Sensory input drives rapid homeostatic scaling of the axon initial segment in mouse barrel cortex.


Journal

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

Informations de publication

Date de publication:
04 01 2021
Historique:
received: 06 03 2020
accepted: 16 11 2020
entrez: 5 1 2021
pubmed: 6 1 2021
medline: 14 1 2021
Statut: epublish

Résumé

The axon initial segment (AIS) is a critical microdomain for action potential initiation and implicated in the regulation of neuronal excitability during activity-dependent plasticity. While structural AIS plasticity has been suggested to fine-tune neuronal activity when network states change, whether it acts in vivo as a homeostatic regulatory mechanism in behaviorally relevant contexts remains poorly understood. Using the mouse whisker-to-barrel pathway as a model system in combination with immunofluorescence, confocal analysis and electrophysiological recordings, we observed bidirectional AIS plasticity in cortical pyramidal neurons. Furthermore, we find that structural and functional AIS remodeling occurs in distinct temporal domains: Long-term sensory deprivation elicits an AIS length increase, accompanied with an increase in neuronal excitability, while sensory enrichment results in a rapid AIS shortening, accompanied by a decrease in action potential generation. Our findings highlight a central role of the AIS in the homeostatic regulation of neuronal input-output relations.

Identifiants

pubmed: 33397944
doi: 10.1038/s41467-020-20232-x
pii: 10.1038/s41467-020-20232-x
pmc: PMC7782484
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

23

Références

Nature. 2004 Dec 9;432(7018):758-61
pubmed: 15592414
Cereb Cortex. 2017 Sep 1;27(9):4662-4675
pubmed: 28922860
Neuron. 2020 Apr 22;106(2):265-276.e6
pubmed: 32109363
Curr Opin Neurobiol. 2018 Aug;51:52-59
pubmed: 29533849
Neuroscientist. 2017 Aug;23(4):364-373
pubmed: 27143656
Neuroscience. 2002;109(4):687-99
pubmed: 11927151
Brain Struct Funct. 2014 Jul;219(4):1433-50
pubmed: 23728480
Proc Natl Acad Sci U S A. 2017 Sep 26;114(39):10479-10484
pubmed: 28894008
Front Neuroanat. 2014 Mar 11;8:11
pubmed: 24653680
Elife. 2020 Mar 30;9:
pubmed: 32223890
Eur J Neurosci. 2019 Sep;50(6):2955-2969
pubmed: 30941846
J Neurosci. 2006 Apr 19;26(16):4155-65
pubmed: 16624936
Nature. 2010 Jun 24;465(7301):1070-4
pubmed: 20543823
J Neurophysiol. 2004 Jul;92(1):144-56
pubmed: 14973314
Neuron. 2012 Jan 26;73(2):235-47
pubmed: 22284179
Front Cell Neurosci. 2017 Jun 06;11:157
pubmed: 28634442
Nat Neurosci. 2009 Aug;12(8):996-1002
pubmed: 19633666
Cell. 2012 May 25;149(5):1125-39
pubmed: 22632975
J Neurosci. 2007 Sep 5;27(36):9648-52
pubmed: 17804625
J Neurosci. 2009 Sep 2;29(35):10890-9
pubmed: 19726647
Elife. 2019 Dec 20;8:
pubmed: 31860443
Proc Natl Acad Sci U S A. 2015 Aug 4;112(31):9757-62
pubmed: 26195803
Eur J Neurosci. 2011 Nov;34(10):1609-19
pubmed: 22103418
Cereb Cortex. 2017 Oct 1;27(10):4835-4850
pubmed: 27620976
Neuroscience. 2011 Feb 3;174:10-25
pubmed: 21115101
Eur J Neurosci. 2008 Sep;28(5):849-61
pubmed: 18691332
Proc Natl Acad Sci U S A. 2017 Nov 21;114(47):E10234-E10243
pubmed: 29109270
Nat Commun. 2020 Jan 3;11(1):100
pubmed: 31900387
J Neurosci. 2016 Feb 17;36(7):2261-6
pubmed: 26888935
Elife. 2020 Mar 03;9:
pubmed: 32125273
Exp Neurol. 2018 Apr;302:169-180
pubmed: 29305051
J Neurosci. 2013 Apr 17;33(16):6950-63
pubmed: 23595753
J Physiol. 1957 Dec 3;139(2):232-49
pubmed: 13492210
J Neurosci. 2010 Feb 24;30(8):3082-92
pubmed: 20181605
Science. 2005 Nov 4;310(5749):810-5
pubmed: 16272113
J Physiol. 2012 Nov 15;590(22):5571-9
pubmed: 23027822
J Neurosci. 2016 Sep 21;36(38):9922-32
pubmed: 27656029
Front Cell Neurosci. 2019 Oct 15;13:456
pubmed: 31680869
Somatosens Mot Res. 2003;20(2):157-62
pubmed: 12850825
Sci Adv. 2015 Sep 11;1(8):e1500301
pubmed: 26523289
Dev Psychobiol. 2017 Jan;59(1):39-47
pubmed: 27473368
Neuron. 2019 Apr 17;102(2):358-372.e9
pubmed: 30846310
J Neurosci. 2011 Mar 23;31(12):4456-65
pubmed: 21430146
Behav Brain Res. 2015;287:146-55
pubmed: 25823761
Nat Neurosci. 2008 Feb;11(2):178-86
pubmed: 18204443
J Neurophysiol. 1996 Apr;75(4):1714-29
pubmed: 8727408
Neuroscience. 2018 Jan 1;368:268-282
pubmed: 28739523
Front Cell Neurosci. 2014 Jun 10;8:151
pubmed: 24959118
Cereb Cortex. 2016 Feb;26(2):820-37
pubmed: 26564256
Front Cell Neurosci. 2017 Nov 06;11:332
pubmed: 29170630
Cell Rep. 2015 Nov 10;13(6):1233-1245
pubmed: 26526995
Dev Neurobiol. 2007 Oct;67(12):1574-88
pubmed: 17542015
Proc Natl Acad Sci U S A. 2015 Jan 27;112(4):957-64
pubmed: 25552556
J Neurosci. 2015 Jan 28;35(4):1573-90
pubmed: 25632134
Neuron. 2010 Nov 4;68(3):500-11
pubmed: 21040850
Neuron. 2007 Oct 25;56(2):339-55
pubmed: 17964250
Trends Neurosci. 2016 Oct;39(10):656-667
pubmed: 27637565
Proc Natl Acad Sci U S A. 2016 Dec 20;113(51):14841-14846
pubmed: 27930291
Eur J Neurosci. 2012 May;35(10):1540-53
pubmed: 22607000
Somatosens Mot Res. 2006 Mar-Jun;23(1-2):1-10
pubmed: 16846954
Nature. 2010 Jun 24;465(7301):1075-8
pubmed: 20543825
J Neurosci. 2018 Feb 28;38(9):2135-2145
pubmed: 29378864
Neuron. 2009 Jan 29;61(2):259-71
pubmed: 19186168
J Neurosci. 2020 Aug 26;40(35):6709-6721
pubmed: 32719016
Cell Rep. 2015 Dec 29;13(12):2781-93
pubmed: 26711344
Neuron. 2019 Nov 6;104(3):458-470.e5
pubmed: 31542321
Proc Natl Acad Sci U S A. 2015 Jan 27;112(4):1214-9
pubmed: 25552561
J Comp Neurol. 1996 Sep 23;373(3):340-54
pubmed: 8889932
Neuron. 2001 Aug 2;31(2):305-15
pubmed: 11502260
Neuron. 2007 Aug 16;55(4):633-47
pubmed: 17698015
Prog Neurobiol. 2013 Apr;103:3-27
pubmed: 23195880
Neuron. 2019 Oct 23;104(2):305-321.e8
pubmed: 31474508
Nat Rev Neurosci. 2019 Sep;20(9):533-546
pubmed: 31367018

