Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users

Sandmann, Pascale; Dillier, Norbert; Eichele, Tom; Meyer, Martin; Kegel, Andrea; Pascual-Marqui, Roberto D.; Marcar, Valentine L.; Jäncke, Lutz; Debener, Stefan

doi:10.1093/brain/awr329

Cited by 205 publications

(224 citation statements)

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“…It has been assumed that visual language may compromise the ability of auditory brain regions to respond to sound after implantation (3,16) and that maladaptive cross-modal plasticity must be reversed for CI success (4). To explore the mechanisms underlying hearing restoration, we examined whether an increase in responsiveness of auditory brain regions to auditory speech stimulation after implantation was dependent on a decrease in cross-modal activation to visual speech.…”

Section: Resultsmentioning

confidence: 99%

“…This cross-modal plasticity within auditory cortex can provide adaptive benefits such as superior visual localization and motion detection abilities (2). On the other hand, cross-modal plasticity can limit a deaf individual's ability to understand speech after their hearing is restored with a cochlear implant (3,4). Therefore, it is assumed that this maladaptive cross-modal activation of auditory brain regions must decrease following cochlear implantation for speech understanding to be restored successfully (4).…”

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confidence: 99%

“…On the other hand, cross-modal plasticity can limit a deaf individual's ability to understand speech after their hearing is restored with a cochlear implant (3,4). Therefore, it is assumed that this maladaptive cross-modal activation of auditory brain regions must decrease following cochlear implantation for speech understanding to be restored successfully (4). However, in recent years, this traditional dichotomous stance on the adaptive effects of cross-modal plasticity during sensory deprivation versus its maladaptive effects during sensory restoration has been highlighted as too simplistic (5).…”

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confidence: 99%

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Adaptive benefit of cross-modal plasticity following cochlear implantation in deaf adults

Anderson

Wiggins

Kitterick

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

118

134

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It has been suggested that visual language is maladaptive for hearing restoration with a cochlear implant (CI) due to cross-modal recruitment of auditory brain regions. Rehabilitative guidelines therefore discourage the use of visual language. However, neuroscientific understanding of cross-modal plasticity following cochlear implantation has been restricted due to incompatibility between established neuroimaging techniques and the surgically implanted electronic and magnetic components of the CI. As a solution to this problem, here we used functional near-infrared spectroscopy (fNIRS), a noninvasive optical neuroimaging method that is fully compatible with a CI and safe for repeated testing. The aim of this study was to examine cross-modal activation of auditory brain regions by visual speech from before to after implantation and its relation to CI success. Using fNIRS, we examined activation of superior temporal cortex to visual speech in the same profoundly deaf adults both before and 6 mo after implantation. Patients' ability to understand auditory speech with their CI was also measured following 6 mo of CI use. Contrary to existing theory, the results demonstrate that increased cross-modal activation of auditory brain regions by visual speech from before to after implantation is associated with better speech understanding with a CI. Furthermore, activation of auditory cortex by visual and auditory speech developed in synchrony after implantation. Together these findings suggest that cross-modal plasticity by visual speech does not exert previously assumed maladaptive effects on CI success, but instead provides adaptive benefits to the restoration of hearing after implantation through an audiovisual mechanism. cochlear implantation | cross-modal plasticity | functional near-infrared spectroscopy | superior temporal cortex | visual speech

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Adaptive benefit of cross-modal plasticity following cochlear implantation in deaf adults

Anderson

Wiggins

Kitterick

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

118

134

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“…However, in noisy surroundings, the speech understanding typically decreases remarkably in CI users (Hochmair-Desoyer et al, 1997;Wilson and Dorman, 2008;Zeng et al, 2011). In general, there is a high variability in speech recognition ability across CI users which is likely caused by factors related to the implant, the auditory nerve, and the reorganization of the central auditory system (Drennan and Rubinstein, 2008;Nadol et al, 1989;Sandmann et al, 2012Sandmann et al, , 3 2015. In particular, electrical hearing may require additional explicit processing due to a mismatch between the attributes of the current CI input and the attributes stored in the longterm memory (Finke et al, 2015;Rönnberg et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

