Primary somatosensory cortex bidirectionally modulates sensory gain and nociceptive behavior in a layer-specific manner.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
24 05 2023
Historique:
received: 01 08 2022
accepted: 16 05 2023
medline: 26 5 2023
pubmed: 25 5 2023
entrez: 24 5 2023
Statut: epublish

Résumé

The primary somatosensory cortex (S1) is a hub for body sensation of both innocuous and noxious signals, yet its role in somatosensation versus pain is debated. Despite known contributions of S1 to sensory gain modulation, its causal involvement in subjective sensory experiences remains elusive. Here, in mouse S1, we reveal the involvement of cortical output neurons in layers 5 (L5) and 6 (L6) in the perception of innocuous and noxious somatosensory signals. We find that L6 activation can drive aversive hypersensitivity and spontaneous nocifensive behavior. Linking behavior to neuronal mechanisms, we find that L6 enhances thalamic somatosensory responses, and in parallel, strongly suppresses L5 neurons. Directly suppressing L5 reproduced the pronociceptive phenotype induced by L6 activation, suggesting an anti-nociceptive function for L5 output. Indeed, L5 activation reduced sensory sensitivity and reversed inflammatory allodynia. Together, these findings reveal a layer-specific and bidirectional role for S1 in modulating subjective sensory experiences.

Identifiants

pubmed: 37225702
doi: 10.1038/s41467-023-38798-7
pii: 10.1038/s41467-023-38798-7
pmc: PMC10209111
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2999

Informations de copyright

© 2023. The Author(s).

