A biophysical model explains the spontaneous bursting behavior in the developing retina.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
12 02 2019
12 02 2019
Historique:
received:
24
11
2017
accepted:
21
12
2018
entrez:
14
2
2019
pubmed:
14
2
2019
medline:
24
9
2020
Statut:
epublish
Résumé
During early development, waves of activity propagate across the retina and play a key role in the proper wiring of the early visual system. During a particular phase of the retina development (stage II) these waves are triggered by a transient network of neurons, called Starburst Amacrine Cells (SACs), showing a bursting activity which disappears upon further maturation. The underlying mechanisms of the spontaneous bursting and the transient excitability of immature SACs are not completely clear yet. While several models have attempted to reproduce retinal waves, none of them is able to mimic the rhythmic autonomous bursting of individual SACs and reveal how these cells change their intrinsic properties during development. Here, we introduce a mathematical model, grounded on biophysics, which enables us to reproduce the bursting activity of SACs and to propose a plausible, generic and robust, mechanism that generates it. The core parameters controlling repetitive firing are fast depolarizing V-gated calcium channels and hyperpolarizing V-gated potassium channels. The quiescent phase of bursting is controlled by a slow after hyperpolarization (sAHP), mediated by calcium-dependent potassium channels. Based on a bifurcation analysis we show how biophysical parameters, regulating calcium and potassium activity, control the spontaneously occurring fast oscillatory activity followed by long refractory periods in individual SACs. We make a testable experimental prediction on the role of voltage-dependent potassium channels on the excitability properties of SACs and on the evolution of this excitability along development. We also propose an explanation on how SACs can exhibit a large variability in their bursting periods, as observed experimentally within a SACs network as well as across different species, yet based on a simple, unique, mechanism. As we discuss, these observations at the cellular level have a deep impact on the retinal waves description.
Identifiants
pubmed: 30755684
doi: 10.1038/s41598-018-38299-4
pii: 10.1038/s41598-018-38299-4
pmc: PMC6372601
doi:
Substances chimiques
Calmodulin
0
Potassium Channels
0
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1859Références
J Neurosci. 1999 May 1;19(9):3580-93
pubmed: 10212317
J Neurosci. 1999 May 15;19(10):3874-87
pubmed: 10234019
J Neurosci. 2000 Jan 15;20(2):RC56
pubmed: 10632622
Neuron. 2001 Jun;30(3):771-80
pubmed: 11430810
Nature. 2002 Nov 28;420(6914):411-4
pubmed: 12459782
J Neurophysiol. 2004 Jan;91(1):324-35
pubmed: 12917389
J Neurosci. 2004 Aug 18;24(33):7335-43
pubmed: 15317859
Neuron. 2004 Dec 2;44(5):851-64
pubmed: 15572115
J Neurophysiol. 2006 Apr;95(4):2404-16
pubmed: 16371454
Nat Neurosci. 2006 Mar;9(3):363-71
pubmed: 16462736
J Neurosci. 2006 May 10;26(19):5190-7
pubmed: 16687510
Nat Rev Neurosci. 2006 Jul;7(7):563-74
pubmed: 16791145
J Neurophysiol. 2007 Jun;97(6):4225-34
pubmed: 17428902
PLoS Comput Biol. 2007 Nov;3(11):e245
pubmed: 18052546
J Neurosci. 2009 Jan 28;29(4):1077-86
pubmed: 19176816
Mol Biosyst. 2009 Dec;5(12):1527-35
pubmed: 19763323
Phys Rev E Stat Nonlin Soft Matter Phys. 2010 Jul;82(1 Pt 1):011127
pubmed: 20866585
Vis Neurosci. 2012 Jan;29(1):61-71
pubmed: 21787461
J Neurosci. 2012 Jan 18;32(3):850-63
pubmed: 22262883
PLoS Comput Biol. 2012;8(8):e1002628
pubmed: 22912566
J Comput Neurosci. 2013 Apr;34(2):345-66
pubmed: 23053862
J Biol Phys. 2005 May;31(2):183-206
pubmed: 23345891
J Physiol. 2014 Apr 1;592(7):1545-63
pubmed: 24366261
J Neurophysiol. 2014 Sep 15;112(6):1491-504
pubmed: 25008417
PLoS Comput Biol. 2014 Dec 04;10(12):e1003953
pubmed: 25474327
J Neurosci. 2016 Mar 30;36(13):3871-86
pubmed: 27030771
PLoS Comput Biol. 2017 Feb 15;13(2):e1005275
pubmed: 28199326
Biophys J. 1981 Jul;35(1):193-213
pubmed: 7260316
J Neurosci. 1994 Dec;14(12):7426-39
pubmed: 7996185
Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8057-62
pubmed: 8755602
Neuron. 1997 Aug;19(2):293-306
pubmed: 9292720
J Neurosci. 1998 Jun 1;18(11):4155-65
pubmed: 9592095