Neural Correlates of Speech Processing in Prelingually Deafened Children and Adolescents with Cochlear Implants

Prelingually deafened children with cochlear implants stand a good chance of developing satisfactory speech performance. Nevertheless, their eventual language performance is highly variable and not fully explainable by the duration of deafness and hearing experience. In this study, two groups of cochlear implant users (CI groups) with very good basic hearing abilities but non-overlapping speech performance (very good or very bad speech performance) were matched according to hearing age and age at implantation. We assessed whether these CI groups differed with regard to their phoneme discrimination ability and auditory sensory memory capacity, as suggested by earlier studies. These functions were measured behaviorally and with the Mismatch Negativity (MMN). Phoneme discrimination ability was comparable in the CI group of good performers and matched healthy controls, which were both better than the bad performers. Source analyses revealed larger MMN activity (155–225 ms) in good than in bad performers, which was generated in the frontal cortex and positively correlated with measures of working memory. For the bad performers, this was followed by an increased activation of left temporal regions from 225 to 250 ms with a focus on the auditory cortex. These results indicate that the two CI groups developed different auditory speech processing strategies and stress the role of phonological functions of auditory sensory memory and the prefrontal cortex in positively developing speech perception and production

When Hearing Is Tricky: Speech Processing Strategies in Prelingually Deafened Children and Adolescents with Cochlear Implants Having Good and Poor Speech Performance

Cochlear implants provide individuals who are deaf with access to speech. Although substantial advancements have been made by novel technologies, there still is high variability in language development during childhood, depending on adaptation and neural plasticity. These factors have often been investigated in the auditory domain, with the mismatch negativity as an index for sensory and phonological processing. Several studies have demonstrated that the MMN is an electrophysiological correlate for hearing improvement with cochlear implants. In this study, two groups of cochlear implant users, both with very good basic hearing abilities but with non-overlapping speech performance (very good or very poor speech performance), were matched according to device experience and age at implantation. We tested the perception of phonemes in the context of specific other phonemes from which they were very hard to discriminate (e.g., the vowels in /bu/ vs. /bo/). The most difficult pair was individually determined for each participant. Using behavioral measures, both cochlear implants groups performed worse than matched controls, and the good performers performed better than the poor performers. Cochlear implant groups and controls did not differ during time intervals typically used for the mismatch negativity, but earlier: source analyses revealed increased activity in the region of the right supramarginal gyrus (220-260 ms) in good performers. Poor performers showed increased activity in the left occipital cortex (220-290 ms), which may be an index for cross-modal perception. The time course and the neural generators differ from data from our earlier studies, in which the same phonemes were assessed in an easy-to-discriminate context. The results demonstrate that the groups used different language processing strategies, depending on the success of language development and the particular language context. Overall, our data emphasize the role of neural plasticity and use of adaptive strategies for successful language development with cochlear implants

When Hearing Is Tricky: Speech Processing Strategies in Prelingually Deafened Children and Adolescents with Cochlear Implants Having Good and Poor Speech Performance

Cochlear implants provide individuals who are deaf with access to speech. Although substantial advancements have been made by novel technologies, there still is high variability in language development during childhood, depending on adaptation and neural plasticity. These factors have often been investigated in the auditory domain, with the mismatch negativity as an index for sensory and phonological processing. Several studies have demonstrated that the MMN is an electrophysiological correlate for hearing improvement with cochlear implants. In this study, two groups of cochlear implant users, both with very good basic hearing abilities but with non-overlapping speech performance (very good or very poor speech performance), were matched according to device experience and age at implantation. We tested the perception of phonemes in the context of specific other phonemes from which they were very hard to discriminate (e.g., the vowels in /bu/ vs. /bo/). The most difficult pair was individually determined for each articipant. Using behavioral measures, both cochlear implants groups performed worse than matched controls, and the good performers performed better than the poor performers. Cochlear implant groups and controls did not differ during time intervals typically used for the mismatch negativity, but earlier: source analyses revealed increased activity in the region of the right supramarginal gyrus (220±260 ms) in good performers. Poor performers showed increased activity in the left occipital cortex (220±290 ms), which may be an index for cross-modal perception. The time course and the neural generators differ from data from our earlier studies, in which the same phonemes were assessed in an easy-to-discriminate context. The results demonstrate that the groups used different language processing strategies, depending on the success of language development and the particular language context. Overall, our data emphasize the role of neural plasticity and use of adaptive strategies for successful language development with cochlear implants.</p

Neural Correlates of Speech Processing in Prelingually Deafened Children and Adolescents with Cochlear Implants

