Multisite transcranial Random Noise Stimulation (tRNS) modulates the distress network activity and oscillatory powers in subjects with chronic tinnitus

Highlights

• DLPFC and auditory cortex tRNS was used in sequence for treating chronic tinnitus.

• Multisite-tRNS induced important oscillatory power changes.

• tRNS increased alpha power in the auditory and prefrontal cortex.

• tRNS could modulate the activity and connectivity of the distress network.

• tRNS decreased beta2 activity in the DLPFC, OFC, ACC and the parahippocampus.

Abstract

Tinnitus is a common disorder in which auditory and non-auditory areas are involved as a network. Therefore, the multisite protocol of brain stimulation (tRNS) seems effective in relieving tinnitus symptoms. This study aimed to verify the modulatory effects of multisite tRNS on the tinnitus network. Thirty-two tinnitus-suffering patients received two consecutive sessions of tRNS (SHAM+ REAL) applied over the T3, T4 (the auditory cortex group) and F4, FP1 followed by T3, T4 (the multisite group). A 3-min resting-state EEG was recorded before and immediately after each session. After the multisite-tRNS real session, there was a significantly increased power in the alpha-1 band at the auditory and prefrontal cortex accompanied by decreased power in the delta and beta-2 bands in the prefrontal cortex. Standardized low-resolution brain electromagnetic tomography (sLORETA) showed a significant decrease in beta-2 activity in the prefrontal cortex, anterior cingulate cortex, and the parahippocampus and decreased alpha connectivity between the right prefrontal cortex and the left auditory cortex. No significant effects were noticed for the sham session. This study showed that tRNS has modulatory effects on the electrical activity of the brain and that targeting prefrontal and auditory areas in sequence could modulate the distress network and multiple hubs in the tinnitus network.

Introduction

Tinnitus is a common medical condition that has a significant impact on daily life, function, and emotions [1], [2]. In USA, there are at least 12 million tinnitus sufferers, >2 million of whom suffer debilitating symptoms [3]. Thus, epidemiologic situation has urged researchers to exert more efforts in determining the underlying mechanisms and the neural substrates of tinnitus. The development of neuroimaging studies has helped in this concern [4]. Neuromodulation using electrical stimulation is one such approach which has been well developed and frequently used recently, particularly for its capability to be combined with neuroimaging techniques.

Transcranial random noise stimulation (tRNS), a form of electrical stimulation, was used in tinnitus studies for the first time in comparison with other types of auditory cortex stimulation showing superiority in relieving tinnitus symptoms [5]. tRNS was also used in a multisite protocol in which both auditory and prefrontal areas were targeted in sequence, using tDCS¹ for the prefrontal area [6], and recently tRNS [7] yielding much relief in tinnitus symptoms. The rationale for targeting non-auditory areas depended on reports demonstrated the role of these areas alongside the auditory cortex in generating tinnitus and its related distress [8].

Neuroimaging studies have reported the involvement of the dorsolateral prefrontal cortex (DLPFC) [9], [10], orbitofrontal cortex (OFC) [11], anterior cingulate cortex (ACC) [8], [12], insula [13], amygdala [14], and parahippocampus [14], [15], [16] in tinnitus perception and its related distress. There are functional interactions between these areas and the auditory cortex which is referred to as the “tinnitus network” [17], [18], [19]. EEG studies on tinnitus patients reported some alterations in the power of oscillatory brain activity. The decreased alpha power in the auditory cortex was substituted for by increased theta power; likewise, an increase in gamma power in the contralateral cortex was also reported [20], [21]. A recent EEG study demonstrated the relationship between tinnitus distress and increased beta band activity in the ACC [22]. Moreover, the amount of distress was correlated to the alpha band activity in several brain areas, forming the distress network [11]. The tRNS-EEG combined approach can provide an additional opportunity to study these functional interactions and how they can be modulated in order to reach the therapeutic effects of the intervention [4]. To the best of our knowledge, no previous study has used such approach for tRNS in tinnitus patients; and that was the purpose of the current study.