Biological complexity facilitates tuning of the neuronal parameter space.
Journal
PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
received:
16
02
2023
accepted:
24
05
2023
revised:
18
07
2023
medline:
21
7
2023
pubmed:
3
7
2023
entrez:
3
7
2023
Statut:
epublish
Résumé
The electrical and computational properties of neurons in our brains are determined by a rich repertoire of membrane-spanning ion channels and elaborate dendritic trees. However, the precise reason for this inherent complexity remains unknown, given that simpler models with fewer ion channels are also able to functionally reproduce the behaviour of some neurons. Here, we stochastically varied the ion channel densities of a biophysically detailed dentate gyrus granule cell model to produce a large population of putative granule cells, comparing those with all 15 original ion channels to their reduced but functional counterparts containing only 5 ion channels. Strikingly, valid parameter combinations in the full models were dramatically more frequent at ~6% vs. ~1% in the simpler model. The full models were also more stable in the face of perturbations to channel expression levels. Scaling up the numbers of ion channels artificially in the reduced models recovered these advantages confirming the key contribution of the actual number of ion channel types. We conclude that the diversity of ion channels gives a neuron greater flexibility and robustness to achieve a target excitability.
Identifiants
pubmed: 37399220
doi: 10.1371/journal.pcbi.1011212
pii: PCOMPBIOL-D-23-00254
pmc: PMC10353791
doi:
Substances chimiques
Ion Channels
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1011212Informations de copyright
Copyright: © 2023 Schneider 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
PLoS One. 2009;4(4):e5320
pubmed: 19399173
Neuron. 2003 Jan 9;37(1):109-20
pubmed: 12526777
Proc Natl Acad Sci U S A. 2011 Sep 13;108 Suppl 3:15542-8
pubmed: 21383190
J Neurosci. 2010 Dec 1;30(48):16332-42
pubmed: 21123579
Proc Natl Acad Sci U S A. 2023 Feb 21;120(8):e2219049120
pubmed: 36787352
J Neurophysiol. 2002 Feb;87(2):1129-31
pubmed: 11826077
PLoS Comput Biol. 2011 Jul;7(7):e1002107
pubmed: 21829333
J Physiol. 2008 Mar 15;586(6):1565-79
pubmed: 18187474
Science. 1999 Apr 2;284(5411):96-8
pubmed: 10102826
J Neurosci. 2008 Jul 23;28(30):7476-91
pubmed: 18650326
Elife. 2020 Jul 08;9:
pubmed: 32639229
J Neurosci. 2020 Jan 15;40(3):496-508
pubmed: 31719168
Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13763-8
pubmed: 11698650
Nat Neurosci. 2004 Dec;7(12):1345-52
pubmed: 15558066
Neuron. 2014 May 21;82(4):809-21
pubmed: 24853940
Nat Rev Neurosci. 2006 Jul;7(7):563-74
pubmed: 16791145
Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13187-91
pubmed: 17652510
Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):E5361-70
pubmed: 26354124
Nat Neurosci. 2005 Dec;8(12):1667-76
pubmed: 16299501
Science. 1983 May 13;220(4598):671-80
pubmed: 17813860
Neuroscience. 1988 Jun;25(3):729-49
pubmed: 2457185
Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):E2645-54
pubmed: 23798391
Nat Neurosci. 2006 Mar;9(3):356-62
pubmed: 16444270
J Neurosci. 2003 Oct 8;23(27):9059-67
pubmed: 14534239
J Neurophysiol. 2007 Dec;98(6):3749-58
pubmed: 17855581
PLoS Comput Biol. 2010 Aug 05;6(8):
pubmed: 20700495
J Neurosci. 2007 Aug 8;27(32):8709-18
pubmed: 17687048
Circ Res. 2005 Dec 9;97(12):1342-50
pubmed: 16293790
Elife. 2019 Jan 31;8:
pubmed: 30702427
J Neurophysiol. 2005 Dec;94(6):3730-42
pubmed: 16093338
Neuron. 2021 Nov 17;109(22):3647-3662.e7
pubmed: 34555313
Neural Comput. 1999 Jul 1;11(5):1079-96
pubmed: 10418158
Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):E2098-105
pubmed: 23690584
Annu Rev Neurosci. 2021 Jul 8;44:335-357
pubmed: 33770451
Curr Opin Neurobiol. 2021 Dec;71:84-91
pubmed: 34688051
Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3257-62
pubmed: 10077671
J Comput Neurosci. 1999 Sep-Oct;7(2):149-71
pubmed: 10515252
Trends Neurosci. 1990 Mar;13(3):99-104
pubmed: 1691879
Ann N Y Acad Sci. 1999 Apr 30;868:233-85
pubmed: 10414301
J Neurophysiol. 2005 Nov;94(5):3601-17
pubmed: 16049145
J Neurosci. 2007 Aug 1;27(31):8430-41
pubmed: 17670990
Curr Opin Neurobiol. 2016 Apr;37:44-52
pubmed: 26774694
Curr Res Neurobiol. 2021 Mar 5;2:100007
pubmed: 33997798
Genes (Basel). 2019 Sep 26;10(10):
pubmed: 31561430
J Physiol. 2010 Jan 1;588(Pt 1):157-70
pubmed: 19917565
Hippocampus. 2019 Oct;29(10):980-1022
pubmed: 31301166
J Neurophysiol. 1992 Feb;67(2):318-31
pubmed: 1373762
Nat Rev Neurosci. 2007 Jun;8(6):451-65
pubmed: 17514198
PLoS One. 2014 Oct 31;9(10):e106567
pubmed: 25360752
Cell. 2008 Oct 17;135(2):216-26
pubmed: 18957198
Open Biol. 2022 Jul;12(7):220073
pubmed: 35857898
J Neurosci. 1998 Apr 1;18(7):2309-20
pubmed: 9502792
Nat Neurosci. 1999 Jun;2(6):515-20
pubmed: 10448215
Neuron. 2003 Aug 28;39(5):831-42
pubmed: 12948449
J Neurosci Methods. 2012 Sep 15;210(1):22-34
pubmed: 22524993
Neuroinformatics. 2011 Mar;9(1):91-6
pubmed: 21222051
Cereb Cortex. 2012 Sep;22(9):2087-101
pubmed: 22038909
Annu Rev Neurosci. 2014;37:329-46
pubmed: 25032499
Front Neurosci. 2007 Oct 15;1(1):7-18
pubmed: 18982116
J Physiol. 2009 Sep 1;587(Pt 17):4213-33
pubmed: 19564397
Sci Rep. 2018 Sep 11;8(1):13637
pubmed: 30206240
PLoS Comput Biol. 2006 Jul 21;2(7):e94
pubmed: 16848639
J Neurophysiol. 2003 Dec;90(6):3998-4015
pubmed: 12944532
Neural Comput. 1997 Aug 15;9(6):1179-209
pubmed: 9248061
J Comput Neurosci. 2013 Apr;34(2):211-29
pubmed: 22878689
Am Sci. 1948 Oct;36(4):536-44
pubmed: 18882675
Elife. 2022 Mar 16;11:
pubmed: 35293858
J Neurosci. 2005 Apr 6;25(14):3509-20
pubmed: 15814781
Nature. 2006 Nov 30;444(7119):643-6
pubmed: 17122776
Elife. 2017 Nov 22;6:
pubmed: 29165247
Biol Cybern. 2008 Nov;99(4-5):241-51
pubmed: 19011918