• Modeling neuron-astrocyte inte...

Treffer: Modeling neuron-astrocyte interactions in neural networks using distributed simulation.

Title:
Modeling neuron-astrocyte interactions in neural networks using distributed simulation.
Authors:
Jiang HJ; Institute for Advanced Simulation (IAS-6), Jülich Research Centre, Jülich, Germany.; Institute of Zoology, Faculty of Mathematics and Natural Sciences, University of Cologne, Cologne, Germany., Aćimović J; Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland., Manninen T; Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland., Ahokainen I; Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland., Stapmanns J; Institute for Advanced Simulation (IAS-6), Jülich Research Centre, Jülich, Germany.; Department of Physics, Faculty 1, RWTH Aachen University, Aachen, Germany., Lehtimäki M; Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland., Diesmann M; Institute for Advanced Simulation (IAS-6), Jülich Research Centre, Jülich, Germany.; Department of Physics, Faculty 1, RWTH Aachen University, Aachen, Germany.; Department of Psychiatry, Psychotherapy and Psychosomatics, School of Medicine, RWTH Aachen University, Aachen, Germany., van Albada SJ; Institute for Advanced Simulation (IAS-6), Jülich Research Centre, Jülich, Germany.; Institute of Zoology, Faculty of Mathematics and Natural Sciences, University of Cologne, Cologne, Germany., Plesser HE; Institute for Advanced Simulation (IAS-6), Jülich Research Centre, Jülich, Germany.; Department of Data Science, Faculty of Science and Technology, Norwegian University of Life Sciences, Ås, Norway.; Käte Hamburger Kolleg: Cultures of Research (c:o/re), RWTH Aachen University, Aachen, Germany., Linne ML; Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.
Source:
PLoS computational biology [PLoS Comput Biol] 2025 Sep 19; Vol. 21 (9), pp. e1013503. Date of Electronic Publication: 2025 Sep 19 (Print Publication: 2025).
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238922 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7358 (Electronic) Linking ISSN: 1553734X NLM ISO Abbreviation: PLoS Comput Biol Subsets: MEDLINE
Imprint Name(s):
Original Publication: San Francisco, CA : Public Library of Science, [2005]-
MeSH Terms:
Astrocytes*/physiology , Astrocytes*/cytology , Neurons*/physiology , Models, Neurological* , Nerve Net*/physiology , Nerve Net*/cytology, Computer Simulation ; Humans ; Computational Biology ; Animals ; Cell Communication/physiology ; Neural Networks, Computer
References:
Brain Struct Funct. 2017 Jul;222(5):2017-2029. (PMID: 28280934)
Neuroscience. 2012 Mar 15;205:18-28. (PMID: 22233780)
Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10058-63. (PMID: 16782808)
Front Neuroinform. 2015 Sep 09;9:22. (PMID: 26441628)
Eur J Neurosci. 2016 Apr;43(7):923-32. (PMID: 27041234)
J Physiol. 2010 Mar 1;588(Pt 5):831-46. (PMID: 20083514)
Nat Commun. 2018 Sep 3;9(1):3554. (PMID: 30177844)
Neuron. 2020 Dec 23;108(6):1146-1162.e10. (PMID: 33086039)
Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9895-9. (PMID: 1329108)
Nature. 2023 Oct;622(7981):120-129. (PMID: 37674083)
Nat Neurosci. 2015 Jul;18(7):942-52. (PMID: 26108722)
Physiol Rev. 2018 Jan 1;98(1):239-389. (PMID: 29351512)
Neuron. 2018 May 16;98(4):726-735.e4. (PMID: 29706581)
Front Cell Neurosci. 2017 Feb 01;11:16. (PMID: 28203147)
Nat Neurosci. 2019 Feb;22(2):154-166. (PMID: 30664773)
Biol Cybern. 2008 Nov;99(4-5):335-47. (PMID: 19011922)
Proc Natl Acad Sci U S A. 2007 Feb 6;104(6):1995-2000. (PMID: 17259307)
Philos Trans R Soc Lond B Biol Sci. 2002 Dec 29;357(1428):1695-708. (PMID: 12626004)
Front Neuroinform. 2018 Feb 16;12:2. (PMID: 29503613)
Cereb Cortex. 2013 May;23(5):1240-6. (PMID: 22581850)
Aging Cell. 2023 Sep;22(9):e13939. (PMID: 37489544)
Front Neuroanat. 2015 Jun 10;9:76. (PMID: 26113811)
Cereb Cortex. 2021 Oct 22;31(12):5686-5703. (PMID: 34387659)
Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):E2832-41. (PMID: 23012414)
J Physiol Paris. 2006 Mar-May;99(2-3):98-102. (PMID: 16646155)
Nat Neurosci. 2023 Sep;26(9):1541-1554. (PMID: 37563296)
