Electrophysiological differences and similarities in audiovisual speech processing in CI users with unilateral and bilateral hearing loss.

Audiovisual speech perception Bilateral hearing loss Cochlear implant Cortical plasticity Event-related potential Multisensory integration Single-sided-deafness

Journal

Current research in neurobiology
ISSN: 2665-945X
Titre abrégé: Curr Res Neurobiol
Pays: Netherlands
ID NLM: 101778135

Informations de publication

Date de publication:
2022
Historique:
received: 25 04 2022
revised: 24 08 2022
accepted: 07 10 2022
entrez: 21 11 2022
pubmed: 22 11 2022
medline: 22 11 2022
Statut: epublish

Résumé

Hearing with a cochlear implant (CI) is limited compared to natural hearing. Although CI users may develop compensatory strategies, it is currently unknown whether these extend from auditory to visual functions, and whether compensatory strategies vary between different CI user groups. To better understand the experience-dependent contributions to multisensory plasticity in audiovisual speech perception, the current event-related potential (ERP) study presented syllables in auditory, visual, and audiovisual conditions to CI users with unilateral or bilateral hearing loss, as well as to normal-hearing (NH) controls. Behavioural results revealed shorter audiovisual response times compared to unisensory conditions for all groups. Multisensory integration was confirmed by electrical neuroimaging, including topographic and ERP source analysis, showing a visual modulation of the auditory-cortex response at N1 and P2 latency. However, CI users with bilateral hearing loss showed a distinct pattern of N1 topography, indicating a stronger visual impact on auditory speech processing compared to CI users with unilateral hearing loss and NH listeners. Furthermore, both CI user groups showed a delayed auditory-cortex activation and an additional recruitment of the visual cortex, and a better lip-reading ability compared to NH listeners. In sum, these results extend previous findings by showing distinct multisensory processes not only between NH listeners and CI users in general, but even between CI users with unilateral and bilateral hearing loss. However, the comparably enhanced lip-reading ability and visual-cortex activation in both CI user groups suggest that these visual improvements are evident regardless of the hearing status of the contralateral ear.

Identifiants

pubmed: 36405629
doi: 10.1016/j.crneur.2022.100059
pii: S2665-945X(22)00032-8
pmc: PMC9672392
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100059

Informations de copyright

© 2022 The Authors.