Références

Sci Rep. 2017 May 30;7(1):2482
pubmed: 28559582
Pain. 2012 Apr;153(4):885-892
pubmed: 22365310
Nat Commun. 2023 May 24;14(1):2999
pubmed: 37225702
J Neurosci. 2020 Apr 1;40(14):2849-2858
pubmed: 32075900
Neuron. 2014 Sep 17;83(6):1431-43
pubmed: 25175879
Trends Cogn Sci. 2017 Feb;21(2):100-110
pubmed: 28025007
Neuron. 2017 Jul 5;95(1):180-194.e5
pubmed: 28625486
Curr Biol. 2021 Dec 6;31(23):5121-5137.e7
pubmed: 34614389
Neuroimage. 2021 Jul 1;234:117957
pubmed: 33744457
J Neurosci Methods. 2015 Nov 30;255:92-103
pubmed: 26296284
Proc Natl Acad Sci U S A. 2014 May 6;111(18):6798-803
pubmed: 24748112
J Physiol. 2007 May 15;581(Pt 1):139-54
pubmed: 17317752
Sci Rep. 2017 Oct 6;7(1):12743
pubmed: 28986567
Neurorehabil Neural Repair. 2012 Jul-Aug;26(6):646-52
pubmed: 22331213
Nature. 2021 Dec;600(7887):100-104
pubmed: 34614503
Physiol Rev. 2021 Jan 1;101(1):213-258
pubmed: 32525759
Nat Neurosci. 2017 Aug;20(8):1122-1132
pubmed: 28671692
Science. 1997 Aug 15;277(5328):968-71
pubmed: 9252330
Nature. 2017 May 11;545(7653):219-223
pubmed: 28467827
Elife. 2022 Mar 22;11:
pubmed: 35315775
Brain. 2005 Oct;128(Pt 10):2359-71
pubmed: 16109750
Nat Neurosci. 2015 Feb;18(2):170-81
pubmed: 25622573
J Neurosci. 2008 Feb 27;28(9):2006-14
pubmed: 18305235
Brain Res. 1989 Sep 4;496(1-2):357-60
pubmed: 2804648
J Neurosci. 2006 Aug 16;26(33):8441-50
pubmed: 16914669
Neuroscience. 2018 Sep 1;387:58-71
pubmed: 28978414
J Neurophysiol. 2010 Sep;104(3):1717-25
pubmed: 20660417
J Neurosci. 2014 Jul 16;34(29):9656-64
pubmed: 25031405
Nature. 2018 Sep;561(7724):547-550
pubmed: 30209395
J Neurophysiol. 2007 Aug;98(2):668-80
pubmed: 17537905
Sci Adv. 2021 Mar 19;7(12):
pubmed: 33741588
J Physiol. 2018 May 1;596(9):1639-1657
pubmed: 29313982
Science. 2022 Jul 8;377(6602):198-204
pubmed: 35857536
Front Neural Circuits. 2021 Sep 09;15:730211
pubmed: 34566583
Nat Neurosci. 2021 Dec;24(12):1711-1720
pubmed: 34764474
Nat Neurosci. 2014 Feb;17(2):183-91
pubmed: 24473266
J Stat Softw. 2008 Jun 1;26(1):1-21
pubmed: 19777145
J Comp Neurol. 2019 Feb 15;527(3):640-650
pubmed: 29524229
J Neurophysiol. 2016 Jul 1;116(1):159-70
pubmed: 27098028
Nature. 1994 Jun 9;369(6480):479-82
pubmed: 8202137
Cell. 2018 Mar 22;173(1):140-152.e15
pubmed: 29570993
Cell Rep. 2019 Sep 17;28(12):3131-3143.e5
pubmed: 31533036
Trends Cogn Sci. 2020 Oct;24(10):814-825
pubmed: 32855048
Science. 2006 Jun 16;312(5780):1622-7
pubmed: 16778049
Elife. 2021 Sep 09;10:
pubmed: 34497004
Neuron. 2015 May 6;86(3):768-82
pubmed: 25913856
Neurosci Lett. 2008 Dec 19;448(1):134-8
pubmed: 18805459
J Neurosci. 2022 Jul 20;:
pubmed: 35863890
Cell Rep. 2018 May 1;23(5):1314-1325
pubmed: 29719247
Nat Neurosci. 2015 Jan;18(1):104-11
pubmed: 25501036
Nature. 2012 Feb 22;483(7387):47-52
pubmed: 22367547
PLoS Biol. 2007 May;5(5):e133
pubmed: 17456008
Elife. 2021 Sep 27;10:
pubmed: 34570697
Nat Rev Neurosci. 2021 Jul;22(7):389-406
pubmed: 33958775
Pain. 2013 Jul;154(7):1156-1158
pubmed: 23590938
Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7705-9
pubmed: 10393884
J Neurophysiol. 2017 Jul 1;118(1):507-519
pubmed: 28331010
Nat Commun. 2019 Feb 28;10(1):983
pubmed: 30816113
Science. 2021 Apr 16;372(6539):
pubmed: 33859006
Nat Commun. 2022 May 11;13(1):2585
pubmed: 35546553
Nat Commun. 2018 Oct 8;9(1):4125
pubmed: 30297821
Proc Natl Acad Sci U S A. 2017 Jul 25;114(30):E6222-E6230
pubmed: 28698363
Nat Rev Neurosci. 2021 Aug;22(8):458-471
pubmed: 34127843
Curr Biol. 2021 Jan 25;31(2):310-321.e5
pubmed: 33157020
Pain. 2013 Mar;154(3):334-344
pubmed: 23245864
Pain. 2012 Apr;153(4):742-743
pubmed: 22365311
Front Mol Neurosci. 2017 Sep 06;10:284
pubmed: 28932184
Proc Natl Acad Sci U S A. 2020 Jun 9;117(23):13066-13077
pubmed: 32461374
Nat Neurosci. 2017 Nov;20(11):1591-1601
pubmed: 28920932
Pain. 2011 Nov;152(11):2505-2513
pubmed: 21906880
Neuroscience. 2003;117(3):715-22
pubmed: 12617975
Synapse. 2007 May;61(5):335-42
pubmed: 17318884
Curr Protoc Pharmacol. 2012 Mar;Chapter 5:Unit5.4
pubmed: 22382999
Nat Neurosci. 2010 Dec;13(12):1534-41
pubmed: 21102447
Neuron. 2015 Aug 5;87(3):474-91
pubmed: 26247858
Neuron. 2014 Apr 16;82(2):474-85
pubmed: 24656931
Life Sci. 1995;56(23-24):2111-8
pubmed: 7776839

Auteurs

Katharina Ziegler (K)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Ross Folkard (R)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Antonio J Gonzalez (AJ)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Jan Burghardt (J)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Sailaja Antharvedi-Goda (S)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Jesus Martin-Cortecero (J)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Emilio Isaías-Camacho (E)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany.

Sanjeev Kaushalya (S)

Department of Molecular Pharmacology, Institute for Pharmacology, Heidelberg University, Heidelberg, Germany.

Linette Liqi Tan (LL)

Department of Molecular Pharmacology, Institute for Pharmacology, Heidelberg University, Heidelberg, Germany.

Thomas Kuner (T)

Institute for Anatomy and Cell Biology, Heidelberg University, Heidelberg, Germany.

Claudio Acuna (C)

Chica and Heinz Schaller Research Group, Institute for Anatomy and Cell Biology, Heidelberg University, Heidelberg, Germany.

Rohini Kuner (R)

Department of Molecular Pharmacology, Institute for Pharmacology, Heidelberg University, Heidelberg, Germany.

Rebecca Audrey Mease (RA)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany. beckin@gmail.com.

Alexander Groh (A)

Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Heidelberg, Germany. groh@uni-heidelberg.de.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH