Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents
Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with...
Gespeichert in:
Veröffentlicht in: | Human brain mapping 2022-08, Vol.43 (12), p.3662-3679 |
---|---|
Hauptverfasser: | , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 3679 |
---|---|
container_issue | 12 |
container_start_page | 3662 |
container_title | Human brain mapping |
container_volume | 43 |
creator | Anderson, Carly A. Cushing, Sharon L. Papsin, Blake C. Gordon, Karen A. |
description | Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with 13 bilaterally profoundly deaf adolescents who received unilateral access to sound via a cochlear implant (CI) in their right ear in early childhood before receiving bilateral access to sound a decade later via a second CI in their left ear. Auditory‐evoked cortical responses to unilateral and bilateral stimulation were measured repeatedly using electroencephalogram from 1 week to 14 months after activation of their second CI. Early cortical responses from the newly implanted ear and bilateral stimulation were atypically lateralized to the left ipsilateral auditory cortex. Duration of unilateral deafness predicted an unexpectedly stronger representation of inputs from the newly implanted, compared to the first implanted ear, in left auditory cortex. Significant initial reductions in responses were observed, yet a left‐hemisphere bias and unequal weighting of inputs favoring the long‐term deaf ear did not converge to a balanced state observed in the binaurally developed system. Bilateral response enhancement was significantly reduced in left auditory cortex suggesting deficits in ipsilateral response inhibition of new, dominant, inputs during bilateral processing. These findings paradoxically demonstrate the adaptive capacity of the adolescent auditory system beyond an early sensitive period for bilateral input, as well as restrictions on its potential to fully reverse cortical imbalances driven by long‐term unilateral deafness.
Bilateral auditory processing deficits are pervasive and restrictive in deaf cochlear implant patients, but the cortical mechanisms remain poorly understood. This longitudinal electroencephalogram study identified a persistent cortical imbalance towards the long‐deprived ear driven by delayed restoration that disrupts bilateral integration mechanisms. |
doi_str_mv | 10.1002/hbm.25875 |
format | Article |
fullrecord | <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9294307</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A744297260</galeid><sourcerecordid>A744297260</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4405-c9c5a98cb2a95ebdc82e338afc37be288f7f6a7de9c1aecb618070b117d18b6f3</originalsourceid><addsrcrecordid>eNp1kkFv1DAQhSMEoqVw4A-gSFzgkK3txLF9QSoroEhFXODAybKd8a4rJy52ttX-eyZsqVoEysGR_c0bv-epqpeUrCgh7HRrxxXjUvBH1TElSjSEqvbx8t_zRnWCHlXPSrkkhFJO6NPqqOUdU0S2x9WPdcpzcCbWYbQmmslB7VOM6SZMm3qAaPYw1BnKnLKZQ5rq5GsbopkhY9EWTF7AMCFrfG2GFKE4mObyvHriTSzw4nY9qb5__PBtfd5cfP30eX120biuI7xxynGjpLPMKA52cJJB20rjXSssMCm98L0RAyhHDTjbU0kEsZSKgUrb-_akenfQvdrZEYalN95MX-UwmrzXyQT98GQKW71J11ox1bVEoMCbW4Gcfu7QqR4DWogYBqRd0azntJeYIkH09V_oZdrlCe0hpSjrMd971MZE0GHyCfu6RVSfiQ6TF6xfqNU_KPwGGINLE_iA-w8K3h4KXE6lZPB3HinRyxxonAP9ew6QfXU_lDvyz8MjcHoAbrDL_v9K-vz9l4PkLwm7vQ4</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2691261500</pqid></control><display><type>article</type><title>Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents</title><source>Wiley Online Library Open Access</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Wiley Online Library All Journals</source><source>PubMed Central</source><creator>Anderson, Carly A. ; Cushing, Sharon L. ; Papsin, Blake C. ; Gordon, Karen A.</creator><creatorcontrib>Anderson, Carly A. ; Cushing, Sharon L. ; Papsin, Blake C. ; Gordon, Karen A.</creatorcontrib><description>Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with 13 bilaterally profoundly deaf adolescents who received unilateral access to sound via a cochlear implant (CI) in their right ear in early childhood before receiving bilateral access to sound a decade later via a second CI in their left ear. Auditory‐evoked cortical responses to unilateral and bilateral stimulation were measured repeatedly using electroencephalogram from 1 week to 14 months after activation of their second CI. Early cortical responses from the newly implanted ear and bilateral stimulation were atypically lateralized to the left ipsilateral auditory cortex. Duration of unilateral deafness predicted an unexpectedly stronger representation of inputs from the newly implanted, compared to the first implanted ear, in left auditory cortex. Significant initial reductions in responses were observed, yet a left‐hemisphere bias and unequal weighting of inputs favoring the long‐term deaf ear did not converge to a balanced state observed in the binaurally developed system. Bilateral response enhancement was significantly reduced in left auditory cortex suggesting deficits in ipsilateral response inhibition of new, dominant, inputs during bilateral processing. These findings paradoxically demonstrate the adaptive capacity of the adolescent auditory system beyond an early sensitive period for bilateral input, as well as restrictions on its potential to fully reverse cortical imbalances driven by long‐term unilateral deafness.