On the relationship between auditory cognition and speech intelligibility in cochlear implant users: An ERP study

et al. 2016

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There is a high degree of variability in speech intelligibility outcomes across cochlear-implant (CI) users. To better understand how auditory cognition affects speech intelligibility with the CI, we performed an electroencephalography study in which we examined the relationship between central auditory processing, cognitive abilities, and speech intelligibility. Postlingually deafened CI users (N=13) and matched normal-hearing (NH) listeners (N=13) performed an oddball task with words presented in different background conditions (quiet, stationary noise, modulated noise). Participants had to categorize words as living (targets) or non-living entities (standards). We also assessed participants' working memory (WM) capacity and verbal abilities. For the oddball task, we found lower hit rates and prolonged response times in CI users when compared with NH listeners. Noise-related prolongation of the N1 amplitude was found for all participants. Further, we observed group-specific modulation effects of event-related potentials (ERPs) as a function of background noise. While NH listeners showed stronger noise-related modulation of the N1 latency, CI users revealed enhanced modulation effects of the N2/N4 latency. In general, higher-order processing (N2/N4, P3) was prolonged in CI users in all background conditions when compared with NH listeners. Longer N2/N4 latency in CI users suggests that these individuals have difficulties to map acoustic-phonetic features to lexical representations. These difficulties seem to be increased for speech-in-noise conditions when compared with speech in quiet background. Correlation analyses showed that shorter ERP latencies were related to enhanced speech intelligibility (N1, N2/N4), better lexical fluency (N1), and lower ratings of listening effort (N2/N4) in CI users. In sum, our findings suggest that CI users and NH listeners differ with regards to both the sensory and the higher-order processing of speech in quiet as well as in noisy background conditions. Our results also revealed that verbal abilities are related to speech processing and speech intelligibility in CI users, confirming the view that auditory cognition plays an important role for CI outcome. We conclude that differences in auditory-cognitive processing contribute to the variability in speech performance outcomes observed in CI users. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Hannover, Finke.Mareike@mh-hannover.de AbstractThere is a high degree of variability in speech intelligibility outcomes across cochlear-implant (CI) users. To better understand how auditory cognition aff...

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“…It has been postulated that greater dependency on the visual function performed by the occipito-temporal region due to auditory deprivation may interfere with the acquisition of auditory language [5] . Similarly, Sandmann et al [28] reported a visual takeover type of reorganization in the auditory cortex of cochlear implant users and that the extent of this cross-modal reorganization was systematically related to speech recognition ability with a cochlear implant. In other words, visual processing dominance was inversely related to speech recognition ability with a cochlear implant.…”

Section: Discussionmentioning

confidence: 88%

Factors Contributing to Speech Performance in Elderly Cochlear Implanted Patients: An FDG-PET Study: A Preliminary Study

et al. 2015

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OBJECTIVE:The purpose was to evaluate brain plasticity that contributes to speech performance after cochlear implantation (CI) in postlingual elderly (>60 years) patients. MATERIALS and METHODS:Fifteen elderly postlingual deaf patients who underwent preoperative brain fluorodeoxyglucose positron emission tomography (FDG-PET) and were followed-up for more than 1 year after CI were included. The mean age of these patients was 64.6 years (range, 60-80 years). Based on their sentence score at 1 year after CI surgery, the patients were classified into two groups: poor performers (CID score of <80) and good performers (CID score of ≥80). The duration of deafness, age at operation, preoperative residual hearing, and preoperative brain metabolism were analyzed. SPM5 software was used for FDG-PET image preprocessing and statistical analysis. RESULTS:Neither deafness duration nor preoperative residual hearing was associated with speech performance. The age at operation had little association with speech performance. Deaf patients whose brain metabolism was higher in frontotemporal regions became good CI users but those with higher metabolism in visual association areas became poor CI users. No significant cortical area of higher metabolism was associated with the duration of deafness. CONCLUSION:Overactivation in the visual processing pathway correlated with a poor CI outcome at 1 year. Deaf patients who are going to be poorer performers with CI devices maintain visual information processing during preoperative silent resting periods.

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Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users

Cited by 205 publications

References 88 publications

Adaptive benefit of cross-modal plasticity following cochlear implantation in deaf adults

Adaptive benefit of cross-modal plasticity following cochlear implantation in deaf adults

On the relationship between auditory cognition and speech intelligibility in cochlear implant users: An ERP study

Factors Contributing to Speech Performance in Elderly Cochlear Implanted Patients: An FDG-PET Study: A Preliminary Study

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