Bursting gamma oscillations in neural mass models.

Manoj Kumar Nandi, Michele Valla, Matteo di Volo
Author Information
  1. Manoj Kumar Nandi: Université Claude Bernard Lyon 1, Lyon, Rhône-Alpes, France.
  2. Michele Valla: Université Claude Bernard Lyon 1, Lyon, Rhône-Alpes, France.
  3. Matteo di Volo: Université Claude Bernard Lyon 1, Lyon, Rhône-Alpes, France.

Abstract

Gamma oscillations (30-120 Hz) in the brain are not periodic cycles, but they typically appear in short-time windows, often called oscillatory bursts. While the origin of this bursting phenomenon is still unclear, some recent studies hypothesize its origin in the external or endogenous noise of neural networks. We demonstrate that an exact neural mass model of excitatory and inhibitory quadratic-integrate and fire-spiking neurons theoretically predicts the emergence of a different regime of intrinsic bursting gamma (IBG) oscillations without any noise source, a phenomenon due to collective chaos. This regime is indeed observed in the direct simulation of spiking neurons, characterized by highly irregular spiking activity. IBG oscillations are distinguished by higher phase-amplitude coupling to slower theta oscillations concerning noise-induced bursting oscillations, thus indicating an increased capacity for information transfer between brain regions. We demonstrate that this phenomenon is present in both globally coupled and sparse networks of spiking neurons. These results propose a new mechanism for gamma oscillatory activity, suggesting deterministic collective chaos as a good candidate for the origin of gamma bursts.

Keywords

References

  1. Phys Rev Lett. 2023 Mar 3;130(9):097402 [PMID: 36930929]
  2. Neuron. 2013 Mar 20;77(6):1002-16 [PMID: 23522038]
  3. Prog Brain Res. 2006;159:275-95 [PMID: 17071238]
  4. J Comput Neurosci. 2024 May;52(2):165-181 [PMID: 38512693]
  5. Phys Rev Lett. 2021 Jul 16;127(3):038301 [PMID: 34328756]
  6. Phys Rev E. 2023 Feb;107(2-1):024311 [PMID: 36932567]
  7. Biophys J. 1972 Jan;12(1):1-24 [PMID: 4332108]
  8. Neural Comput. 2020 Sep;32(9):1615-1634 [PMID: 32687770]
  9. Neural Comput. 1999 Oct 1;11(7):1621-71 [PMID: 10490941]
  10. Curr Opin Neurobiol. 2015 Apr;31:45-50 [PMID: 25168855]
  11. Phys Rev E Stat Nonlin Soft Matter Phys. 2002 Nov;66(5 Pt 1):051917 [PMID: 12513533]
  12. Neuron. 2016 Jul 20;91(2):260-92 [PMID: 27477017]
  13. Neuron. 2020 Jan 8;105(1):180-197.e5 [PMID: 31732258]
  14. Nat Rev Neurosci. 2008 Mar;9(3):182-94 [PMID: 18270514]
  15. PLoS Comput Biol. 2017 Dec 29;13(12):e1005881 [PMID: 29287081]
  16. Chaos. 2008 Sep;18(3):037113 [PMID: 19045487]
  17. Nat Neurosci. 2024 Mar;27(3):547-560 [PMID: 38238431]
  18. Phys Rev E. 2022 Dec;106(6):L062302 [PMID: 36671128]
  19. J Neurophysiol. 2020 Feb 1;123(2):726-742 [PMID: 31774370]
  20. Physiol Rev. 2010 Jul;90(3):1195-268 [PMID: 20664082]
  21. J Comput Neurosci. 2024 Aug;52(3):207-222 [PMID: 38967732]
  22. Front Syst Neurosci. 2021 Dec 10;15:752261 [PMID: 34955768]
  23. Neuron. 2012 Sep 6;75(5):875-88 [PMID: 22958827]
  24. Nat Commun. 2022 Apr 19;13(1):2019 [PMID: 35440540]
  25. Neuron. 2010 Sep 9;67(5):885-96 [PMID: 20826318]
  26. Front Comput Neurosci. 2020 May 28;14:47 [PMID: 32547379]
  27. Nat Commun. 2024 Feb 29;15(1):1849 [PMID: 38418832]
  28. Phys Rev E Stat Nonlin Soft Matter Phys. 2010 Apr;81(4 Pt 2):046119 [PMID: 20481798]
  29. J Neurosci. 2012 Jan 11;32(2):423-35 [PMID: 22238079]
  30. Nat Methods. 2020 Mar;17(3):261-272 [PMID: 32015543]
  31. Elife. 2023 Mar 14;12: [PMID: 36917621]
  32. Phys Rev E. 2022 Apr;105(4-1):044402 [PMID: 35590671]
  33. Neural Comput. 2019 Apr;31(4):653-680 [PMID: 30764741]
  34. Science. 2001 Feb 23;291(5508):1560-3 [PMID: 11222864]
  35. Annu Rev Neurosci. 2012;35:203-25 [PMID: 22443509]
  36. Neuroimage. 2005 Oct 15;28(1):154-64 [PMID: 16023374]
  37. Sci Rep. 2021 Sep 2;11(1):17611 [PMID: 34475456]
  38. Cereb Cortex. 2016 Sep;26(9):3744-3753 [PMID: 26250776]
  39. Science. 2006 Sep 15;313(5793):1626-8 [PMID: 16973878]
  40. Phys Rev Lett. 2018 Sep 21;121(12):128301 [PMID: 30296134]
  41. Neuron. 2015 Oct 7;88(1):220-35 [PMID: 26447583]
  42. J Neurophysiol. 2020 Mar 1;123(3):1042-1051 [PMID: 31851573]
  43. Neuron. 2009 Sep 24;63(6):727-32 [PMID: 19778503]
  44. Hum Brain Mapp. 2009 Jun;30(6):1758-71 [PMID: 19343801]

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