The neural code of auditory phantom perception

Abstract

Tinnitus is defined by an auditory perception in the absence of an external source of sound. This condition provides the distinctive possibility of extracting neural coding of perceptual representation. Previously, we had established that tinnitus is characterized by enhanced magnetic slow-wave activity (approximately 4 Hz) in perisylvian or putatively auditory regions. Because of works linking high-frequency oscillations to conscious sensory perception and positive symptoms in a variety of disorders, we examined gamma band activity during brief periods of marked enhancement of slow-wave activity. These periods were extracted from 5 min of resting spontaneous magnetoencephalography activity in 26 tinnitus and 21 control subjects. Results revealed the following, particularly within a frequency range of 50-60 Hz: (1) Both groups showed significant increases in gamma band activity after onset of slow waves. (2) Gamma is more prominent in tinnitus subjects than in controls. (3) Activity at approximately 55 Hz determines the laterality of the tinnitus perception. Based on present and previous results, we have concluded that cochlear damage, or similar types of deafferentation from peripheral input, triggers reorganization in the central auditory system. This produces permanent alterations in the ongoing oscillatory dynamics at the higher layers of the auditory hierarchical stream. The change results in enhanced slow-wave activity reflecting altered corticothalamic and corticolimbic interplay. Such enhancement facilitates and sustains gamma activity as a neural code of phantom perception, in this case auditory.

Figure 1.

Time-frequency representation of high-frequency oscillatory activity triggered to the onset of SWA. Top panels depict ERSPs for both groups and p values derived from t tests for the left temporal source, whereas the bottom panels show this for the right temporal source. Note that a difference between the groups can be seen at 50–60 Hz, particularly for the right temporal source. The reason for this difference can be seen more clearly in Figure 2.

Figure 2.

Overlay of SWA (black line; left y-axis) and 55–60 Hz activity (gray line; right y-axis) for tinnitus and control subjects at the right temporal source. Control subjects in particular show a clear increase of gamma activity along with SWA, starting before SWA onset. In the same window, tinnitus subjects reduce their gamma activity, leading to the significant group difference observed in Figure 1.

Figure 3.

Time-frequency representation of cross-correlation (Cross-Corr.) between the SWA–ERSP and the ERSPs of the other frequencies. A marked difference can be seen between the groups, particularly at the right temporal source, reflecting higher cross-correlation between SWA and ∼55 Hz in the control group. This indicates that these time series are more similar in the control group.

Figure 4.

Normalized power spectrum averaged (±SE) over left and right temporal sources shows that gamma activity increases after onset of strong SWA in both groups. Generally, however, the content of 55–60 Hz activity to the overall power is increased in tinnitus. BL, Baseline.

Figure 5.

Tinnitus laterality is reflected by 55 Hz oscillatory activity as measured by the laterality index (mean ±SE). Participants with right lateralized tinnitus have left dominant 55 Hz activity and vice versa in left lateralized tinnitus. Bilateral tinnitus subjects exhibit a laterality index close to zero, indicating absence of a hemispheric dominance of 55 Hz activity.