Cochlear output synchrony underlies brain oscillations as a marker for tinnitus - an OPM-MEG study

Despite its high prevalence and socioeconomic costs, the condition of tinnitus shares with related neuropsychiatric disorders the characteristic that, to this day, it cannot be cured. Two contradictory views of the origin of tinnitus (peripheral hyperexcitability and central brain oscillation changes linked to prediction error) are currently discussed without any regard for one another. We now firstly used a compact 64 sensor optically pumped magnetometer (OPM)-MEG system to study a group of tinnitus subjects without co-morbidity of hyperacusis. This new technology provided an unprecedented opportunity for analyzing hemisphere-specific brain activity changes with high spatial resolution in response to pure-tones with a pitch within or outside the tinnitus frequency. We observed in tinnitus smaller ABR amplitudes (reflecting reduced cochlear output synchrony) linked with reduced alpha and enhanced gamma activity at rest (reflecting elevated excitement of intracortical circuits). In tinnitus, reduced alpha and enhanced gamma brain activity at rest were associated with reduced evoked alpha, beta, and gamma in response to pure-tones within tinnitus frequencies (reflecting low signal-to-noise ratios in auditory target regions). Furthermore, elevated gamma activity in key regions in the brain involved in attention control was observed in tinnitus subjects: "hypergamma" activity was seen in posterior/frontal regions, that -when hyperactive - are predicted to trigger excessive attention to irrelevant stimuli. Weakened cochlear output synchrony, possibly through lowering tonic inhibitory strength in the ascending auditory pathway, can thus reduce alpha activity (default-mode network) and unleash cortical regions that control attention to irrelevant stimuli -- tracing tinnitus to perception. Highlights We first used a 64-sensor OPM-MEG to analyze brain activity in tinnitus subjects In tinnitus, brain activity at rest was reduced in the alpha band and increased in the gamma band In tinnitus, the altered brain activity at rest was significantly related to smaller ABR In tinnitus, the higher gamma at rest was linked to lower evoked alpha, beta, and gamma In tinnitus, "hypergamma" posterior/frontal activity indicates attention to irrelevant stimuli In tinnitus, the weak cochlear output synchrony disinhibits brain regions for selective attention