Bilateral auditory processing deficits are pervasive and restrictive in deaf cochlear implant patients, but the cortical mechanisms remain poorly understood. This longitudinal electroencephalogram study identified a persistent cortical imbalance towards the long‐deprived ear driven by delayed restoration that disrupts bilateral integration mechanisms.</description><identifier>ISSN: 1065-9471</identifier><identifier>EISSN: 1097-0193</identifier><identifier>DOI: 10.1002/hbm.25875</identifier><identifier>PMID: 35429083</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adolescents ; Auditory deprivation ; auditory development ; Auditory system ; bilateral processing ; binaural ; Child development ; Children ; Cochlea ; Cochlear implants ; Cortex (auditory) ; cortical plasticity ; Critical period ; Deafness ; Deprivation ; Ear ; Ears & hearing ; EEG ; electroencephalography ; Hearing loss ; hemispheric asymmetry ; Hemispheric laterality ; Implants, Artificial ; longitudinal ; pediatric ; Prosthesis ; Sensory stimulation ; sequential cochlear implantation ; Sound ; Teenagers ; Transplants & implants ; Youth</subject><ispartof>Human brain mapping, 2022-08, Vol.43 (12), p.3662-3679</ispartof><rights>2022 The Authors. published by Wiley Periodicals LLC.</rights><rights>2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.</rights><rights>COPYRIGHT 2022 John Wiley & Sons, Inc.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4405-c9c5a98cb2a95ebdc82e338afc37be288f7f6a7de9c1aecb618070b117d18b6f3</citedby><cites>FETCH-LOGICAL-c4405-c9c5a98cb2a95ebdc82e338afc37be288f7f6a7de9c1aecb618070b117d18b6f3</cites><orcidid>0000-0002-2491-3125 ; 0000-0003-1704-3026 ; 0000-0003-0928-4145 ; 0000-0001-9226-4510</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9294307/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9294307/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11541,27901,27902,45550,45551,46027,46451,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35429083$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Anderson, Carly A.</creatorcontrib><creatorcontrib>Cushing, Sharon L.</creatorcontrib><creatorcontrib>Papsin, Blake C.</creatorcontrib><creatorcontrib>Gordon, Karen A.</creatorcontrib><title>Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents</title><title>Human brain mapping</title><addtitle>Hum Brain Mapp</addtitle><description>Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with 13 bilaterally profoundly deaf adolescents who received unilateral access to sound via a cochlear implant (CI) in their right ear in early childhood before receiving bilateral access to sound a decade later via a second CI in their left ear. Auditory‐evoked cortical responses to unilateral and bilateral stimulation were measured repeatedly using electroencephalogram from 1 week to 14 months after activation of their second CI. Early cortical responses from the newly implanted ear and bilateral stimulation were atypically lateralized to the left ipsilateral auditory cortex. Duration of unilateral deafness predicted an unexpectedly stronger representation of inputs from the newly implanted, compared to the first implanted ear, in left auditory cortex. Significant initial reductions in responses were observed, yet a left‐hemisphere bias and unequal weighting of inputs favoring the long‐term deaf ear did not converge to a balanced state observed in the binaurally developed system. Bilateral response enhancement was significantly reduced in left auditory cortex suggesting deficits in ipsilateral response inhibition of new, dominant, inputs during bilateral processing. These findings paradoxically demonstrate the adaptive capacity of the adolescent auditory system beyond an early sensitive period for bilateral input, as well as restrictions on its potential to fully reverse cortical imbalances driven by long‐term unilateral deafness.
