Somatosensory Evoked Potentials Reveal Reduced Embodiment of Emotions in Autism.


Journal

The Journal of neuroscience : the official journal of the Society for Neuroscience
ISSN: 1529-2401
Titre abrégé: J Neurosci
Pays: United States
ID NLM: 8102140

Informations de publication

Date de publication:
16 03 2022
Historique:
received: 02 04 2021
revised: 03 01 2022
accepted: 05 01 2022
pubmed: 23 1 2022
medline: 22 4 2022
entrez: 22 1 2022
Statut: ppublish

Résumé

Consistent with current models of embodied emotions, this study investigates whether the somatosensory system shows reduced sensitivity to facial emotional expressions in autistic compared with neurotypical individuals, and whether these differences are independent from between-group differences in visual processing of facial stimuli. To investigate the dynamics of somatosensory activity over and above visual carryover effects, we recorded EEG activity from two groups of autism spectrum disorder (ASD) or typically developing (TD) humans (male and female), while they were performing a facial emotion discrimination task and a control gender task. To probe the state of the somatosensory system during face processing, in 50% of trials we evoked somatosensory activity by delivering task-irrelevant tactile taps on participants' index finger, 105 ms after visual stimulus onset. Importantly, we isolated somatosensory from concurrent visual activity by subtracting visual responses from activity evoked by somatosensory and visual stimuli. Results revealed significant task-dependent group differences in mid-latency components of somatosensory evoked potentials (SEPs). ASD participants showed a selective reduction of SEP amplitudes (P100) compared with TD during emotion task; and TD, but not ASD, showed increased somatosensory responses during emotion compared with gender discrimination. Interestingly, autistic traits, but not alexithymia, significantly predicted SEP amplitudes evoked during emotion, but not gender, task. Importantly, we did not observe the same pattern of group differences in visual responses. Our study provides direct evidence of reduced recruitment of the somatosensory system during emotion discrimination in ASD and suggests that this effect is not a byproduct of differences in visual processing.

Identifiants

pubmed: 35064001
pii: JNEUROSCI.0706-21.2022
doi: 10.1523/JNEUROSCI.0706-21.2022
pmc: PMC8936392
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2298-2312

Informations de copyright

Copyright © 2022 the authors.

