The impact of mild-to-severe hearing loss on the neural dynamics serving verbal working memory processing in children

Abstract

Children with hearing loss (CHL) exhibit delays in language function relative to children with normal hearing (CNH). However, evidence on whether these delays extend into other cognitive domains such as working memory is mixed, with some studies showing decrements in CHL and others showing CHL performing at the level of CNH. Despite the growing literature investigating the impact of hearing loss on cognitive and language development, studies of the neural dynamics that underlie these cognitive processes are notably absent. This study sought to identify the oscillatory neural responses serving verbal working memory processing in CHL compared to CNH. To this end, participants with and without hearing loss performed a verbal working memory task during magnetoencephalography. Neural oscillatory responses associated with working memory encoding and maintenance were imaged separately, and these responses were statistically evaluated between CHL and CNH. While CHL performed as well on the task as CNH, CHL exhibited significantly elevated alpha-beta activity in the right frontal and precentral cortices during encoding relative to CNH. In contrast, CHL showed elevated alpha maintenance-related activity in the right precentral and parieto-occipital cortices. Crucially, right superior frontal encoding activity and right parieto-occipital maintenance activity correlated with language ability across groups. These data suggest that CHL may utilize compensatory right-hemispheric activity to achieve verbal working memory function at the level of CNH. Neural behavior in these regions may impact language function during crucial developmental ages.

Keywords: Audiology; Cognition; Hearing aids; Neurophysiology; Oscillations.

Fig. 1

Task paradigm. Participants were initially presented with a fixation for 1.3 s. A 2 × 3 grid of 6 consonants was then presented for 2.0 s (i.e., encoding phase). The letters then disappeared from the grid for 3.0 s (i.e., maintenance phase). Finally, a single probe letter was presented in the top middle square of the grid (i.e., retrieval phase). Participants were instructed to respond via button press whether the probe letter was one of the six letters presented in the previous encoding set. A total of 128 trials were presented.

Fig. 2

Behavioral Results. Box plots of accuracy (in percent correct; left) and reaction time (in ms; right) are shown. The center line within each box denotes the median frequency, and the bottom and top of each box designate the first and third quartile, respectively. Each lower and upper stem reflects the minimum and maximum values. The CNH are denoted in blue, while the CHL are shown in green. There was a marginal difference in reaction time between groups, such that CHL were slower to respond than CNH, t(28) = 1.803, p = .082. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

Significant time–frequency windows serving working memory processing. Time-frequency spectrogram from a representative sensor averaged across CNH and CHL is shown on the bottom, with frequency (in Hz) shown on the y-axis and time (in s; 0.0 s = encoding stimulus onset) shown on the x-axis. Color bars denote the percentage change from baseline, with warmer colors reflecting increases in power from baseline (i.e., ERS) and cooler colors reflecting decreases in neural power from baseline (i.e., ERD). Dotted boxes denote time–frequency components that were selected for source imaging. The topographic distribution of activity across all sensors within each time–frequency window is shown on top (left: encoding; right: maintenance). Note that the same sensor is highlighted with a black box in each topographic map and shown in the bottom panel.

Fig. 4

Grand averaged maps of encoding and maintenance-related neural activity. A) Grand averages (pseudo-t) of alpha–beta encoding-related activity for CNH (top) and CHL (bottom). Left hemispheric activity is shown on the left, while right hemispheric activity is shown on the right. Pseudo-t values are denoted with the color bar to the right, whereby warmer colors denote an increase (ERS) from baseline, while cooler colors denote a decrease (ERD) from baseline. B) Grand averages (pseudo-t) of alpha maintenance-related activity for CNH (top) and CHL (bottom). Left hemispheric activity is shown on the left, while right hemispheric activity is shown on the right. Pseudo-t values are denoted with the color bar to the right.

Fig. 5

Impact of hearing loss on working memory neural dynamics. A) Whole-brain statistical analyses showed that CHL had significantly greater alpha–beta activity in the right superior and inferior frontal and precentral gyri relative to CNH, p < .005 (corrected). B) Response power (pseudo-t, y-axis) in the right superior frontal cortex (starred in A) was significantly correlated with WASI-II Verbal Composite scores (x-axis) across groups, p = .034. Data is color-coded by group, with CNH in blue and CHL in green. C) Whole-brain statistical analyses showed significant elevations in alpha activity during the maintenance phase in CHL relative to CNH in the right parieto-occipital cortex and right precentral gyrus, p < .005 (corrected). D) Maintenance-related alpha activity (pseudo-t, y-axis) in the parieto-occipital cortex (starred in C) was significantly positively correlated with WASI-II Verbal Composite scores (x-axis) across groups, p = .020. Data is color-coded by group, with CNH in blue and CHL in green. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)