Interhemispheric Auditory Cortical Synchronization in Asymmetric Hearing Loss

Abstract

Objectives: Auditory cortical activation of the two hemispheres to monaurally presented tonal stimuli has been shown to be asynchronous in normal hearing (NH) but synchronous in the extreme case of adult-onset asymmetric hearing loss (AHL) with single-sided deafness. We addressed the wide knowledge gap between these two anchoring states of interhemispheric temporal organization. The objectives of this study were as follows: (1) to map the trajectory of interhemispheric temporal reorganization from asynchrony to synchrony using magnitude of interaural threshold difference as the independent variable in a cross-sectional study and (2) to evaluate reversibility of interhemispheric synchrony in association with hearing in noise performance by amplifying the aidable poorer ear in a repeated measures, longitudinal study.

Design: The cross-sectional and longitudinal cohorts were comprised of 49 subjects (AHL; N = 21; 11 male, 10 female; mean age = 48 years) and NH (N = 28; 16 male, 12 female; mean age = 45 years). The maximum interaural threshold difference of the two cohorts spanned from 0 to 65 dB. Magnetoencephalography analyses focused on latency of the M100 peak response from auditory cortex in both hemispheres between 50 msec and 150 msec following monaural tonal stimulation at the frequency (0.5, 1, 2, 3, or 4 kHz) corresponding to the maximum and minimum interaural threshold difference for better and poorer ears separately. The longitudinal AHL cohort was drawn from three subjects in the cross-sectional AHL cohort (all male; ages 49 to 60 years; varied AHL etiologies; no amplification for at least 2 years). All longitudinal study subjects were treated by monaural amplification of the poorer ear and underwent repeated measures examination of the M100 response latency and quick speech in noise hearing in noise performance at baseline, and postamplification months 3, 6, and 12.

Results: The M100 response peak latency values in the ipsilateral hemisphere lagged those in the contralateral hemisphere for all stimulation conditions. The mean (SD) interhemispheric latency difference values (ipsilateral less contralateral) to better ear stimulation for three categories of maximum interaural threshold difference were as follows: NH (≤ 10 dB)-8.6 (3.0) msec; AHL (15 to 40 dB)-3.0 (1.2) msec; AHL (≥ 45 dB)-1.4 (1.3) msec. In turn, the magnitude of difference values were used to define interhemispheric temporal organization states of asynchrony, mixed asynchrony and synchrony, and synchrony, respectively. Amplification of the poorer ear in longitudinal subjects drove interhemispheric organization change from baseline synchrony to postamplification asynchrony and hearing in noise performance improvement in those with baseline impairment over a 12-month period.

Conclusions: Interhemispheric temporal organization in AHL was anchored between states of asynchrony in NH and synchrony in single-sided deafness. For asymmetry magnitudes between 15 and 40 dB, the intermediate mixed state of asynchrony and synchrony was continuous and reversible. Amplification of the poorer ear in AHL improved hearing in noise performance and restored normal temporal organization of auditory cortices in the two hemispheres. The return to normal interhemispheric asynchrony from baseline synchrony and improvement in hearing following monoaural amplification of the poorer ear evolved progressively over a 12-month period.

Fig. 1.

Raw MEG sensor data and M100 peak source localization from normal hearing and asymmetric hearing loss subjects. Left column, MEG data traces by hemisphere relative to the stimulated ear. Right column, M100 response peak localization to auditory cortex (MRI insets) and latency determination (dashed lines). Interhemispheric latency difference is greater for the normal hearing subject. MEG indicates magnetoencephalography; MRI, magnetic resonance imaging.

Fig. 2.

M100 auditory cortical response latency in the hemisphere referenced to the stimulated ear. M100 median latencies in the NH cohort are 100.4 msec (contralateral) and 108.6 msec (ipsilateral) and AHL cohort are 98.3 msec (contralateral, better ear), 100.8 msec (ipsilateral, better), 100.0 msec (contralateral, poorer ear), and 105.8 msec (ipsilateral, poorer ear). Ipsilateral cortical response latency to both better and poorer ear stimulation in the AHL cohort is shorter compared with the NH cohort. Tukey boxplots truncated at the 10th and 90th percentiles. AHL indicates asymmetric hearing loss; Contra, contralateral; Ipsi, ipsilateral; NH, normal hearing.

Fig. 3.

M100 interhemispheric latency difference referenced to stimulation at the frequency corresponding to minimum (min) and maximum (max) interaural threshold difference. The min and max interaural threshold difference in the NH cohort is essentially identical, denoted by min/max. M100 median interhemispheric difference latencies in the NH cohort are 8.3 msec and AHL cohort are 5.8 msec (min, better ear), 2.5 msec (max, better), 5.8 msec (min, poorer ear), and 4.6 msec (max, poorer ear). Using NH cohort as the comparator, pairwise comparisons show all four AHL interhemispheric latency differences are smaller (p < 0.001, t test with Bonferroni correction, denoted by *). Tukey boxplots truncated at the 10th and 90th percentiles. AHL indicates asymmetric hearing loss; max, maximum interaural threshold difference; min, minimum interaural threshold difference; NH, normal hearing.

Fig. 4.

M100 interhemispheric latency difference surrounding the frequency at maximum interaural threshold difference in notched AHL audiometric profile. X axis indicates the number of frequency steps away from the frequency at maximum interaural threshold difference. Interhemispheric latency difference values increase at lower and higher frequencies away from the minimum interhemispheric latency value at maximum interaural threshold difference (p = 0.05, Wilcoxon signed-rank test). Interhemispheric synchrony is focal to the frequency at maximum interaural threshold difference in notch shaped AHL pattern. Letter symbols are used to denote individual subjects. AHL indicates asymmetric hearing loss.

Fig. 5.

Reversal of the M100 interhemispheric latency difference from synchrony to asynchrony and hearing in noise improvement in three AHL subjects treated by monaural amplification of the poorer ear. Assessments at baseline, and months 3, 6, and 12 following poorer ear amplification are exhibited. A–C, Audiometric profiles of the three subjects. D and E, M100 interhemispheric latency difference values show steady progression toward values expected of normal-hearing subjects over a 12 mo period of monaural amplification. Interhemispheric temporal organization reverses from synchrony to asynchrony by increasing activity of the poorer ear in AHL. F, Poorer ear hearing in noise performance improvement is evident at month 6 and plateaus thereafter in the two subjects (R1940 and R2006) with abnormal baseline performance. AHL indicates asymmetric hearing loss; QuickSIN, quick speech in noise.