Cingulo-Opercular Function During Word Recognition in Noise for Older Adults with Hearing Loss

Abstract

Background/study context: Adaptive control, reflected by elevated activity in cingulo-opercular brain regions, optimizes performance in challenging tasks by monitoring outcomes and adjusting behavior. For example, cingulo-opercular function benefits trial-level word recognition in noise for normal-hearing adults. Because auditory system deficits may limit the communicative benefit from adaptive control, we examined the extent to which cingulo-opercular engagement supports word recognition in noise for older adults with hearing loss (HL).

Methods: Participants were selected to form groups with Less HL (n = 12; mean pure tone threshold, pure tone average [PTA] = 19.2 ± 4.8 dB HL [hearing level]) and More HL (n = 12; PTA = 38.4 ± 4.5 dB HL, 0.25-8 kHz, both ears). A word recognition task was performed with words presented in multitalker babble at +3 or +10 dB signal-to-noise ratios (SNRs) during a sparse acquisition fMRI experiment. The participants were middle-aged and older (ages: 64.1 ± 8.4 years) English speakers with no history of neurological or psychiatric diagnoses.

Results: Elevated cingulo-opercular activity occurred with increased likelihood of correct word recognition on the next trial (t(23) = 3.28, p = .003), and this association did not differ between hearing loss groups. During trials with word recognition errors, the More HL group exhibited higher blood oxygen level-dependent (BOLD) contrast in occipital and parietal regions compared with the Less HL group. Across listeners, more pronounced cingulo-opercular activity during recognition errors was associated with better overall word recognition performance.

Conclusion: The trial-level word recognition benefit from cingulo-opercular activity was equivalent for both hearing loss groups. When speech audibility and performance levels are similar for older adults with mild to moderate hearing loss, cingulo-opercular adaptive control contributes to word recognition in noise.

Figure 1

Mean pure tone thresholds across ears with standard error bars for the hearing loss groups. The Less HL group had a mild sloping hearing loss, while the More HL group had a mild to moderate sloping hearing loss that affected sensitivity for pure tones at 2 kHz and above.

Figure 2

A) A block design was used to present rest trials, babble (B), and words in babble (W+B). Lower and higher blocks depict the +3 and +10 dB SNR, respectively. B) The BOLD response to conditions, as modelled by the GLM. C) Error effects were estimated by comparing BOLD after incorrect versus correct responses. D) Predictive activity compared the likelihood of correct responses after increased or decreased BOLD.

Figure 3

A) The word recognition task trials elicited elevated BOLD contrast within temporal and frontal regions (red; Task > Rest). When trials that presented words in babble were contrasted with babble-only presentations, BOLD contrast increased in the left anterior insula and inferior frontal gyrus (green; Task > Babble). Overlapping effects are shown in motor cortex in yellow (green + red). Cingulo-opercular BOLD contrast increased during recognition error trials (blue; Incorrect > Correct Recognition). B) During trials with recognition errors, the More HL group increased BOLD contrast in inferior occipital and left superior parietal cortices while the Less HL group exhibited a relative decrease. C) BOLD contrast increased to a greater extent during trials in the +3 dB SNR compared to +10 dB SNR (red) in right anterior insula/frontal operculum and middle temporal cortices. BOLD contrast decreased to a greater extent when +3 dB SNR trials were compared to +10 dB SNR trials throughout a default mode network distribution (blue). D) Voxel-level results where elevated BOLD contrast was associated with correct recognition on the next trial. E) Cingulo-opercular BOLD contrast within the mask region (red) was significantly related to next trial word recognition and this effect did not decline significantly with increasing hearing loss. F) Participants with better overall word recognition demonstrated the largest error-related cingulo-opercular activations within the same mask. Note: LH and RH indicate left and right hemispheres, respectively.