Journal Article

Switching tinnitus on or off: An initial investigation into the role of the pregenual and rostral to dorsal anterior cingulate cortices

Verplancke, Thierry, De Ridder, Dirk, Byczynski, Gabriel, Ost, Jan, Song, Jae-Jin, Vanneste, Sven

2024

Overview

•Increased theta activity in the pregenual anterior cingulate cortex triggers tinnitus.•Decreased theta functional connectivity between pregenual anterior cingulate cortex and auditory cortex accompanies tinnitus onset.•Alpha differences in the pregenual anterior cingulate cortex and increased alpha functional connectivity differentiate the no-tinnitus state from healthy subjects.•Insights into mechanisms of tinnitus generation and potential treatment strategies akin to chronic neuropathic pain. Research indicates that hearing loss significantly contributes to tinnitus, but it alone does not fully explain its occurrence, as many people with hearing loss do not experience tinnitus. To identify a secondary factor for tinnitus generation, we examined a unique dataset of individuals with intermittent chronic tinnitus, who experience fluctuating periods of tinnitus. EEGs of healthy controls were compared to EEGs of participants who reported perceiving tinnitus on certain days, but no tinnitus on other days.. The EEG data revealed that tinnitus onset is associated with increased theta activity in the pregenual anterior cingulate cortex and decreased theta functional connectivity between the pregenual anterior cingulate cortex and the auditory cortex. Additionally, there is increased alpha effective connectivity from the dorsal anterior cingulate cortex to the pregenual anterior cingulate cortex. When tinnitus is not perceived, differences from healthy controls include increased alpha activity in the pregenual anterior cingulate cortex and heightened alpha connectivity between the pregenual anterior cingulate cortex and auditory cortex. This suggests that tinnitus is triggered by a switch involving increased theta activity in the pregenual anterior cingulate cortex and decreased theta connectivity between the pregenual anterior cingulate cortex and auditory cortex, leading to increased theta-gamma cross-frequency coupling, which correlates with tinnitus loudness. Increased alpha activity in the dorsal anterior cingulate cortex correlates with distress. Conversely, increased alpha activity in the pregenual anterior cingulate cortex can transiently suppress the phantom sound by enhancing theta connectivity to the auditory cortex. This mechanism parallels chronic neuropathic pain and suggests potential treatments for tinnitus by promoting alpha activity in the pregenual anterior cingulate cortex and reducing alpha activity in the dorsal anterior cingulate cortex through pharmacological or neuromodulatory approaches.

• Publisher: Elsevier Inc,Elsevier Limited,Elsevier
• Subject: Adult / Aged / Alpha Rhythm - physiology / Auditory Cortex - diagnostic imaging / Auditory Cortex - physiopathology / Chronic pain / Cortex (auditory) / Cortex (cingulate) / Distress / Dorsal anterior cingulate cortex / Ears & hearing / Electroencephalography / Female / Gyrus Cinguli - diagnostic imaging / Gyrus Cinguli - physiopathology / Hearing loss / Humans / Hypotheses / Male / Middle Aged / Neural networks / Neuralgia / On/off switch / Pregenual anterior cingulate cortex / Questionnaires / Theta Rhythm - physiology / Theta rhythms / Tinnitus / Tinnitus - diagnostic imaging / Tinnitus - physiopathology