Déclaration de conflit d'intérêts

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Références

J Neurosci. 2010 Sep 22;30(38):12572-80
pubmed: 20861363
Brain Topogr. 2022 Jul;35(4):431-452
pubmed: 35668310
Front Psychol. 2021 Oct 21;12:753339
pubmed: 34744930
Otol Neurotol. 2011 Jan;32(1):39-47
pubmed: 21068690
Hear Res. 2015 Oct;328:133-47
pubmed: 26302946
Brain. 2006 Dec;129(Pt 12):3376-83
pubmed: 17003067
Neuroimage. 2010 Oct 15;53(1):1-15
pubmed: 20547229
J Acoust Soc Am. 2016 Jun;139(6):3116
pubmed: 27369134
J Acoust Soc Am. 1990 Aug;88(2):745-53
pubmed: 2212299
Brain Res. 2008 Jan 10;1188:87-99
pubmed: 18062941
Trends Hear. 2019 Jan-Dec;23:2331216519858311
pubmed: 31364496
PLoS One. 2016 Jan 25;11(1):e0147793
pubmed: 26807850
Brain Res Cogn Brain Res. 2002 Jun;14(1):115-28
pubmed: 12063135
Eur J Neurosci. 2021 Aug;54(3):5016-5037
pubmed: 34146363
Clin Neurophysiol. 2010 Dec;121(12):2070-82
pubmed: 20570555
Cereb Cortex. 2007 Jul;17(7):1672-9
pubmed: 16968869
Exp Brain Res. 2004 Oct;158(4):405-14
pubmed: 15221173
Neural Comput. 1995 Nov;7(6):1129-59
pubmed: 7584893
Trans N Y Acad Sci. 1962 Mar;24:574-90
pubmed: 14489538
Ophthalmologe. 2010 Sep;107(9):821-6
pubmed: 20665033
Brain Topogr. 2014 Nov;27(6):707-30
pubmed: 24722880
Behav Res Methods. 2007 May;39(2):291-302
pubmed: 17695357
Comput Intell Neurosci. 2011;2011:879716
pubmed: 21584256
Eur J Neurosci. 2004 Oct;20(8):2225-34
pubmed: 15450102
Brain. 2009 Jul;132(Pt 7):1967-79
pubmed: 19293240
Brain Res Cogn Brain Res. 1993 Dec;1(4):227-40
pubmed: 8003922
Psychophysiology. 2000 Mar;37(2):163-78
pubmed: 10731767
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7295-300
pubmed: 17404220
Neuroimage Clin. 2017 Sep 04;16:514-523
pubmed: 28971005
Ear Hear. 2018 May/Jun;39(3):503-516
pubmed: 29068860
Neuroimage. 2014 Jul 1;94:172-184
pubmed: 24636881
Electroencephalogr Clin Neurophysiol. 1980 Jun;48(6):609-21
pubmed: 6155251
Ear Hear. 2002 Dec;23(6):532-9
pubmed: 12476090
Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):11793-9
pubmed: 11050211
Brain. 2001 Jul;124(Pt 7):1307-16
pubmed: 11408326
Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14608-13
pubmed: 16983092
Nat Neurosci. 2010 Nov;13(11):1421-7
pubmed: 20935644
Front Syst Neurosci. 2013 Oct 25;7:71
pubmed: 24478637
HNO. 2017 Jul;65(7):586-598
pubmed: 27995277
Audiology. 1987;26(1):31-43
pubmed: 3593099
Otol Neurotol. 2005 Jul;26(4):649-54
pubmed: 16015162
Neural Plast. 2016;2016:4382656
pubmed: 26819766
Curr Biol. 2019 Feb 4;29(3):R80-R85
pubmed: 30721678
Brain Res Cogn Brain Res. 2000 Sep;10(1-2):77-83
pubmed: 10978694
Ear Hear. 2011 Feb;32(1):53-60
pubmed: 20890206
Hear Res. 2005 Jul;205(1-2):184-92
pubmed: 15953527
Front Psychol. 2013 Oct 16;4:719
pubmed: 24137143
Psychophysiology. 1987 Jul;24(4):375-425
pubmed: 3615753
Neuroimage Clin. 2022;33:102942
pubmed: 35033811
Front Hum Neurosci. 2014 Jun 27;8:385
pubmed: 25018719
Am J Otol. 1995 Jul;16(4):514-20
pubmed: 8588653
Neuroimage Clin. 2022;34:102982
pubmed: 35303598
Cochlear Implants Int. 2021 Sep;22(5):283-290
pubmed: 33761831
Audiol Neurootol. 2014;19 Suppl 1:21-26
pubmed: 25733362
Electroencephalogr Clin Neurophysiol. 1989 Feb;72(2):184-7
pubmed: 2464490
Clin Neurophysiol. 2021 Sep;132(9):2290-2305
pubmed: 34120838
Brain. 2013 Dec;136(Pt 12):3682-95
pubmed: 24136826
Brain. 2012 Feb;135(Pt 2):555-68
pubmed: 22232592
Neuroimage. 2015 Nov 1;121:159-70
pubmed: 26220741
Hum Brain Mapp. 2014 Jul;35(7):3107-21
pubmed: 24123535
Ear Hear. 2016 May-Jun;37(3):289-302
pubmed: 26886027
Psychophysiology. 2008 Jan;45(1):20-4
pubmed: 17910729
Audiol Neurootol. 2001 Nov-Dec;6(6):381-93
pubmed: 11847465
Hear Res. 2012 Feb;284(1-2):6-15
pubmed: 22234161
Brain Topogr. 2014 May;27(3):412-24
pubmed: 24337445
Clin Neurophysiol. 2001 Oct;112(10):1850-9
pubmed: 11595143
Restor Neurol Neurosci. 2010;28(2):283-91
pubmed: 20404415
PLoS One. 2012;7(11):e48739
pubmed: 23152797
Psychon Bull Rev. 2016 Apr;23(2):640-7
pubmed: 26374437
Neuron. 2001 Jun;30(3):657-63
pubmed: 11430800
Comput Intell Neurosci. 2011;2011:813870
pubmed: 21253358
Hum Brain Mapp. 2017 Apr;38(4):2206-2225
pubmed: 28130910
Audiol Neurootol. 2015;20(3):183-8
pubmed: 25896774
Brain. 2013 Jan;136(Pt 1):180-93
pubmed: 23233722
Psychol Bull. 1979 May;86(3):446-61
pubmed: 451109
Biomed Eng Online. 2010 Sep 06;9:45
pubmed: 20819204
Cereb Cortex. 2010 May;20(5):1217-22
pubmed: 19805418
Cogn Psychol. 1982 Apr;14(2):247-79
pubmed: 7083803
Neuropsychologia. 2016 Jul 1;87:169-181
pubmed: 27212057
J Neurosci Methods. 2015 Jul 30;250:34-46
pubmed: 25128257
Hear Res. 2009 Feb;248(1-2):48-59
pubmed: 19110047
Neuroreport. 2003 Aug 6;14(11):1425-7
pubmed: 12960757
Neuropsychologia. 1971 Mar;9(1):97-113
pubmed: 5146491
Neuroimage. 2012 Jun;61(2):371-85
pubmed: 22227136
J Speech Lang Hear Res. 2004 Apr;47(2):304-20
pubmed: 15157132
Clin Neurophysiol. 2004 Apr;115(4):732-44
pubmed: 15003751
Neuroimage. 2020 Dec;223:117315
pubmed: 32882385
Nat Rev Neurosci. 2002 Jun;3(6):443-52
pubmed: 12042879
Front Neurosci. 2018 May 08;12:309
pubmed: 29867321
Cereb Cortex. 2004 Oct;14(10):1088-99
pubmed: 15115745
Clin Neurophysiol. 2015 Mar;126(3):594-607
pubmed: 25065298
Brain Res Cogn Brain Res. 2003 Feb;15(3):207-13
pubmed: 12527095
Audiol Neurootol. 2015;20 Suppl 1:79-86
pubmed: 25997991
Audiol Neurootol. 2016;21(5):305-315
pubmed: 27866186
Neuroimage. 2006 May 15;31(1):160-71
pubmed: 16520063
Clin Neurophysiol. 2018 Jan;129(1):133-142
pubmed: 29182915
J Rehabil Res Dev. 2008;45(5):779-89
pubmed: 18816426
Clin Neurophysiol. 2004 Oct;115(10):2195-222
pubmed: 15351361
Neuroimage. 2018 Oct 15;180(Pt B):577-593
pubmed: 29196270
Neuron. 2000 Apr;26(1):55-67
pubmed: 10798392
Brain Topogr. 2008 Jun;20(4):249-64
pubmed: 18347966
Otol Neurotol. 2010 Dec;31(9):1381-5
pubmed: 20729788
Cereb Cortex. 2005 Jul;15(7):963-74
pubmed: 15537674
Brain Res. 1995 Apr 24;678(1-2):177-90
pubmed: 7620886
Neuroscience. 2014 Dec 26;283:44-63
pubmed: 25139761
Hum Brain Mapp. 2012 Aug;33(8):1929-40
pubmed: 21557388
Ann N Y Acad Sci. 1982;388:125-38
pubmed: 6807171
Curr Opin Neurobiol. 2020 Feb;60:108-114
pubmed: 31864104
J Am Acad Audiol. 2005 Jan;16(1):42-53
pubmed: 15715067
J Neurosci Methods. 2004 Mar 15;134(1):9-21
pubmed: 15102499
Cereb Cortex. 2019 Dec 17;29(11):4530-4538
pubmed: 30590422

Auteurs

Natalie Layer (N)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany.

Anna Weglage (A)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany.

Verena Müller (V)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany.

Hartmut Meister (H)

Jean-Uhrmacher-Institute for Clinical ENT Research, University of Cologne, Germany.

Ruth Lang-Roth (R)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany.

Martin Walger (M)

University 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, Germany.

Micah M Murray (MM)

The 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, USA.

Pascale Sandmann (P)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Otorhinolaryngology, Head and Neck Surgery, Audiology and Pediatric Audiology, Cochlear Implant Center, Germany.

Classifications MeSH