Imaging Neurosci (Camb). 2024 Apr 18;2:. (PMID: 40800542)
Nat Commun. 2020 Apr 20;11(1):1906. (PMID: 32312988)
Glia. 2018 Oct;66(10):2188-2199. (PMID: 30144319)
IEEE Trans Neural Netw Learn Syst. 2013 May;24(5):789-99. (PMID: 24808428)
Neuron. 2019 May 22;102(4):735-744. (PMID: 31121126)
J Neurosci. 2005 Mar 2;25(9):2192-203. (PMID: 15745945)
Neuroinformatics. 2023 Apr;21(2):375-406. (PMID: 36959372)
Nat Commun. 2014;5:3262. (PMID: 24500276)
Neuron. 2004 Sep 2;43(5):729-43. (PMID: 15339653)
PLoS Comput Biol. 2022 Sep 8;18(9):e1010086. (PMID: 36074778)
J Neurosci. 2015 Jan 21;35(3):1089-105. (PMID: 25609625)
J Biol Phys. 2009 Oct;35(4):413-23. (PMID: 19669414)
PLoS Comput Biol. 2016 Jun 06;12(6):e1004963. (PMID: 27271768)
Proc Natl Acad Sci U S A. 2022 Oct 25;119(43):e2207912119. (PMID: 36256810)
Nat Neurosci. 2012 Mar 25;15(5):746-53. (PMID: 22446881)
J Neurosci. 2011 May 25;31(21):7637-47. (PMID: 21613477)
Front Comput Neurosci. 2018 Apr 04;12:14. (PMID: 29670517)
Trends Neurosci. 2003 Oct;26(10):523-30. (PMID: 14522144)
J Neurosci. 2007 Jun 13;27(24):6473-7. (PMID: 17567808)
Front Neuroinform. 2018 May 01;12:20. (PMID: 29765315)
Proc Natl Acad Sci U S A. 2016 May 10;113(19):E2675-84. (PMID: 27122314)
J Neurosci. 2009 Mar 11;29(10):3276-87. (PMID: 19279265)
Cereb Cortex. 2020 May 18;30(6):3800-3819. (PMID: 31989178)
Neuron. 2018 Sep 19;99(6):1170-1187.e9. (PMID: 30174118)
J Neurosci. 2006 Jan 25;26(4):1219-30. (PMID: 16436609)
Nat Neurosci. 2015 May;18(5):708-17. (PMID: 25894291)
Science. 2007 Aug 24;317(5841):1083-6. (PMID: 17717185)
Cereb Cortex. 2018 Jan 1;28(1):184-198. (PMID: 28968832)
J Neurosci. 2002 Jan 1;22(1):183-92. (PMID: 11756501)
Curr Biol. 2023 Apr 10;33(7):1249-1264.e7. (PMID: 36921605)
Nat Commun. 2020 Sep 1;11(1):4388. (PMID: 32873805)
Nat Neurosci. 2001 Aug;4(8):803-12. (PMID: 11477426)
J Neurophysiol. 2010 Aug;104(2):713-25. (PMID: 20554846)
Front Neurosci. 2018 May 23;12:291. (PMID: 29875620)
J Neurosci. 2018 Jan 3;38(1):3-13. (PMID: 29298904)
Neurobiol Dis. 2013 Oct;58:68-75. (PMID: 23702310)
Phys Rev Lett. 2003 Dec 31;91(26 Pt 1):268101. (PMID: 14754091)
Trends Mol Med. 2007 Feb;13(2):54-63. (PMID: 17207662)
J Neurosci. 2004 Aug 4;24(31):6920-7. (PMID: 15295027)
Front Neuroinform. 2022 May 11;16:837549. (PMID: 35645755)
Glia. 2022 Aug;70(8):1554-1580. (PMID: 35297525)
Exp Neurol. 2006 Feb;197(2):495-504. (PMID: 16289054)
Eur J Neurosci. 1998 Jun;10(6):2129-42. (PMID: 9753099)
J Gen Physiol. 2010 Jun;135(6):583-94. (PMID: 20479112)
J Neurosci. 2018 Jan 3;38(1):14-25. (PMID: 29298905)
PLoS Comput Biol. 2015 Sep 01;11(9):e1004490. (PMID: 26325661)
PLoS Comput Biol. 2017 Mar 31;13(3):e1005467. (PMID: 28362877)
Neural Comput. 2005 Aug;17(8):1776-801. (PMID: 15969917)
PLoS Biol. 2012 Feb;10(2):e1001259. (PMID: 22347811)
Nature. 1994 Jun 30;369(6483):744-7. (PMID: 7911978)
Elife. 2022 Jul 06;11:. (PMID: 35792600)
PLoS Comput Biol. 2022 Jul 21;18(7):e1010296. (PMID: 35862433)
Biol Cybern. 2008 Nov;99(4-5):319-34. (PMID: 19011921)
Prog Neurobiol. 2022 Jun;213:102264. (PMID: 35283239)
J Neurophysiol. 2005 Nov;94(5):3637-42. (PMID: 16014787)
J Neurosci. 2017 Oct 11;37(41):9859-9870. (PMID: 28899919)
ASN Neuro. 2015 Oct 21;7(5):. (PMID: 26489684)
Prog Neurobiol. 2019 Dec;183:101696. (PMID: 31550514)
J Comput Neurosci. 2000 May-Jun;8(3):183-208. (PMID: 10809012)
J Theor Biol. 1994 Feb 21;166(4):461-73. (PMID: 8176949)
Trends Neurosci. 1999 May;22(5):208-15. (PMID: 10322493)
Nat Commun. 2020 Jul 23;11(1):3689. (PMID: 32704144)
Science. 2002 Oct 25;298(5594):824-7. (PMID: 12399590)
Elife. 2019 Aug 20;8:. (PMID: 31429824)
PLoS Comput Biol. 2011 May;7(5):e1002059. (PMID: 21625580)
PLoS Comput Biol. 2009 Aug;5(8):e1000456. (PMID: 19662159)
Neuron. 2008 Apr 24;58(2):168-78. (PMID: 18439402)
Cereb Cortex. 2011 Aug;21(8):1889-900. (PMID: 21212170)
J Neurosci. 1998 Sep 1;18(17):6822-9. (PMID: 9712653)
Entry Date(s):
Date Created: 20250919 Date Completed: 20251003 Latest Revision: 20251005
Update Code:
20251005
PubMed Central ID:
PMC12494295
DOI:
10.1371/journal.pcbi.1013503
PMID:
40971948
Database:
MEDLINE

