Alterations of brain activity and functional connectivity in transition from acute to chronic tinnitus.

Liping Lan,Chang‐Dong Wang,Yanhong Chen,Yiqing Zheng,Jiahao Liu,Jiahong Li,Yuexin Cai,Yuchen Chen,Fei Zhao,Yuanqing Li,Guisheng Chen,Wenrui Li,Wan Chen

doi:10.1002/hbm.25238

Abstract

The objective of this study was to investigate alterations to brain activity and functional connectivity in patients with tinnitus, exploring neural features in the transition from acute to chronic phantom perception. Twenty‐four patients with acute tinnitus, 23 patients with chronic tinnitus, and 32 healthy controls were recruited. High‐density electroencephalography (EEG) was used to explore changes in brain areas and functional connectivity in different groups. When compared with healthy subjects, acute tinnitus patients had a significant reduction in superior frontal cortex activity across all frequency bands, whereas chronic tinnitus patients had a significant reduction in the superior frontal cortex at beta 3 and gamma frequency bands as well as a significant increase in the inferior frontal cortex at delta‐band and superior temporal cortex at alpha 1 frequency band. When compared to the chronic tinnitus group, the acute tinnitus group activity was significantly increased in the middle frontal and parietal gyrus at the gamma‐band. Functional connectivity analysis showed that the chronic tinnitus group had increased connections between the parahippocampus gyrus, posterior cingulate cortex, and precuneus when compared with the healthy group. Alterations of local brain activity and connections between the parahippocampus gyrus and other nonauditory areas appeared in the transition from acute to chronic tinnitus. This indicates that the appearance and development of tinnitus is a dynamic process involving aberrant local neural activity and abnormal connectivity in multifunctional brain networks.

Highlights

Tinnitus is the perception of a phantom sound lacking any external or internal sound stimulation
Acute tinnitus patients had a significant reduction in superior frontal cortex (BA 6) activity across all frequency bands when compared with the healthy subjects
Chronic tinnitus subjects had a significant increase brain activity in the inferior frontal cortex (BA 47) for the delta-band and the superior temporal cortex (BA 13) for alpha 1 frequency band when compared with the healthy subjects

Summary

Introduction

Tinnitus is the perception of a phantom sound lacking any external or internal sound stimulation. Recent studies have found that abnormal central reorganization in subjective chronic tinnitus involves auditory and nonauditory brain areas such as the frontal cortex, parahippocampal gyrus, caudate nucleus, cingulate cortex, and insula (Araneda et al, 2018; Besteher et al, 2019; De et al, 2014; Elgoyhen, Langguth, Ridder, & Vanneste, 2015; Henderson-Sabes et al, 2019; Schlee et al, 2009; Vanneste, Alsalman, & De Ridder, 2018; Xu et al, 2019), and that these central neural changes were possible contributors to the clinical symptoms of tinnitus, for example, impairment of perception, cognition, attention, memory, and emotion (Besteher et al, 2019; Chen et al, 2017; De, Elgoyhen, Romo, & Langguth, 2011; Husain, 2016; Joos, Vanneste, & De Ridder, 2012; Pattyn et al, 2016; Vanneste, To, & De Ridder, 2019). As the parahippocampal area has been hypothesized to play a crucial role in memory recollection, sending information from the hippocampus to the association areas, such a correlation might indicate its involvement in the generation of tinnitus

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