Spoken language processing activates the primary visual cortex.
Journal
PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081
Informations de publication
Date de publication:
2023
2023
Historique:
received:
27
02
2023
accepted:
24
07
2023
medline:
14
8
2023
pubmed:
11
8
2023
entrez:
11
8
2023
Statut:
epublish
Résumé
Primary visual cortex (V1) is generally thought of as a low-level sensory area that primarily processes basic visual features. Although there is evidence for multisensory effects on its activity, these are typically found for the processing of simple sounds and their properties, for example spatially or temporally-congruent simple sounds. However, in congenitally blind individuals, V1 is involved in language processing, with no evidence of major changes in anatomical connectivity that could explain this seemingly drastic functional change. This is at odds with current accounts of neural plasticity, which emphasize the role of connectivity and conserved function in determining a neural tissue's role even after atypical early experiences. To reconcile what appears to be unprecedented functional reorganization with known accounts of plasticity limitations, we tested whether V1's multisensory roles include responses to spoken language in sighted individuals. Using fMRI, we found that V1 in normally sighted individuals was indeed activated by comprehensible spoken sentences as compared to an incomprehensible reversed speech control condition, and more strongly so in the left compared to the right hemisphere. Activation in V1 for language was also significant and comparable for abstract and concrete words, suggesting it was not driven by visual imagery. Last, this activation did not stem from increased attention to the auditory onset of words, nor was it correlated with attentional arousal ratings, making general attention accounts an unlikely explanation. Together these findings suggest that V1 responds to spoken language even in sighted individuals, reflecting the binding of multisensory high-level signals, potentially to predict visual input. This capability might be the basis for the strong V1 language activation observed in people born blind, re-affirming the notion that plasticity is guided by pre-existing connectivity and abilities in the typically developed brain.
Identifiants
pubmed: 37566582
doi: 10.1371/journal.pone.0289671
pii: PONE-D-23-05785
pmc: PMC10420367
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0289671Subventions
Organisme : NCATS NIH HHS
ID : TL1 TR001431
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD105735
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC001692
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD105328
Pays : United States
Informations de copyright
Copyright: © 2023 Seydell-Greenwald et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Cereb Cortex. 2019 Aug 14;29(9):3993-4005
pubmed: 30418533
Trends Cogn Sci. 2016 Apr;20(4):282-290
pubmed: 26944219
PLoS One. 2009;4(2):e4645
pubmed: 19247451
BMC Neurosci. 2013 Jul 23;14:74
pubmed: 23879896
Proc Natl Acad Sci U S A. 2018 Jul 24;115(30):7801-7806
pubmed: 29997174
Neuroreport. 1998 Jul 13;9(10):2409-13
pubmed: 9694237
Prog Brain Res. 2001;134:427-45
pubmed: 11702559
Science. 1999 Apr 2;284(5411):167-70
pubmed: 10102821
Trends Cogn Sci. 2006 Jun;10(6):278-85
pubmed: 16713325
Neuroimage. 2006 May 1;30(4):1414-32
pubmed: 16413796
Neuroimage. 2006 Oct 1;32(4):1826-36
pubmed: 16781167
Science. 1995 May 12;268(5212):889-93
pubmed: 7754376
Cereb Cortex. 2007 Jul;17(7):1672-9
pubmed: 16968869
PLoS Biol. 2020 Nov 6;18(11):e3000921
