The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs
A cochlear implant (CI) is an auditory prosthesis which can partially restore the auditory function in patients with severe to profound hearing loss. However, this bionic device provides only limited auditory information, and CI patients may compensate for this limitation by means of a stronger inte...
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Elsevier
2022-01-01
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Series: | NeuroImage: Clinical |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S221315822200047X |
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author | Natalie Layer Anna Weglage Verena Müller Hartmut Meister Ruth Lang-Roth Martin Walger Micah M. Murray Pascale Sandmann |
author_facet | Natalie Layer Anna Weglage Verena Müller Hartmut Meister Ruth Lang-Roth Martin Walger Micah M. Murray Pascale Sandmann |
author_sort | Natalie Layer |
collection | DOAJ |
description | A cochlear implant (CI) is an auditory prosthesis which can partially restore the auditory function in patients with severe to profound hearing loss. However, this bionic device provides only limited auditory information, and CI patients may compensate for this limitation by means of a stronger interaction between the auditory and visual system. To better understand the electrophysiological correlates of audiovisual speech perception, the present study used electroencephalography (EEG) and a redundant target paradigm. Postlingually deafened CI users and normal-hearing (NH) listeners were compared in auditory, visual and audiovisual speech conditions. The behavioural results revealed multisensory integration for both groups, as indicated by shortened response times for the audiovisual as compared to the two unisensory conditions. The analysis of the N1 and P2 event-related potentials (ERPs), including topographic and source analyses, confirmed a multisensory effect for both groups and showed a cortical auditory response which was modulated by the simultaneous processing of the visual stimulus. Nevertheless, the CI users in particular revealed a distinct pattern of N1 topography, pointing to a strong visual impact on auditory speech processing. Apart from these condition effects, the results revealed ERP differences between CI users and NH listeners, not only in N1/P2 ERP topographies, but also in the cortical source configuration. When compared to the NH listeners, the CI users showed an additional activation in the visual cortex at N1 latency, which was positively correlated with CI experience, and a delayed auditory-cortex activation with a reversed, rightward functional lateralisation. In sum, our behavioural and ERP findings demonstrate a clear audiovisual benefit for both groups, and a CI-specific alteration in cortical activation at N1 latency when auditory and visual input is combined. These cortical alterations may reflect a compensatory strategy to overcome the limited CI input, which allows the CI users to improve the lip-reading skills and to approximate the behavioural performance of NH listeners in audiovisual speech conditions. Our results are clinically relevant, as they highlight the importance of assessing the CI outcome not only in auditory-only, but also in audiovisual speech conditions. |
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series | NeuroImage: Clinical |
spelling | doaj.art-294a1f5dbd214b7aae808eaf649d42d42022-12-22T03:35:14ZengElsevierNeuroImage: Clinical2213-15822022-01-0134102982The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPsNatalie Layer0Anna Weglage1Verena Müller2Hartmut Meister3Ruth Lang-Roth4Martin Walger5Micah M. Murray6Pascale Sandmann7University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany; Corresponding author.University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, GermanyUniversity of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, GermanyJean-Uhrmacher-Institute for Clinical ENT Research, University of Cologne, GermanyUniversity of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, GermanyUniversity of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany; Jean-Uhrmacher-Institute for Clinical ENT Research, University of Cologne, GermanyThe Sense Innovation and Research Center, Lausanne and Sion, Switzerland; The LINE (The Laboratory for Investigative Neurophysiology), Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland; CIBM Center for Biomedical Imaging of Lausanne and Geneva, Lausanne, Switzerland; Department of Hearing and Speech Sciences, Vanderbilt University, Nashville, TN, USAUniversity of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, GermanyA cochlear implant (CI) is an auditory prosthesis which can partially restore the auditory function in patients with severe to profound hearing loss. However, this bionic device provides only limited auditory information, and CI patients may compensate for this limitation by means of a stronger interaction between the auditory and visual system. To better understand the electrophysiological correlates of audiovisual speech perception, the present study used electroencephalography (EEG) and a redundant target paradigm. Postlingually deafened CI users and normal-hearing (NH) listeners were compared in auditory, visual and audiovisual speech conditions. The behavioural results revealed multisensory integration for both groups, as indicated by shortened response times for the audiovisual as compared to the two unisensory conditions. The analysis of the N1 and P2 event-related potentials (ERPs), including topographic and source analyses, confirmed a multisensory effect for both groups and showed a cortical auditory response which was modulated by the simultaneous processing of the visual stimulus. Nevertheless, the CI users in particular revealed a distinct pattern of N1 topography, pointing to a strong visual impact on auditory speech processing. Apart from these condition effects, the results revealed ERP differences between CI users and NH listeners, not only in N1/P2 ERP topographies, but also in the cortical source configuration. When compared to the NH listeners, the CI users showed an additional activation in the visual cortex at N1 latency, which was positively correlated with CI experience, and a delayed auditory-cortex activation with a reversed, rightward functional lateralisation. In sum, our behavioural and ERP findings demonstrate a clear audiovisual benefit for both groups, and a CI-specific alteration in cortical activation at N1 latency when auditory and visual input is combined. These cortical alterations may reflect a compensatory strategy to overcome the limited CI input, which allows the CI users to improve the lip-reading skills and to approximate the behavioural performance of NH listeners in audiovisual speech conditions. Our results are clinically relevant, as they highlight the importance of assessing the CI outcome not only in auditory-only, but also in audiovisual speech conditions.http://www.sciencedirect.com/science/article/pii/S221315822200047XCochlear implantEvent-related potentialCortical plasticityMultisensory integrationAudiovisual interactionAudiovisual speech perception |
spellingShingle | Natalie Layer Anna Weglage Verena Müller Hartmut Meister Ruth Lang-Roth Martin Walger Micah M. Murray Pascale Sandmann The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs NeuroImage: Clinical Cochlear implant Event-related potential Cortical plasticity Multisensory integration Audiovisual interaction Audiovisual speech perception |
title | The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs |
title_full | The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs |
title_fullStr | The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs |
title_full_unstemmed | The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs |
title_short | The timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by ERPs |
title_sort | timecourse of multisensory speech processing in unilaterally stimulated cochlear implant users revealed by erps |
topic | Cochlear implant Event-related potential Cortical plasticity Multisensory integration Audiovisual interaction Audiovisual speech perception |
url | http://www.sciencedirect.com/science/article/pii/S221315822200047X |
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