Abstract
We investigated the impact of hearing loss (HL) on emotional processing using task- and rest-based functional magnetic resonance imaging. Two age-matched groups of middle-aged participants were recruited: one with bilateral high-frequency HL and a control group with normal hearing (NH). During the task-based portion of the experiment, participants were instructed to rate affective stimuli from the International Affective Digital Sounds (IADS) database as pleasant, unpleasant, or neutral. In the resting state experiment, participants were told to fixate on a “+” sign on a screen for 5 min. The results of both the task-based and resting state studies suggest that NH and HL patients differ in their emotional response. Specifically, in the task-based study, we found slower response to affective but not neutral sounds by the HL group compared to the NH group. This was reflected in the brain activation patterns, with the NH group employing the expected limbic and auditory regions including the left amygdala, left parahippocampus, right middle temporal gyrus and left superior temporal gyrus to a greater extent in processing affective stimuli when compared to the HL group. In the resting state study, we observed no significant differences in connectivity of the auditory network between the groups. In the dorsal attention network (DAN), HL patients exhibited decreased connectivity between seed regions and left insula and left postcentral gyrus compared to controls. The default mode network (DMN) was also altered, showing increased connectivity between seeds and left middle frontal gyrus in the HL group. Further targeted analysis revealed increased intrinsic connectivity between the right middle temporal gyrus and the right precentral gyrus. The results from both studies suggest neuronal reorganization as a consequence of HL, most notably in networks responding to emotional sounds.
Highlights
Hearing loss (HL) remains one of the most common chronic conditions affecting older adults (Cruickshanks et al, 1998), with the prevalence rate increasing from between 25 and 40% in adults above 65 years of age to greater than 80% in people older than 85 years (Yueh et al, 2003)
The HL group was significantly slower for both pleasant and unpleasant sounds compared to the normal hearing (NH) group (Figure 1A)
Note that the experimental design used an equal number of sounds classified as P, N, and U according to the normative International Affective Digital Sounds (IADS) scores (Bradley and Lang, 2007)
Summary
Hearing loss (HL) remains one of the most common chronic conditions affecting older adults (Cruickshanks et al, 1998), with the prevalence rate increasing from between 25 and 40% in adults above 65 years of age to greater than 80% in people older than 85 years (Yueh et al, 2003). A few brain imaging studies have investigated the impact of HL on aging (Wong et al, 2010; Peelle et al, 2011); these remain the best sources to understand the neural correlates of HL These neural correlates are manifested in decrease in gray matter in the frontal cortex (Wong et al, 2010; Peelle et al, 2011) and a decreased response in the superior temporal cortex, thalamus and brainstem in a speech comprehension task (Peelle et al, 2011). A companion functional study noted increased response of the regions in the frontal and parietal cortices, possibly which related to increased attention processing (Husain et al, 2011b) In the latter fMRI study, participants had mild-to-moderately severe HL with an average age in the mid-fifties and were asked to perform a discrimination task with simple tones and tonal sweeps. When compared to rest trials, task trials resulted in greater response in the temporal, frontal and parietal cortices in the HL group relative to the normal hearing (NH) controls
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