Psychoacoustic tinnitus loudness and tinnitus-related distress show different associations with oscillatory brain activity

Abstract

Background: The phantom auditory perception of subjective tinnitus is associated with aberrant brain activity as evidenced by magneto- and electroencephalographic studies. We tested the hypotheses (1) that psychoacoustically measured tinnitus loudness is related to gamma oscillatory band power, and (2) that tinnitus loudness and tinnitus-related distress are related to distinct brain activity patterns as suggested by the distinction between loudness and distress experienced by tinnitus patients. Furthermore, we explored (3) how hearing impairment, minimum masking level, and (4) psychological comorbidities are related to spontaneous oscillatory brain activity in tinnitus patients.

Methods and findings: Resting state oscillatory brain activity recorded electroencephalographically from 46 male tinnitus patients showed a positive correlation between gamma band oscillations and psychoacoustic tinnitus loudness determined with the reconstructed tinnitus sound, but not with the other psychoacoustic loudness measures that were used. Tinnitus-related distress did also correlate with delta band activity, but at electrode positions different from those associated with tinnitus loudness. Furthermore, highly distressed tinnitus patients exhibited a higher level of theta band activity. Moreover, mean hearing loss between 0.125 kHz and 16 kHz was associated with a decrease in gamma activity, whereas minimum masking levels correlated positively with delta band power. In contrast, psychological comorbidities did not express significant correlations with oscillatory brain activity.

Conclusion: Different clinically relevant tinnitus characteristics show distinctive associations with spontaneous brain oscillatory power. Results support hypothesis (1), but exclusively for the tinnitus loudness derived from matching to the reconstructed tinnitus sound. This suggests to preferably use the reconstructed tinnitus spectrum to determine psychoacoustic tinnitus loudness. Results also support hypothesis (2). Moreover, hearing loss and minimum masking level correlate with oscillatory power in distinctive frequency bands. The lack of an association between psychological comorbidities and oscillatory power may be attributed to the overall low level of mental health problems in the present sample.

Figure 1. Averaged audiograms of the patient and control groups.

Hearing ability was determined between 0.125 kHz and 16 kHz. Group means are shown. Tinnitus patients exhibit more pronounced hearing loss than controls above 2 kHz. Note that the controls as a group exhibit noticeable hearing impairment above 10 kHz.

Figure 2. Spatio-spectral distribution of correlation strength between tinnitus loudness and oscillatory band power for the subgroup with pure tone tinnitus.

Group averages are shown. Power spectra were interpolated with a resolution of 40 points per 1 Hz. Tinnitus loudness was determined by adjusting the contribution of each frequency component and the loudness of such a reconstructed tinnitus spectrum to the perceived tinnitus. Correlations were controlled for age, global psychological distress (GPD), and mean hearing loss (MHL) between 0.125 kHz and 16 kHz. (A) Correlation strength (Spearman's ) at each electrode and frequency point is shown. Plots (B) and (C) show correlation maps corresponding to (A) with averaged correlation strength () topographies for the tinnitus loudness and delta (B) or gamma (C) oscillatory power. Correlation strength for delta band power and tinnitus loudness was highest in the frontal half of the brain and lowest at posterior locations. For the correlation between gamma band power and tinnitus loudness the distribution of correlation strength across electrode positions was more uniform. Highest correlation strength was reached at the left temporal and right occipital electrode positions. After FDR correction (FDR 0.05: ) correlations remained significant at all electrode positions except for T8 and P8 locations for the gamma band, whereas significant correlations in the delta band were attained at the fronto-central locations Fp2, F1, Fz, F2, F4, F8, C3, Cz, and at P7.

Figure 3. Correlation strength between tinnitus loudness and oscillatory band power for the subgroup with unilateral pure tone tinnitus.

Group averages are shown. Electrode positions of left and right hemisphere were interchanged for right-sided tinnitus. Left ear in the plots is the tinnitus ear. Power spectra were interpolated with a resolution of 40 points per 1 Hz. Tinnitus loudness was determined by matching the contribution of each frequency component and the loudness of such a reconstructed tinnitus spectrum to the perceived tinnitus. Correlations with oscillatory band power were controlled for age, global psychological distress (GPD), and mean hearing loss (MHL) between 0.125 kHz and 16 kHz. Note that correlation strength for tinnitus loudness and delta band power is highest at the fronto-central electrodes contralateral to the tinnitus ear (A), whereas it is highest at the contralateral fronto-temporal electrodes for tinnitus loudness and gamma band power (B). Correlation strengths did not remain significant after FDR correction (FDR 0.05).

Figure 4. Correlation strength between MML and oscillatory band power.

Group average for all tinnitus patients is shown. Power spectra were interpolated with a resolution of 40 points per 1 Hz. Correlations were controlled for age, global psychological distress (GPD) and mean hearing loss (MHL) between 0.125 kHz and 16 kHz. (A) Correlation strength (Spearman's ) at each electrode and frequency point is shown. Plot (B) shows the correlation map with averaged correlation strength () topographies between MML and delta oscillatory power. After FDR correction, correlations at the F8 and T8 electrode position remained significant (FDR 0.05: ).

Figure 5. Correlation strength between tinnitus-related distress and oscillatory band power.

Group average for all tinnitus patients is shown. Power spectra were interpolated with a resolution of 40 points per 1 Hz. (A) Correlation strength (Spearman's ) at each electrode and frequency point is shown. Plot (B) shows the correlation map with averaged correlation strength () topographies between tinnitus-related distress and delta band power. Irrespective of tinnitus laterality, correlation strength is most pronounced at frontal and temporal locations of the left hemisphere. After FDR correction (FDR 0.05) correlations did not remain significant.