pubmed: 33156829
Brain Struct Funct. 2018 Apr;223(3):1165-1190
pubmed: 29094306
Curr Biol. 2015 Oct 19;25(20):2690-5
pubmed: 26441356
Cogn Affect Behav Neurosci. 2004 Jun;4(2):117-26
pubmed: 15460918
Cereb Cortex. 1991 Jan-Feb;1(1):1-47
pubmed: 1822724
Ann Neurol. 2014 Jan;75(1):33-42
pubmed: 24038442
Brain Lang. 2006 Aug;98(2):127-39
pubmed: 16716387
Trends Cogn Sci. 2015 Jul;19(7):374-82
pubmed: 26072689
Curr Biol. 2020 Aug 3;30(15):3039-3044.e2
pubmed: 32559449
Neuroimage. 2001 Apr;13(4):601-12
pubmed: 11305889
Proc Natl Acad Sci U S A. 2011 Mar 15;108(11):4429-34
pubmed: 21368161
J Cogn Neurosci. 2000 Nov;12(6):1013-23
pubmed: 11177421
Neuroimage. 2012 Feb 15;59(4):4064-73
pubmed: 22040738
J Neurophysiol. 2003 Sep;90(3):1965-82
pubmed: 12789013
Curr Opin Neurobiol. 2013 Apr;23(2):195-201
pubmed: 23402951
Cereb Cortex Commun. 2021 Jan 18;2(1):tgab002
pubmed: 33718874
Neurosci Biobehav Rev. 2014 Apr;41:64-77
pubmed: 24157726
Curr Biol. 2018 Nov 5;28(21):3435-3440.e4
pubmed: 30344121
Curr Biol. 2016 Feb 22;26(4):509-14
pubmed: 26853368
Biolinguistics (Nicos). 2017;11:407-422
pubmed: 30556058
J Neurosci. 2007 Jan 31;27(5):1090-6
pubmed: 17267563
Curr Biol. 2005 Jul 12;15(13):R488-90
pubmed: 16005276
Hear Res. 2021 Sep 1;408:108307
pubmed: 34311190
Brain Struct Funct. 2019 Apr;224(3):1167-1183
pubmed: 30637491
PLoS One. 2013 Nov 18;8(11):e80564
pubmed: 24260420
Hum Brain Mapp. 1997;5(6):422-36
pubmed: 20408245
Curr Biol. 2012 May 8;22(9):807-13
pubmed: 22503499
Neurology. 2002 Jul 23;59(2):238-44
pubmed: 12136064
Nature. 1994 Jun 16;369(6481):525
pubmed: 8031403
Curr Opin Psychol. 2019 Oct;29:193-198
pubmed: 31022562
Nat Neurosci. 2011 Dec 25;15(2):321-7
pubmed: 22197830
Brain Struct Funct. 2015 Mar;220(2):955-77
pubmed: 24384580
Annu Rev Neurosci. 2011;34:569-99
pubmed: 21692662
Behav Res Methods Instrum Comput. 2002 Aug;34(3):424-34
pubmed: 12395559
Neuroimage. 2010 Apr 1;50(2):818-25
pubmed: 20004247
Neuropsychologia. 2016 Mar;83:161-169
pubmed: 26275965
J Physiol. 1962 Jan;160:106-54
pubmed: 14449617
Brain. 2015 Jun;138(Pt 6):1679-95
pubmed: 25869851
Philos Trans R Soc Lond B Biol Sci. 2017 Feb 19;372(1714):
pubmed: 28044015
J Physiol. 1968 Mar;195(1):215-43
pubmed: 4966457
J Comp Neurol. 1998 Jul 13;396(4):493-510
pubmed: 9651007
Trends Cogn Sci. 2019 May;23(5):423-434
pubmed: 30876729
Annu Rev Neurosci. 2004;27:649-77
pubmed: 15217346
Neuroscience. 2006 Oct 27;142(3):843-58
pubmed: 16934941
Neuroimage. 1999 Jul;10(1):1-5
pubmed: 10385576
Ann N Y Acad Sci. 2018 Mar 31;:
pubmed: 29604082
J Neurophysiol. 2002 Jan;87(1):589-607
pubmed: 11784773
Curr Opin Neurobiol. 2005 Aug;15(4):454-8
pubmed: 16019202
Neuroscience. 2018 May 1;377:12-25
pubmed: 29408368
Cereb Cortex. 2007 Jun;17(6):1249-59
pubmed: 16861335
Brain. 2000 Jan;123 ( Pt 1):74-81
pubmed: 10611122
Neuropsychologia. 2010 Jun;48(7):2075-81
pubmed: 20363236
Neurology. 2007 Oct 30;69(18):1761-71
pubmed: 17967992
Cereb Cortex. 2012 Apr;22(4):754-64
pubmed: 21693783
Cortex. 2020 May;126:253-264
pubmed: 32092494
Cereb Cortex. 2015 Sep;25(9):2507-16
pubmed: 24642421
Neuroimage. 2013 Apr 15;70:258-67
pubmed: 23296187
Ann N Y Acad Sci. 2017 May;1396(1):92-107
pubmed: 28253445
Nat Commun. 2018 Dec 7;9(1):5250
pubmed: 30531889
Neuroreport. 2000 Feb 7;11(2):237-40
pubmed: 10674462
Neurosci Biobehav Rev. 2014 Apr;41:36-52
pubmed: 23954750
Brain. 1998 Jul;121 ( Pt 7):1213-29
pubmed: 9679774
Nat Neurosci. 2016 Sep;19(9):1250-5
pubmed: 27500407
Curr Opin Neurobiol. 2015 Dec;35:169-77
pubmed: 26469211
PLoS Comput Biol. 2009 Jul;5(7):e1000436
pubmed: 19609344
Proc Natl Acad Sci U S A. 2013 May 28;110(22):9136-41
