Brain Structural and Functional Reorganization in Tinnitus Patients Without Hearing Loss After Sound Therapy: A Preliminary Longitudinal Study

Abstract

Sound therapy is one of the most common first-line treatments for idiopathic tinnitus. We aimed to investigate the brain structural and functional alterations between patients with idiopathic tinnitus without hearing loss (HL) and healthy controls (HCs) and between patients before and after sound therapy (narrow band noise). Structural and resting-state functional images were acquired from 13 tinnitus patients without HL and 18 HCs before and after 6 months of narrow band sound therapy (only patients received the treatment). Voxel-based morphometry (VBM) and independent component analysis (ICA) were conducted to separately investigate the brain structural and functional changes. Associations between brain changes and clinical variables were also performed. After the treatment, the % improvement of THI score was −1.30% (± 63.40%). Compared with HCs, tinnitus patients showed gray matter and white matter atrophy in the left middle temporal gyrus at baseline, and the gray matter volume was further reduced after the treatment. The patients also showed increased white matter volume in the cingulum (cingulate), right calcarine, left rolandic operculum, and left parietal and frontal lobes. Additionally, compared with HCs, tinnitus patients exhibited positive [medial visual network (mVN) and sensorimotor network (SMN), mVN and auditory network (AN)] and negative [mVN and lateral visual network (lVN)] internetwork functional connectivity (FC) at baseline and negative [left frontoparietal network (LFPN) and dorsal attention network (DAN), AN and posterior default mode network (pDMN)] internetwork FC after the narrow band sound therapy. The patients also showed negative [LFPN and right frontoparietal network (RFPN), LFPN and RFPN, anterior default mode network (aDMN) and AN, aDMN and DAN] internetwork FC after the treatment when compared with baseline. Our findings suggest that although the outcomes of idiopathic tinnitus patients without HL were not very good when the improvement of THI scores was used as an evaluation indicator, the patients experienced significant differences in auditory-related and non-auditory-related brain reorganization before and after the narrow band sound therapy, that is, sound therapy may have a significant effect on brain reorganization in patients with idiopathic tinnitus. This study may provide some new useful information for the understanding of mechanisms underlying idiopathic tinnitus.

Pretreatment intranetwork connectivity can predict the outcomes in idiopathic tinnitus patients treated with sound therapy

“…Regarding the FC changes in the lVN (nonprimary regions of the visual cortex), consistent with one of our prior studies (Chen et al, 2021b), we speculated that because of the increased compensatory stimulation between the auditory and visual networks caused by tinnitus through the thalamus, the relay station (Chen et al, 2019), the increased intranetwork FC in the MOG may reflect an abnormal overactive state of the visual network in tinnitus patients. Meanwhile, we also observed decreased intranetwork FC in the DAN.…”

“…The DAN is involved in visual attention (Gitelman, 2003). Previous studies have shown increased FC between the DAN and other RSNs (such as the DMN; Chen et al, 2021b; Schmidt et al, 2013), and the authors suggested that this change could be a compensatory attempt to transfer the phantom stimulus to the limbic system (Golm, Schmidt‐Samoa, Dechent, & Kröner‐Herwig, 2013; Ooms et al, 2013). Thus, increased FC in the DAN of IG patients may represent abnormal compensation caused by the enhanced connectivity between the DAN and other RSNs, although the exact mechanism is still not clear.…”

“…As a lateralized and independent network (Smith et al, 2009), the frontoparietal network (FPN) supports decision‐making and cognitive control functions (Vincent, Kahn, Snyder, Raichle, & Buckner, 2008). Studies have reported tinnitus‐related changes in the LFPN or RFPN (Chen et al, 2021b; Lanting et al, 2016). In line with these studies, we considered that the intranetwork FC changes in the FPN in our study may indicate that the brain regions related to executive control, advanced cognition, and language are in an abnormal or dysfunctional state in tinnitus patients.…”

“…In addition to the distinct intranetwork connectivity changes between the EG and the IG observed in this study, we also found that the EG, compared with the IG, showed increased internetwork FC between the SN and ECN and the pDMN and DAN. There is evidence in patients with idiopathic tinnitus that FC between RSNs (auditory or nonauditory‐related networks) undergoes significant changes (Chen et al, 2021b; Husain & Schmidt, 2014; Schmidt et al, 2013). For example, in the study by Schmidt et al (2013), they found that connectivity increased among the DMN, DAN, and AUN, and therapies that mitigated the increased connectivity among them and the decreased coherence of the DMN could be effective in reducing tinnitus‐related distress.…”

“…For example, in the study by Schmidt et al (2013), they found that connectivity increased among the DMN, DAN, and AUN, and therapies that mitigated the increased connectivity among them and the decreased coherence of the DMN could be effective in reducing tinnitus‐related distress. Moreover, one recent study reported that the changed internetwork FC between RSNs may reflect abnormal large‐scale functional interactions among the functional networks (Chen et al, 2021b). Therefore, we speculated that, in line with these studies, the increase in FC between these networks may be the result of abnormal brain network interactions after tinnitus or a reflection of the abnormal state caused by tinnitus (Chen et al, 2021b), while the exact mechanisms are still not very clear.…”