Temporal-spectral signaling of sensory information and expectations in the cerebral processing of pain.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
04 01 2022
Historique:
accepted: 22 11 2021
entrez: 5 1 2022
pubmed: 6 1 2022
medline: 5 3 2022
Statut: ppublish

Résumé

The perception of pain is shaped by somatosensory information about threat. However, pain is also influenced by an individual's expectations. Such expectations can result in clinically relevant modulations and abnormalities of pain. In the brain, sensory information, expectations (predictions), and discrepancies thereof (prediction errors) are signaled by an extended network of brain areas which generate evoked potentials and oscillatory responses at different latencies and frequencies. However, a comprehensive picture of how evoked and oscillatory brain responses signal sensory information, predictions, and prediction errors in the processing of pain is lacking so far. Here, we therefore applied brief painful stimuli to 48 healthy human participants and independently modulated sensory information (stimulus intensity) and expectations of pain intensity while measuring brain activity using electroencephalography (EEG). Pain ratings confirmed that pain intensity was shaped by both sensory information and expectations. In contrast, Bayesian analyses revealed that stimulus-induced EEG responses at different latencies (the N1, N2, and P2 components) and frequencies (alpha, beta, and gamma oscillations) were shaped by sensory information but not by expectations. Expectations, however, shaped alpha and beta oscillations before the painful stimuli. These findings indicate that commonly analyzed EEG responses to painful stimuli are more involved in signaling sensory information than in signaling expectations or mismatches of sensory information and expectations. Moreover, they indicate that the effects of expectations on pain are served by brain mechanisms which differ from those conveying effects of sensory information on pain.

Identifiants

pubmed: 34983852
pii: 2116616119
doi: 10.1073/pnas.2116616119
pmc: PMC8740684
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2021 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