pubmed: 23676276
Neuroimage. 2010 Aug 15;52(2):617-32
pubmed: 20412861
Cereb Cortex. 2020 Mar 21;30(2):597-606
pubmed: 31216008
Cereb Cortex. 1994 May-Jun;4(3):300-13
pubmed: 8075534
Trends Neurosci. 2019 Sep;42(9):589-603
pubmed: 31399289
J Neurosci. 2015 Sep 16;35(37):12859-68
pubmed: 26377472
Neuroimage. 2007 Jun;36(2):411-7
pubmed: 17442594
Brain. 2007 Aug;130(Pt 8):2085-96
pubmed: 17533167
Nat Neurosci. 2004 Nov;7(11):1266-70
pubmed: 15467719
Curr Biol. 2015 Jan 19;25(2):231-235
pubmed: 25544613
Nature. 1995 Nov 30;378(6556):496-8
pubmed: 7477406
Hum Brain Mapp. 2008 Jul;29(7):848-57
pubmed: 18412133
Brain Lang. 2012 Aug;122(2):114-9
pubmed: 22672735
J Neurosci. 2003 May 15;23(10):4005-11
pubmed: 12764085
Cereb Cortex. 2005 Oct;15(10):1570-83
pubmed: 15689519
Cereb Cortex. 2012 Feb;22(2):372-80
pubmed: 21666128
J Neurosci. 2002 Jul 1;22(13):5749-59
pubmed: 12097528
Brain. 2012 May;135(Pt 5):1566-77
pubmed: 22427328
Neuroimage. 2012 Aug 15;62(2):816-47
pubmed: 22584224
Eur J Neurosci. 2002 Sep;16(5):930-6
pubmed: 12372029
Nature. 1997 Sep 11;389(6647):180-3
pubmed: 9296495
Trends Cogn Sci. 2011 Mar;15(3):97-103
pubmed: 21317022
Vision Res. 2011 Apr 13;51(7):718-37
pubmed: 20692278
Cereb Cortex. 2019 Dec 17;29(11):4725-4742
pubmed: 30715236
J Cogn Neurosci. 2011 Mar;23(3):552-69
pubmed: 20350179
Proc Natl Acad Sci U S A. 2020 Sep 22;117(38):23477-23483
pubmed: 32900940
Nat Neurosci. 2004 Mar;7(3):295-301
pubmed: 14966525
Brain Res. 1991 Dec 13;567(1):133-9
pubmed: 1726139
Trends Cogn Sci. 2022 Feb;26(2):128-141
pubmed: 34973925
Brain Res Cogn Brain Res. 2002 Jun;14(1):20-30
pubmed: 12063127
Cereb Cortex. 2004 Apr;14(4):452-65
pubmed: 15028649
Neuroimage. 2019 Feb 1;186:549-556
pubmed: 30472373
Hum Brain Mapp. 2009 Jan;30(1):220-7
pubmed: 18072278
Psychol Bull. 2003 Sep;129(5):723-46
pubmed: 12956541
Nat Neurosci. 2003 Jul;6(7):758-66
pubmed: 12808458
Trends Cogn Sci. 2017 Sep;21(9):637-648
pubmed: 28821345
Curr Biol. 2014 Jun 2;24(11):1256-62
pubmed: 24856208
J Neurophysiol. 2002 Dec;88(6):3359-71
pubmed: 12466452
Neuroimage. 2013 Oct 1;79:19-29
pubmed: 23624493
Multisens Res. 2015;28(3-4):331-49
pubmed: 26288903
Front Neuroanat. 2011 Jun 22;5:35
pubmed: 21734867
Exp Brain Res. 2008 Oct;190(4):413-30
pubmed: 18641978
Neuropsychologia. 2000;38(11):1482-502
pubmed: 10906374
Neuropsychologia. 2007 Feb 1;45(3):531-9
pubmed: 16797610
Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11172-11177
pubmed: 27638209
J Cogn Neurosci. 2000;12 Suppl 2:15-23
pubmed: 11506644
Cortex. 2020 Jun;127:371-387
pubmed: 32289581
Hum Brain Mapp. 2008 May;29(5):533-43
pubmed: 17525980
Neuroimage. 2020 Apr 1;209:116509
pubmed: 31899288
Elife. 2019 May 23;8:
pubmed: 31115334
Neuron. 2014 Mar 19;81(6):1240-1253
pubmed: 24656248
Neuron. 2007 Oct 25;56(2):366-83
pubmed: 17964252
PLoS One. 2011 Mar 23;6(3):e17832
pubmed: 21448274
Brain Struct Funct. 2019 Jan;224(1):111-131
pubmed: 30288557
Neuroimage. 2001 Jul;14(1 Pt 2):S76-84
pubmed: 11373136
Hum Brain Mapp. 2003 Mar;18(3):176-85
pubmed: 12599275
J Neurophysiol. 2015 Nov;114(5):3023-8
pubmed: 26334017
Curr Biol. 2009 Nov 17;19(21):1799-805
pubmed: 19836243
Int J Psychophysiol. 2003 Oct;50(1-2):19-26
pubmed: 14511833
Hum Brain Mapp. 2014 Jun;35(6):2573-81
pubmed: 24038713
Annu Rev Neurosci. 2012;35:73-89
pubmed: 22524787
Cortex. 2013 Nov-Dec;49(10):2728-34
pubmed: 23419789
Front Syst Neurosci. 2014 Apr 07;8:51
pubmed: 24778608
Neuroreport. 1998 Nov 16;9(16):3669-74
pubmed: 9858377
Brain Imaging Behav. 2020 Oct;14(5):1908-1920
pubmed: 31183774
Cereb Cortex. 2006 Nov;16(11):1653-61
pubmed: 16400157