Références

Autism. 2018 Feb;22(2):227-231
pubmed: 27811193
Psychophysiology. 1982 Mar;19(2):146-59
pubmed: 7071293
Int J Psychophysiol. 1994 Oct;18(1):49-65
pubmed: 7876038
Cereb Cortex. 2008 Nov;18(11):2686-700
pubmed: 18372293
Biol Psychiatry. 2019 Oct 1;86(7):557-567
pubmed: 31301757
Arch Gen Psychiatry. 2003 May;60(5):524-30
pubmed: 12742874
PLoS One. 2018 Dec 4;13(12):e0208034
pubmed: 30513087
Psychon Bull Rev. 2021 Jun;28(3):813-826
pubmed: 33037582
Hum Brain Mapp. 2016 Jan;37(1):351-65
pubmed: 26503033
Electroencephalogr Clin Neurophysiol. 1992 Jul-Aug;84(4):301-14
pubmed: 1377999
Neuroimage. 2019 Jul 15;195:140-149
pubmed: 30905836
Hum Brain Mapp. 2011 Jul;32(7):1013-28
pubmed: 20645311
Neuroimage. 1998 May;7(4 Pt 1):377-86
pubmed: 9626677
Neuropsychologia. 2005;43(6):957-66
pubmed: 15716166
Neuroimage. 2008 Feb 1;39(3):1104-20
pubmed: 17997111
Mol Autism. 2015 Jan 14;6:2
pubmed: 25874074
J Abnorm Psychol. 2018 Aug;127(6):612-622
pubmed: 30102067
Philos Trans R Soc Lond B Biol Sci. 2011 Jun 12;366(1571):1726-38
pubmed: 21536556
Electroencephalogr Clin Neurophysiol. 1996 Mar;100(2):126-40
pubmed: 8617151
J Autism Dev Disord. 2013 Jul;43(7):1517-26
pubmed: 23114566
J Neurosci. 2008 Sep 3;28(36):8929-33
pubmed: 18768686
Trends Cogn Sci. 2000 Jun;4(6):223-233
pubmed: 10827445
Dev Neuropsychol. 2005;27(3):403-24
pubmed: 15843104
Neuroimage. 2020 Nov 15;222:117251
pubmed: 32798682
Biol Psychiatry. 2009 Jan 1;65(1):55-62
pubmed: 18814863
J Neurosci. 2000 Apr 1;20(7):2683-90
pubmed: 10729349
Biol Psychiatry Cogn Neurosci Neuroimaging. 2018 Aug;3(8):657-666
pubmed: 30092916
Cortex. 2020 Aug;129:11-22
pubmed: 32422421
Behav Brain Res. 2013 Aug 15;251:155-62
pubmed: 23124137
Electroencephalogr Clin Neurophysiol. 1994 Sep;92(5):373-91
pubmed: 7523081
Psychophysiology. 2018 Jun;55(6):e13049
pubmed: 29266241
Insight J. 2006;2006:209
pubmed: 25364771
Front Integr Neurosci. 2012 Dec 04;6:113
pubmed: 23316143
Nat Rev Neurosci. 2010 Jun;11(6):417-28
pubmed: 20445542
Mol Autism. 2019 Nov 27;10:39
pubmed: 31798816
Psychol Methods. 2021 Jun;26(3):295-314
pubmed: 32673043
Nat Neurosci. 2006 Jan;9(1):28-30
pubmed: 16327784
Neuropsychologia. 2012 Jan;50(1):104-17
pubmed: 22100721
J Psychosom Res. 1994 Jan;38(1):23-32
pubmed: 8126686
Brain Res Cogn Brain Res. 2005 Jul;24(2):190-8
pubmed: 15993757
Cereb Cortex. 2007 Nov;17(11):2553-61
pubmed: 17205974
Neuroimage. 2018 Jul 1;174:153-163
pubmed: 29548846
Brain Commun. 2020 Jan 17;2(1):fcaa003
pubmed: 32954277
Neuropsychologia. 2018 Aug;117:75-83
pubmed: 29738793
Mol Autism. 2018 Jan 30;9:7
pubmed: 29423133
Psychophysiology. 2003 Jul;40(4):629-39
pubmed: 14570170
Psychophysiology. 2017 Jan;54(1):146-157
pubmed: 28000253
Neuropsychol Rev. 2010 Sep;20(3):290-322
pubmed: 20809200
Psychol Sci. 2013 May;24(5):723-32
pubmed: 23528789
Exp Brain Res. 2005 Aug;165(1):8-18
pubmed: 15883807
Front Hum Neurosci. 2012 Jun 15;6:175
pubmed: 22715325
Psychophysiology. 1980 Sep;17(5):499-503
pubmed: 7465719
Cortex. 2015 Apr;65:184-94
pubmed: 25835522
Dev Cogn Neurosci. 2013 Jan;3:91-105
pubmed: 23245224
Cognition. 2005 Jan;94(3):193-213
pubmed: 15617671
Neuroimage. 2010 Jan 1;49(1):1055-65
pubmed: 19647799
Schizophr Res. 2014 Sep;158(1-3):204-12
pubmed: 24998031
Cortex. 2020 Apr;125:332-344
pubmed: 32120169
Electroencephalogr Clin Neurophysiol. 1997 Jul;104(4):281-9
pubmed: 9246065
J Neurosci. 2014 Feb 26;34(9):3263-7
pubmed: 24573285
Brain Cogn. 2019 Dec;137:103616
pubmed: 31734588
Trends Cogn Sci. 2020 Jul;24(7):529-541
pubmed: 32430229
Science. 2007 May 18;316(5827):1002-5
pubmed: 17510358
J Neurosci. 2012 Mar 28;32(13):4531-9
pubmed: 22457500
Neuropsychologia. 2009 Jul;47(8-9):1816-25
pubmed: 19428413
Neurosci Biobehav Rev. 2017 Sep;80:488-515
pubmed: 28698082
Biol Psychiatry. 2005 Mar 15;57(6):655-60
pubmed: 15780853
Neuroimage. 2015 Sep;118:193-8
pubmed: 26080311
Psychophysiology. 1987 Jul;24(4):449-63
pubmed: 3615757
Methods Find Exp Clin Pharmacol. 2002;24 Suppl D:5-12
pubmed: 12575463
Electroencephalogr Clin Neurophysiol. 1984 Mar;57(3):254-63
pubmed: 6199186
J Neurosci. 1996 Dec 1;16(23):7678-87
pubmed: 8922424
J Autism Dev Disord. 2001 Feb;31(1):5-17
pubmed: 11439754
Neuroimage. 2005 Jun;26(2):581-91
pubmed: 15907315
Soc Neurosci. 2008;3(2):97-112
pubmed: 18633852
J Neurosci. 2012 Jan 18;32(3):799-805
pubmed: 22262878
Curr Opin Neurobiol. 2009 Dec;19(6):666-71
pubmed: 19880311
Electroencephalogr Clin Neurophysiol. 1983 Apr;55(4):468-84
pubmed: 6187540
J Autism Dev Disord. 2011 Jan;41(1):66-72
pubmed: 20422277
Biol Psychol. 2016 Feb;114:117-26
pubmed: 26724504
Transl Psychiatry. 2013 Jul 23;3:e285
pubmed: 23880881
Neuroimage. 2018 Feb 15;167:372-383
pubmed: 29203456
Eur J Neurosci. 2004 Dec;20(12):3507-15
pubmed: 15610183
Nat Rev Neurosci. 2005 Aug;6(8):641-51
pubmed: 16062171
Front Psychol. 2018 Jul 17;9:1196
pubmed: 30065681
Hum Brain Mapp. 2011 Jan;32(1):127-40
pubmed: 21157879
Nat Neurosci. 2020 Jul;23(7):788-799
pubmed: 32601411
Neuropsychologia. 2008 Apr;46(5):1558-65
pubmed: 18304590
Electroencephalogr Clin Neurophysiol. 1990 Feb;75(2):13-21
pubmed: 1688769
Biol Psychiatry. 2007 Aug 1;62(3):207-17
pubmed: 17400195
Electroencephalogr Clin Neurophysiol. 1989 Sep-Oct;74(5):321-46
pubmed: 2476292

Auteurs

Martina Fanghella (M)

Department of Psychology, City, University of London, London, EC1V 0HB, United Kingdom martina.fanghella@city.ac.uk.
Department of Psychology, University of Rome, La Sapienza, Rome, I-00185, Italy.
IRCCS, Fondazione Santa Lucia, Rome, I-00179, Italy.
Department of Philosophy, University of Milan, Milan, 20122, Italy.

Sebastian B Gaigg (SB)

Department of Psychology, City, University of London, London, EC1V 0HB, United Kingdom.

Matteo Candidi (M)

Department of Psychology, University of Rome, La Sapienza, Rome, I-00185, Italy.
IRCCS, Fondazione Santa Lucia, Rome, I-00179, Italy.

Bettina Forster (B)

Department of Psychology, City, University of London, London, EC1V 0HB, United Kingdom.

Beatriz Calvo-Merino (B)

Department of Psychology, City, University of London, London, EC1V 0HB, United Kingdom martina.fanghella@city.ac.uk.

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Classifications MeSH