covering synaptic remodeling (Eggermont and Roberts, 2004), neuronal spontaneous hyperactivity or hypoactivity (Chen et al, 2014), increased neuronal synchronicity (Eggermont, 2007; Langers et al, 2012), and changes in tonotopic representation of sound (Langers et al, 2012). Many studies have investigated this area over the years, the neuropathological mechanism underlying tinnitus generation remains an enigma
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