Weitere Informationen

Astrocytes engage in local interactions with neurons, synapses, other glial cell types, and the vasculature through intricate cellular and molecular processes, playing an important role in brain information processing, plasticity, cognition, and behavior. This study advances understanding of local interactions and self-organization of neuron-astrocyte networks and contributes to the broader investigation of their potential relationship with global activity regimes and overall brain function. We present six new contributions: (1) the development of a new model-building framework for neuron-astrocyte networks, (2) the introduction of connectivity concepts for tripartite neuron-astrocyte interactions in biological neural networks, (3) the design of a scalable architecture capable of simulating networks with up to a million cells, (4) a formalized description of neuron-astrocyte modeling that facilitates reproducibility, (5) the integration of experimental data to a greater extent than existing studies, and (6) simulation results demonstrating how neuron-astrocyte interactions drive the emergence of synchronization in local neuronal groups. Specifically, we develop a new technology for representing astrocytes and their interactions with neurons in distributed simulation code for large-scale spiking neuronal networks. This includes an astrocyte model with calcium dynamics, an extended neuron model receiving calcium-dependent signals from astrocytes, and a parallelized connectivity generation scheme for tripartite interactions between pre- and postsynaptic neurons and astrocytes. We verify the efficiency of our reference implementation through benchmarks varying in computing resources and network sizes. Our in silico experiments reproduce experimental data on astrocytic effects on neuronal synchronization, demonstrating that astrocytes consistently induce local synchronization in groups of neurons across various connectivity schemes and global activity regimes. By adjusting the strength of neuron-astrocyte interactions, we can switch the global activity regime from asynchronous to network-wide synchronization. This work represents an advancement in neuron-astrocyte modeling, introducing a novel framework that enables large-scale simulations of astrocytic influence on neuronal networks.
(Copyright: © 2025 Jiang 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.)

The authors have declared that no competing interests exist.