Hearing loss in older adults affects neural systems supporting speech comprehension

Abstract

Hearing loss is one of the most common complaints in adults over the age of 60 and a major contributor to difficulties in speech comprehension. To examine the effects of hearing ability on the neural processes supporting spoken language processing in humans, we used functional magnetic resonance imaging to monitor brain activity while older adults with age-normal hearing listened to sentences that varied in their linguistic demands. Individual differences in hearing ability predicted the degree of language-driven neural recruitment during auditory sentence comprehension in bilateral superior temporal gyri (including primary auditory cortex), thalamus, and brainstem. In a second experiment, we examined the relationship of hearing ability to cortical structural integrity using voxel-based morphometry, demonstrating a significant linear relationship between hearing ability and gray matter volume in primary auditory cortex. Together, these results suggest that even moderate declines in peripheral auditory acuity lead to a systematic downregulation of neural activity during the processing of higher-level aspects of speech, and may also contribute to loss of gray matter volume in primary auditory cortex. More generally, these findings support a resource-allocation framework in which individual differences in sensory ability help define the degree to which brain regions are recruited in service of a particular task.

Figure 1.

Hearing levels for both groups of participants as assessed using pure-tone audiometry. A, Hearing profile for 16 fMRI participants. B, Hearing profile for 25 VBM participants. For both groups, hearing profiles for individual listeners are drawn in light gray, with the average values drawn in black. The cutoff for clinically normal hearing for speech is ≤25 dB HL (shaded) for frequencies up to 4000 Hz.

Figure 2.

Regions in which language-driven activity (object-relative > subject-relative sentences) showed a significant correlation with hearing ability. A, Regions in which poorer-hearing listeners showed less language-driven brain activity. B, Overlap of these regions with cytoarchitectonically defined probable primary auditory cortex (blue outline). C, Thalamic cluster from A (outlined in white) displayed along with probable regions of cortical connectivity from the Oxford Thalamic Connectivity Atlas. The predominant connectivity is to prefrontal cortex, with additional projections to prefrontal and temporal cortices.

Figure 3.

Relationship between regional gray matter volume and hearing ability. We extracted average gray matter values from 25 participants for four cortical regions. Poorer hearing was associated with reduced gray matter volume in right auditory cortex, and showed a similar nonsignificant trend in left auditory cortex; neither of the motor cortex control regions approached significance. Larger markers represent two participants with overlapping scores.