Références

Cereb Cortex. 2006 Apr;16(4):537-40
pubmed: 16033927
Lancet. 2010 Feb 20;375(9715):686-95
pubmed: 20171404
Neuron. 2012 Nov 21;76(4):695-711
pubmed: 23177956
Multivariate Behav Res. 2012 Nov;47(6):877-903
pubmed: 26735007
Brain Res. 2010 Nov 4;1359:137-41
pubmed: 20735999
J Neurosci. 2020 Jan 8;40(2):382-394
pubmed: 31694965
Elife. 2016 Mar 07;5:e11476
pubmed: 26949254
J Neurophysiol. 2008 Aug;100(2):815-28
pubmed: 18525021
Neurosci Lett. 2012 Jun 29;520(2):140-8
pubmed: 22465136
Int J Psychophysiol. 2012 Feb;83(2):120-31
pubmed: 21867734
Neuron. 2016 Jan 20;89(2):384-97
pubmed: 26777277
Wellcome Open Res. 2019 Apr 1;4:63
pubmed: 31069261
PLoS Comput Biol. 2017 Jan 12;13(1):e1005142
pubmed: 28081134
Nat Rev Neurosci. 2013 May;14(5):365-76
pubmed: 23571845
Pain. 2019 Jan;160(1):1-4
pubmed: 30086114
Prog Neurobiol. 2011 Jan;93(1):111-24
pubmed: 21040755
Trends Cogn Sci. 2014 May;18(5):235-41
pubmed: 24656991
Psychophysiology. 2000 Mar;37(2):163-78
pubmed: 10731767
Front Psychol. 2016 Aug 23;7:1270
pubmed: 27602013
Neuroimage. 2010 Mar;50(1):99-111
pubmed: 20004255
Neurophysiol Clin. 2003 Dec;33(6):269-77
pubmed: 14678841
Neuroreport. 1997 Dec 1;8(17):3785-9
pubmed: 9427371
J Neurosci. 2018 Jul 18;38(29):6461-6474
pubmed: 29934355
Nat Commun. 2019 Sep 10;10(1):4096
pubmed: 31506426
Trends Cogn Sci. 2012 Jul;16(7):390-8
pubmed: 22682813
Comput Intell Neurosci. 2011;2011:156869
pubmed: 21253357
J Neurosci. 2010 Dec 8;30(49):16601-8
pubmed: 21147999
Front Neurosci. 2020 Jan 31;14:6
pubmed: 32082106
J Neurosci Methods. 2018 Jan 1;293:117-127
pubmed: 28935423
Pain. 2008 Apr;135(3):240-250
pubmed: 17614199
Science. 2016 Nov 4;354(6312):584-587
pubmed: 27811269
Nat Rev Neurosci. 2010 Feb;11(2):127-38
pubmed: 20068583
Neuron. 2019 Mar 20;101(6):1029-1041
pubmed: 30897355
Brain Behav Immun. 2005 Jul;19(4):283-95
pubmed: 15890494
Pain. 2013 Dec;154 Suppl 1:S29-S43
pubmed: 24021862
Elife. 2017 May 19;6:
pubmed: 28524817
JAMA Neurol. 2018 Nov 1;75(11):1321-1330
pubmed: 30073258
J Psychosom Res. 2002 Feb;52(2):69-77
pubmed: 11832252
Neuron. 2014 Mar 19;81(6):1223-1239
pubmed: 24656247
Pain. 2011 Oct;152(10):2405-2412
pubmed: 21875771
Neurosci Biobehav Rev. 2011 Apr;35(5):1237-53
pubmed: 21185860
Proc Natl Acad Sci U S A. 2019 Jan 29;116(5):1782-1791
pubmed: 30642968
Philos Trans R Soc Lond B Biol Sci. 2005 Apr 29;360(1456):815-36
pubmed: 15937014
Nat Commun. 2018 Oct 26;9(1):4487
pubmed: 30367033
Acta Psychiatr Scand. 1983 Jun;67(6):361-70
pubmed: 6880820
Nat Rev Drug Discov. 2013 Mar;12(3):191-204
pubmed: 23449306
J Neurosci. 2011 Jun 22;31(25):9118-23
pubmed: 21697363
Wiley Interdiscip Rev Cogn Sci. 2011 Sep;2(5):580-593
pubmed: 26302308
PLoS Biol. 2007 May;5(5):e133
pubmed: 17456008
PLoS Biol. 2015 Jan 06;13(1):e1002036
pubmed: 25562688
Elife. 2018 Mar 20;7:
pubmed: 29555019
Pain. 2016 Jun;157(6):1179-1191
pubmed: 26945235
Pain. 2015 Feb;156(2):289-296
pubmed: 25599450
Nat Neurosci. 2020 Dec;23(12):1473-1483
pubmed: 32958924
Neurophysiol Clin. 2003 Dec;33(6):293-301
pubmed: 14678843
PLoS One. 2013 Oct 11;8(10):e78278
pubmed: 24147129
Pain. 2016 Aug;157(8):1588-1589
pubmed: 27428892
Trends Cogn Sci. 2018 Sep;22(9):764-779
pubmed: 30122170
Pain. 2008 Oct 15;139(2):306-314
pubmed: 18538928
Clin Neurophysiol. 2003 Apr;114(4):710-22
pubmed: 12686279
Psychosom Med. 2018 Jun;80(5):422-431
pubmed: 29621046
Behav Res Methods. 2007 May;39(2):175-91
pubmed: 17695343
Nat Commun. 2017 Feb 14;8:14211
pubmed: 28195170
Brain Behav Immun. 2006 May;20(3):219-30
pubmed: 16571371
J Neurosci. 2018 Apr 18;38(16):4020-4030
pubmed: 29581379
Trends Cogn Sci. 2017 Feb;21(2):100-110
pubmed: 28025007
Elife. 2021 Feb 17;10:
pubmed: 33594976
Neurophysiol Clin. 2003 Dec;33(6):279-92
pubmed: 14678842
Trends Cogn Sci. 2020 Mar;24(3):200-207
pubmed: 31954629
J Comput Neurosci. 2021 May;49(2):107-127
pubmed: 33595765
Pain. 2016 Feb;157(2):329-338
pubmed: 26447703
Behav Brain Sci. 2013 Jun;36(3):181-204
pubmed: 23663408
J Neurosci. 2019 Feb 13;39(7):1261-1274
pubmed: 30552181
J Neurosci. 2009 Jun 17;29(24):7909-16
pubmed: 19535602
J Neurosci. 2012 Sep 26;32(39):13389-95
pubmed: 23015429
Pain. 2018 Feb;159(2):206-211
pubmed: 29944612
Sci Data. 2019 Jun 25;6(1):103
pubmed: 31239435
Neuron. 2015 Jan 21;85(2):390-401
pubmed: 25556836
Nat Neurosci. 2020 Jul;23(7):788-799
pubmed: 32601411
Nat Rev Neurol. 2020 Jul;16(7):381-400
pubmed: 32541893
Pain. 2018 Sep;159 Suppl 1:S3-S10
pubmed: 30113941
Nat Rev Neurosci. 2015 Jul;16(7):403-18
pubmed: 26087681
Brain. 2012 Nov;135(Pt 11):3495-512
pubmed: 22641838
Neuron. 2015 Aug 5;87(3):474-91
pubmed: 26247858

Auteurs

Moritz M Nickel (MM)

Department of Neurology, School of Medicine, Technical University of Munich, Munich 81675, Germany.
Technical University of Munich Neuroimaging Center, School of Medicine, Technical University of Munich, Munich 81675, Germany.

Laura Tiemann (L)

Department of Neurology, School of Medicine, Technical University of Munich, Munich 81675, Germany.
Technical University of Munich Neuroimaging Center, School of Medicine, Technical University of Munich, Munich 81675, Germany.

Vanessa D Hohn (VD)

Department of Neurology, School of Medicine, Technical University of Munich, Munich 81675, Germany.
Technical University of Munich Neuroimaging Center, School of Medicine, Technical University of Munich, Munich 81675, Germany.

Elisabeth S May (ES)

Department of Neurology, School of Medicine, Technical University of Munich, Munich 81675, Germany.
Technical University of Munich Neuroimaging Center, School of Medicine, Technical University of Munich, Munich 81675, Germany.

Cristina Gil Ávila (C)

Department of Neurology, School of Medicine, Technical University of Munich, Munich 81675, Germany.
Technical University of Munich Neuroimaging Center, School of Medicine, Technical University of Munich, Munich 81675, Germany.

Falk Eippert (F)

Max Planck Research Group Pain Perception, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig 04103, Germany.

Markus Ploner (M)

Department of Neurology, School of Medicine, Technical University of Munich, Munich 81675, Germany; markus.ploner@tum.de.
Technical University of Munich Neuroimaging Center, School of Medicine, Technical University of Munich, Munich 81675, Germany.
Center for Interdisciplinary Pain Medicine, School of Medicine, Technical University of Munich, Munich 81675, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH