Aberrant functional and effective connectivity of the frontostriatal network in unilateral acute tinnitus patients with hearing loss

Abstract

The present study combined resting-state functional connectivity (FC) and Granger causality analysis (GCA) to explore frontostriatal network dysfunction in unilateral acute tinnitus (AT) patients with hearing loss. Methods:The participants included 42 AT patients and 43 healthy control (HC) subjects who underwent resting-state functional magnetic resonance imaging (fMRI) scans. Based on the seed regions in the frontostriatal network, FC and GCA were conducted between the AT patients and HC subjects. Correlation analyses were used to examine correlations among altered FC values, GCA values, and clinical features in AT patients.Results: Compared with HCs, AT patients showed a general reduction in FC between the seed regions in the frontostriatal network and nonauditory areas, including the frontal cortices, midcingulate cortex (MCC), supramarginal gyrus (SMG), and postcentral gyrus (PoCG). Using the GCA algorithm, we detected abnormal effective connectivity (EC) in the inferior occipital gyrus (IOG), MCC, Cerebelum_Crus1, and PoCG. Furthermore, correlations between disrupted FC/EC and clinical characteristics, especially tinnitus distress-related characteristics, were found in AT patients. Conclusions:Our work demonstrated abnormal FC and EC between the frontostriatal network and several nonauditory regions in AT patients with hearing loss, suggesting that multiple large-scale network dysfunctions and interactions are involved in the perception of tinnitus. These findings not only enhance the current understanding of the frontostriatal network in tinnitus but also serve as a reminder of the importance of focusing on tinnitus at an early stage.

Disrupted intra- and inter-network connectivity in unilateral acute tinnitus with hearing loss

“…On the contrary, a study conducted by Davies et al (2014) has demonstrated that there are no significant differences in the auditory cortical FC between patients with chronic tinnitus and healthy people. Results of this study also found no significant FC changes in auditory regions, which is consistent with our previous reports (Zhou et al, 2019(Zhou et al, , 2021. It was speculated that the inconsistent results obtained may be caused by several reasons: (1) All patients with tinnitus in this study are in the acute stage, so it may be a short time that there are no neuroplastic changes occurred in auditory regions; (2) tinnitus heterogeneity, such as the laterality, hearing level, and severity of tinnitus; and (3) different neuroimaging methods employed.…”

“…Each participant in the HC group was confirmed to have a normal hearing level (hearing thresholds ≤ 20 dB at any tested frequency). In addition, exclusion criteria for this study, which were described in our previously published studies ( Zhou et al, 2019 , 2021 ), included the following: (a) ear diseases that impacted hearing condition (i.e., pulsatile tinnitus, hyperacusis, or Meniere’s disease); (b) a history of severe alcoholism, smoking, and head injury; (c) neurological or psychiatric illness such as stroke, Alzheimer’s disease, Parkinson’s disease, epilepsy, or major depression; (d) major medical illness such as cancer, anemia, or thyroid dysfunction; and (e) MRI contraindications. This study was approved by the Research Ethics Committee of Nanjing Medical University and written informed consent was obtained from all participants before the beginning of the study.…”

Aberrant brain functional network strength related to cognitive impairment in age-related hearing loss

“…On the other hand, the SMG becomes a convergence zone of various networks associated with attention and verbal working memory ( 25 ). In ARHL patients with hearing loss ( 26 ) and bilateral sensorineural hearing loss ( 27 ), SMGs showed reduced connectivity with the cerebellum and nucleus accumbens, indicating that hearing deprivation had a negative impact on SMGs. An intracranial EEG study ( 28 ) provided evidence for SMG's role in encoding episodic memory, while some patients with ARHL in our study had poorer scores on the TMT-B.…”

Aberrant dynamic functional and effective connectivity changes of the primary visual cortex in patients with retinal detachment via machine learning

“…The study revealed abnormalities in FC/EC between the frontostriatal network and various nonauditory regions, as well as their relationship with tinnitus perception 14 . However, no studies to date have identi ed abnormalities in dFC and dEC in the V1 of patients with RD by integrating k-means clustering and SVM methods.…”

“…In the context of rs-fMRI, GCA can be applied to investigate the causal effects between brain regions, aiding in the identi cation of information ow directionality by analyzing the temporal dynamics of BOLD signals. Previous studies have integrated FC and GCA methods [12][13][14] . However, recent research has shown that brain activity exhibits dynamic temporal changes 15 .…”