Auteurs

Nora Jamann (N)

Axonal Signaling Group, Netherlands Institute for Neurosciences (NIN), Royal Netherlands Academy for Arts and Sciences (KNAW), Amsterdam, The Netherlands.
Cell Biology, Neurobiology and Biophysics, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands.
Institute of Neuroanatomy, Mannheim Center for Translational Neuroscience (MCTN), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Dominik Dannehl (D)

Institute of Neuroanatomy, Mannheim Center for Translational Neuroscience (MCTN), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Nadja Lehmann (N)

Institute of Neuroanatomy, Mannheim Center for Translational Neuroscience (MCTN), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Robin Wagener (R)

Clinic of Neurology, University Hospital Heidelberg, Heidelberg, Germany.

Corinna Thielemann (C)

Institute of Neuroanatomy, Mannheim Center for Translational Neuroscience (MCTN), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Christian Schultz (C)

Institute of Neuroanatomy, Mannheim Center for Translational Neuroscience (MCTN), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Jochen Staiger (J)

Institute of Neuroanatomy, University Medical Center, Georg August University of Göttingen, Göttingen, Germany.

Maarten H P Kole (MHP)

Axonal Signaling Group, Netherlands Institute for Neurosciences (NIN), Royal Netherlands Academy for Arts and Sciences (KNAW), Amsterdam, The Netherlands. m.kole@nin.knaw.nl.
Cell Biology, Neurobiology and Biophysics, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands. m.kole@nin.knaw.nl.

Maren Engelhardt (M)

Institute of Neuroanatomy, Mannheim Center for Translational Neuroscience (MCTN), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany. maren.engelhardt@medma.uni-heidelberg.de.

Articles similaires

Humans Meals Time Factors Female Adult

Vancomycin-associated DRESS demonstrates delay in AST abnormalities.

Ahmed Hussein, Kateri L Schoettinger, Jourdan Hydol-Smith et al.
1.00
Humans Drug Hypersensitivity Syndrome Vancomycin Female Male
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

Classifications MeSH