Bilateral auditory processing deficits are pervasive and restrictive in deaf cochlear implant patients, but the cortical mechanisms remain poorly understood. This longitudinal electroencephalogram study identified a persistent cortical imbalance towards the long‐deprived ear driven by delayed restoration that disrupts bilateral integration mechanisms.</description><subject>Adolescents</subject><subject>Auditory deprivation</subject><subject>auditory development</subject><subject>Auditory system</subject><subject>bilateral processing</subject><subject>binaural</subject><subject>Child development</subject><subject>Children</subject><subject>Cochlea</subject><subject>Cochlear implants</subject><subject>Cortex (auditory)</subject><subject>cortical plasticity</subject><subject>Critical period</subject><subject>Deafness</subject><subject>Deprivation</subject><subject>Ear</subject><subject>Ears & hearing</subject><subject>EEG</subject><subject>electroencephalography</subject><subject>Hearing loss</subject><subject>hemispheric asymmetry</subject><subject>Hemispheric laterality</subject><subject>Implants, Artificial</subject><subject>longitudinal</subject><subject>pediatric</subject><subject>Prosthesis</subject><subject>Sensory stimulation</subject><subject>sequential cochlear implantation</subject><subject>Sound</subject><subject>Teenagers</subject><subject>Transplants & implants</subject><subject>Youth</subject><issn>1065-9471</issn><issn>1097-0193</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kkFv1DAQhSMEoqVw4A-gSFzgkK3txLF9QSoroEhFXODAybKd8a4rJy52ttX-eyZsqVoEysGR_c0bv-epqpeUrCgh7HRrxxXjUvBH1TElSjSEqvbx8t_zRnWCHlXPSrkkhFJO6NPqqOUdU0S2x9WPdcpzcCbWYbQmmslB7VOM6SZMm3qAaPYw1BnKnLKZQ5rq5GsbopkhY9EWTF7AMCFrfG2GFKE4mObyvHriTSzw4nY9qb5__PBtfd5cfP30eX120biuI7xxynGjpLPMKA52cJJB20rjXSssMCm98L0RAyhHDTjbU0kEsZSKgUrb-_akenfQvdrZEYalN95MX-UwmrzXyQT98GQKW71J11ox1bVEoMCbW4Gcfu7QqR4DWogYBqRd0azntJeYIkH09V_oZdrlCe0hpSjrMd971MZE0GHyCfu6RVSfiQ6TF6xfqNU_KPwGGINLE_iA-w8K3h4KXE6lZPB3HinRyxxonAP9ew6QfXU_lDvyz8MjcHoAbrDL_v9K-vz9l4PkLwm7vQ4</recordid><startdate>20220815</startdate><enddate>20220815</enddate><creator>Anderson, Carly A.</creator><creator>Cushing, Sharon L.</creator><creator>Papsin, Blake C.</creator><creator>Gordon, Karen A.</creator><general>John Wiley & Sons, Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2491-3125</orcidid><orcidid>https://orcid.org/0000-0003-1704-3026</orcidid><orcidid>https://orcid.org/0000-0003-0928-4145</orcidid><orcidid>https://orcid.org/0000-0001-9226-4510</orcidid></search><sort><creationdate>20220815</creationdate><title>Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents</title><author>Anderson, Carly A. ; Cushing, Sharon L. ; Papsin, Blake C. ; Gordon, Karen A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4405-c9c5a98cb2a95ebdc82e338afc37be288f7f6a7de9c1aecb618070b117d18b6f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adolescents</topic><topic>Auditory deprivation</topic><topic>auditory development</topic><topic>Auditory system</topic><topic>bilateral processing</topic><topic>binaural</topic><topic>Child development</topic><topic>Children</topic><topic>Cochlea</topic><topic>Cochlear implants</topic><topic>Cortex (auditory)</topic><topic>cortical plasticity</topic><topic>Critical period</topic><topic>Deafness</topic><topic>Deprivation</topic><topic>Ear</topic><topic>Ears & hearing</topic><topic>EEG</topic><topic>electroencephalography</topic><topic>Hearing loss</topic><topic>hemispheric asymmetry</topic><topic>Hemispheric laterality</topic><topic>Implants, Artificial</topic><topic>longitudinal</topic><topic>pediatric</topic><topic>Prosthesis</topic><topic>Sensory stimulation</topic><topic>sequential cochlear implantation</topic><topic>Sound</topic><topic>Teenagers</topic><topic>Transplants & implants</topic><topic>Youth</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Anderson, Carly A.</creatorcontrib><creatorcontrib>Cushing, Sharon L.</creatorcontrib><creatorcontrib>Papsin, Blake C.</creatorcontrib><creatorcontrib>Gordon, Karen A.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human brain mapping</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Anderson, Carly A.</au><au>Cushing, Sharon L.</au><au>Papsin, Blake C.</au><au>Gordon, Karen A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents</atitle><jtitle>Human brain mapping</jtitle><addtitle>Hum Brain Mapp</addtitle><date>2022-08-15</date><risdate>2022</risdate><volume>43</volume><issue>12</issue><spage>3662</spage><epage>3679</epage><pages>3662-3679</pages><issn>1065-9471</issn><eissn>1097-0193</eissn><abstract>Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with 13 bilaterally profoundly deaf adolescents who received unilateral access to sound via a cochlear implant (CI) in their right ear in early childhood before receiving bilateral access to sound a decade later via a second CI in their left ear. Auditory‐evoked cortical responses to unilateral and bilateral stimulation were measured repeatedly using electroencephalogram from 1 week to 14 months after activation of their second CI. Early cortical responses from the newly implanted ear and bilateral stimulation were atypically lateralized to the left ipsilateral auditory cortex. Duration of unilateral deafness predicted an unexpectedly stronger representation of inputs from the newly implanted, compared to the first implanted ear, in left auditory cortex. Significant initial reductions in responses were observed, yet a left‐hemisphere bias and unequal weighting of inputs favoring the long‐term deaf ear did not converge to a balanced state observed in the binaurally developed system. Bilateral response enhancement was significantly reduced in left auditory cortex suggesting deficits in ipsilateral response inhibition of new, dominant, inputs during bilateral processing. These findings paradoxically demonstrate the adaptive capacity of the adolescent auditory system beyond an early sensitive period for bilateral input, as well as restrictions on its potential to fully reverse cortical imbalances driven by long‐term unilateral deafness.
Bilateral auditory processing deficits are pervasive and restrictive in deaf cochlear implant patients, but the cortical mechanisms remain poorly understood. This longitudinal electroencephalogram study identified a persistent cortical imbalance towards the long‐deprived ear driven by delayed restoration that disrupts bilateral integration mechanisms.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>35429083</pmid><doi>10.1002/hbm.25875</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-2491-3125</orcidid><orcidid>https://orcid.org/0000-0003-1704-3026</orcidid><orcidid>https://orcid.org/0000-0003-0928-4145</orcidid><orcidid>https://orcid.org/0000-0001-9226-4510</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1065-9471 |
ispartof | Human brain mapping, 2022-08, Vol.43 (12), p.3662-3679 |
issn | 1065-9471 1097-0193 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9294307 |
source | Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Online Library All Journals; PubMed Central |
subjects | Adolescents Auditory deprivation auditory development Auditory system bilateral processing binaural Child development Children Cochlea Cochlear implants Cortex (auditory) cortical plasticity Critical period Deafness Deprivation Ear Ears & hearing EEG electroencephalography Hearing loss hemispheric asymmetry Hemispheric laterality Implants, Artificial longitudinal pediatric Prosthesis Sensory stimulation sequential cochlear implantation Sound Teenagers Transplants & implants Youth |
title | Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T19%3A59%3A24IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Cortical%20imbalance%20following%20delayed%20restoration%20of%20bilateral%20hearing%20in%20deaf%20adolescents&rft.jtitle=Human%20brain%20mapping&rft.au=Anderson,%20Carly%20A.&rft.date=2022-08-15&rft.volume=43&rft.issue=12&rft.spage=3662&rft.epage=3679&rft.pages=3662-3679&rft.issn=1065-9471&rft.eissn=1097-0193&rft_id=info:doi/10.1002/hbm.25875&rft_dat=%3Cgale_pubme%3EA744297260%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2691261500&rft_id=info:pmid/35429083&rft_galeid=A744297260&rfr_iscdi=true |