<div><p>Prelingually deafened children with cochlear implants stand a good chance of developing satisfactory speech performance. Nevertheless, their eventual language performance is highly variable and not fully explainable by the duration of deafness and hearing experience. In this study, two groups of cochlear implant users (CI groups) with very good basic hearing abilities but non-overlapping speech performance (very good or very bad speech performance) were matched according to hearing age and age at implantation. We assessed whether these CI groups differed with regard to their phoneme discrimination ability and auditory sensory memory capacity, as suggested by earlier studies. These functions were measured behaviorally and with the Mismatch Negativity (MMN). Phoneme discrimination ability was comparable in the CI group of good performers and matched healthy controls, which were both better than the bad performers. Source analyses revealed larger MMN activity (155–225 ms) in good than in bad performers, which was generated in the frontal cortex and positively correlated with measures of working memory. For the bad performers, this was followed by an increased activation of left temporal regions from 225 to 250 ms with a focus on the auditory cortex. These results indicate that the two CI groups developed different auditory speech processing strategies and stress the role of phonological functions of auditory sensory memory and the prefrontal cortex in positively developing speech perception and production.</p></div

Source localization for the difference waveforms of the good (A) and poor (B) performers across time.

<p>Visual impression that both groups differ regarding the activation of the right temporal and right supramarginal cortex (GP>BP) before the MMN begins and in the left occipital cortex (BP>GP) during and before the MMN is underlined by statistical analyses (C).</p

MMN Source Localization and Group Differences.

<p>Source localization of MMN in good performers (<b>4A</b>), bad performers (<b>4B</b>) and controls (<b>4C</b>): in both patient groups, the left frontal cortex was activated from 130 to 240 ms lc. In bad performers, the auditory cortex was additionally involved (218–260 ms lc). Healthy controls displayed bilateral activity in fronto-temporal regions from 120 to 210 ms lc. <b>4Di/ii:</b> Difference plots of the minimum norm estimates of good minus bad performers during the early (<b>Di</b>) and late (<b>Dii</b>) interval of the MMN. Grey discs indicate adjacent dipole locations within the two clusters (cluster 1: frontal; cluster 2: left temporal). While good performers showed significantly more activity in the frontal cortex from 155 to 225 ms lc (<b>Di</b>, indicated in red), this was followed by a stronger activation of the auditory cortex in the bad performers from 225 to 250 ms lc (<b>Dii</b>, indicated in blue). <b>Diii:</b> Correct source localization of the averaged CI artifact in the 16 patients who wore their CI on the right side.</p

Source localization for the significant group differences found before the MMN began.

<p>While good performers showed significantly higher activation from 220 to 260 ms in the right marginal cortex (A), poor performers activated their left occipital cortex more strongly from 220 to 280 ms. This allows the conclusion that both groups engaged different neural patterns for the processing of difficult-to-differentiate phoneme pairs. (C) Correct source localization of the averaged CI artifact in the 16 participants who wore their CI on the right side.</p

Correlation analyses.

<p>Activity in the occipital cluster during (A) and before (B) the MMN correlated negatively with phoneme discrimination ability in the difficult condition. The stronger CI users activated their left occipital cortex, the poorer their performance was in the phoneme discrimination test. In contrast to that, there was a trend for higher activity in the right supramarginal cluster being associated with more satisfaction regarding the CI user’s subjectively perceived language intelligibility.</p

MMN in source space.

<p>(A) global power plot for minimum norm estimates of the CI group, separately displayed for deviants, standards and their difference (MMN). The artifact is clearly visible in standards and deviants from 100 to 130 ms, but–as in sensor space–not in their difference waveform. (B) Global power plot of the difference waveform for all three groups and (C) averaged across both CI groups, with a focus on the MMN time window. (D/E) Topographic map of the MMN in the control group and (D) averaged for both CI groups (E). While the control group showed a bilateral MMN in temporal and supramarginal regions, CI users engaged not only auditory, but also frontal and occipital regions during MMN. (F) Poor performers showed (a trend) for significantly higher activity in the left occipital cortex during MMN.</p

Performance in the phoneme discrimination test displayed for each subtest and all groups.

<p>While good performers achieved d’ scores that were close to the typical hearing control group (3 out of 4 subtests), poor performers showed significantly worse phoneme discrimination abilities than the good performers (3 out of 4 subtests). As intended, this changed when phoneme pairs were sorted for each participant’s most difficult condition. Here, good performers performed significantly worse than the control group and better than the poor performers, who only achieved a guessing level. T-values ranged from 1.7 to 15.21 with p-values from 0.05 (marked by an asterisk) to ≤ 0.01 (marked by two or more asterisks).</p