Abstract

Cochlear implantation constitutes a successful therapy of inner ear deafness, with the majority of patients showing good outcomes. There is, however, still some unexplained variability in outcomes with a number of cochlear-implant (CI) users, showing major limitations in speech comprehension. The current study used a multimodal diagnostic approach combining single-photon emission computed tomography (SPECT) and electroencephalography (EEG) to examine the mechanisms underlying speech processing in postlingually deafened CI users (N = 21). In one session, the participants performed a speech discrimination task, during which a 96-channel EEG was recorded and the perfusions marker 99mTc-HMPAO was injected intravenously. The SPECT scan was acquired 1.5 h after injection to measure the cortical activity during the speech task. The second session included a SPECT scan after injection without stimulation at rest. Analysis of EEG and SPECT data showed N400 and P600 event-related potentials (ERPs) particularly evoked by semantic violations in the sentences, and enhanced perfusion in a temporo-frontal network during task compared to rest, involving the auditory cortex bilaterally and Broca’s area. Moreover, higher performance in testing for word recognition and verbal intelligence strongly correlated to the activation in this network during the speech task. However, comparing CI users with lower and higher speech intelligibility [median split with cutoff + 7.6 dB signal-to-noise ratio (SNR) in the Göttinger sentence test] revealed for CI users with higher performance additional activations of parietal and occipital regions and for those with lower performance stronger activation of superior frontal areas. Furthermore, SPECT activity was tightly coupled with EEG and cognitive abilities, as indicated by correlations between (1) cortical activation and the amplitudes in EEG, N400 (temporal and occipital areas)/P600 (parietal and occipital areas) and (2) between cortical activation in left-sided temporal and bilateral occipital/parietal areas and working memory capacity. These results suggest the recruitment of a temporo-frontal network in CI users during speech processing and a close connection between ERP effects and cortical activation in CI users. The observed differences in speech-evoked cortical activation patterns for CI users with higher and lower speech intelligibility suggest distinct processing strategies during speech rehabilitation with CI.

Highlights

  • Cochlear implantation is an established and effective method of treating sensorineural hearing loss (Wilson and Dorman, 2008a,b; Gaylor et al, 2013)

  • Our results suggest a close connection between event-related potentials (ERPs) effects and cortical activation in Cochlear implants (CIs) users and different activation patterns during speech processing between higher and lower performers, pointing to different neural resource allocation and strategies used for speech processing

  • On the descriptive level, our results showed that the amplitudes of the N1, P2, and N400 are reduced in the lower compared to the higher CI performers, while we observed on a descriptive level the opposite pattern, that is an enhanced amplitude, for the P600 in the lower compared to the higher performers

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Summary

Introduction

Cochlear implantation is an established and effective method of treating sensorineural hearing loss (Wilson and Dorman, 2008a,b; Gaylor et al, 2013). The N400, reflecting semantic memory use during language comprehension (Kutas and Federmeier, 2000), has been shown to be prolonged in adult CI users when compared with NH listeners (Hahne et al, 2012; Henkin et al, 2014), suggesting a delayed and a more effortful speech processing with the limited CI input (Finke et al, 2016a) It is currently unknown whether the N400 can distinguish between CI users who have good versus poor speech recognition, such a distinctiveness has been previously shown for other auditory ERPs (Soshi et al, 2014; Turgeon et al, 2014)

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