Functional changes in the auditory cortex and associated regions caused by different acoustic stimuli in patients with presbycusis and tinnitus

Abstract

Presbycusis and tinnitus are the two most common hearing related pathologies. Although both of these conditions presumably originate in the inner ear, there are several reports concerning their central components. Interestingly, the onset of presbycusis coincides with the highest occurrence of tinnitus. The aim of this study was to identify age, hearing loss, and tinnitus related functional changes, within the auditory system and its associated structures. Seventy-eight participants were selected for the study based on their age, hearing, and tinnitus, and they were divided into six groups: young controls (Y-NH-NT), subjects with mild presbycusis (O-NH-NT) or expressed presbycusis (O-HL-NT), young subjects with tinnitus (Y-NH-T), subjects with mild presbycusis and tinnitus (O-NH-T), and subjects with expressed presbycusis and tinnitus (O-HL-T). An MRI functional study was performed with a 3T MRI system, using an event related design (different types of acoustic and visual stimulations and their combinations). The amount of activation of the auditory cortices (ACs) was dependent on the complexity of the stimuli; higher complexity resulted in a larger area of the activated cortex. Auditory stimulation produced a slightly greater activation in the elderly, with a negative effect of hearing loss (lower activation). The congruent audiovisual stimulation led to an increased activity within the default mode network, whereas incongruent stimulation led to increased activation of the visual cortex. The presence of tinnitus increased activation of the AC, specifically in the aged population, with a slight prevalence in the left AC. The occurrence of tinnitus was accompanied by increased activity within the insula and hippocampus bilaterally. Overall, we can conclude that expressed presbycusis leads to a lower activation of the AC, compared to the elderly with normal hearing; aging itself leads to increased activity in the right AC. The complexity of acoustic stimuli plays a major role in the activation of the AC, its support by visual stimulation leads to minimal changes within the AC. Tinnitus causes changes in the activity of the limbic system, as well as in the auditory AC, where it is bound to the left hemisphere.

Keywords: auditory system; functional MRI; limbic system; presbycusis; tinnitus.

FIGURE 1

Delineation of the applied masks. AC in red (structures: part of the superior temporal gyrus, part of the transverse temporal gyrus, central and parietal operculum, planum polare, planum temporale), and tinnitus related structures in green (Amg, HP, Ins).

FIGURE 2

The results of the audiometric examination of all groups. (A) The comparison of the pure tone average among individual groups (ANOVA). (B) The comparison of speech reception thresholds among individual groups. (C) The comparison of speech in noise perception among individual groups expressed as stimulus intensity in 50% speech recognition.

FIGURE 3

Cortical activation evoked by the combination of all acoustic stimuli within the mask of AC, the comparison of all elderly (O-NH-NZT + O-NH-T + O-HL-NT + O-HL-T) vs. young groups (Y-NH-NT + Y-NH-T). The comparison of elderly > young in red (structures: left middle temporal gyrus, central operculum), young > elderly in green (structures: left transverse temporal gyrus, left planum temporale, left superior temporal gyrus and right middle temporal gyrus), p = 0.05, uncorrected.

FIGURE 4

Cortical activation by a combination of all acoustical stimuli within the mask of AC, the comparison of all tinnitus (Y-NH-T + O-NH-T + O-HL-T) vs. no tinnitus (Y-NH-NT + O-NH-NT + O-HL-NT) groups. The comparison of tinnitus > no tinnitus in red (structures: left temporal gyrus, left middle temporal gyrus, left planum temporale), no tinnitus > tinnitus in green (structures: left planum temporale, left central operculum, right superior temporal gyrus, right middle temporal gyrus), p = 0.05 uncorrected.

FIGURE 5

Cortical of activation by a combination of all acoustic stimuli within the tinnitus related structures (Amg, HP, Ins), the comparison of all tinnitus (Y-NH-T + O-NH-T + O-HL-T) vs. no tinnitus (Y-NH-NT + O-NH-NT + O-HL-NT) groups. The comparison of tinnitus > no tinnitus in red (structures: bilateral Ins, HP), no tinnitus > tinnitus in green (structures: no activation), p = 0.05 uncorrected.

FIGURE 6

Cortical activation by a combination of all acoustic stimuli within the mask of AC, the comparison of Y-NH-T vs. Y-NH-NT. The comparison of tinnitus > no tinnitus in red (structures: left middle temporal gyrus), no tinnitus > tinnitus in green (structures: right middle temporal gyrus, transversal temporal gyrus bilaterally), p = 0.05 uncorrected.

FIGURE 7

Cortical activation by a combination of all acoustic stimuli within the mask of AC, a comparison of the elderly with normal hearing (O-NH-NT + O-NH-T) vs. elderly with hearing loss (O-HL-NT + O-HL-T) groups. A comparison of normal hearing > hearing loss in red (structures: right planum temporale), hearing loss > normal hearing in green (structures: none), p = 0.05 uncorrected.

FIGURE 8

Cortical activation was evoked by a combination of the word + babble + visual stimulus. In the case of congruent visual stimulation, the activation is in green (structures of default mode network), incongruent in red (visual cortex), p = 0.001 incorrected.