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Proc Natl Acad Sci U S A. 2021 Nov 23;118(47). doi: 10.1073/pnas.2105395118.

Single-neuron firing cascades underlie global spontaneous brain events.

Proceedings of the National Academy of Sciences of the United States of America

Xiao Liu, David A Leopold, Yifan Yang, Skerritt, Salokangas

Affiliations

  1. Department of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802; [email protected].
  2. Institute for Computational and Data Sciences, The Pennsylvania State University, University Park, PA 16802.
  3. Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, and National Eye Institute, NIH, Bethesda, MD 20892.
  4. Section on Cognitive Neurophysiology and Imaging, Laboratory of Neuropsychology, National Institute of Mental Health, NIH, Bethesda, MD 20892.
  5. Department of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802.

PMID: 34795053 PMCID: PMC8617517 DOI: 10.1073/pnas.2105395118

Abstract

The resting brain consumes enormous energy and shows highly organized spontaneous activity. To investigate how this activity is manifest among single neurons, we analyzed spiking discharges of ∼10,000 isolated cells recorded from multiple cortical and subcortical regions of the mouse brain during immobile rest. We found that firing of a significant proportion (∼70%) of neurons conformed to a ubiquitous, temporally sequenced cascade of spiking that was synchronized with global events and elapsed over timescales of 5 to 10 s. Across the brain, two intermixed populations of neurons supported orthogonal cascades. The relative phases of these cascades determined, at each moment, the response magnitude evoked by an external visual stimulus. Furthermore, the spiking of individual neurons embedded in these cascades was time locked to physiological indicators of arousal, including local field potential power, pupil diameter, and hippocampal ripples. These findings demonstrate that the large-scale coordination of low-frequency spontaneous activity, which is commonly observed in brain imaging and linked to arousal, sensory processing, and memory, is underpinned by sequential, large-scale temporal cascades of neuronal spiking across the brain.

Keywords: global signal; hippocampal ripples; low-frequency resting-state activity; neuronal population dynamics; sequential activations

Conflict of interest statement

The authors declare no competing interest.

References

  1. Hippocampus. 2015 Oct;25(10):1073-188 - PubMed
  2. PLoS Biol. 2021 Jun 1;19(6):e3001233 - PubMed
  3. Nat Neurosci. 2020 Jan;23(1):138-151 - PubMed
  4. Nature. 2012 Nov 22;491(7425):547-53 - PubMed
  5. Nature. 2017 Nov 8;551(7679):232-236 - PubMed
  6. Proc Natl Acad Sci U S A. 2015 Apr 28;112(17):E2235-44 - PubMed
  7. Science. 1996 Sep 27;273(5283):1868-71 - PubMed
  8. Neuroimage. 2013 Mar;68:93-104 - PubMed
  9. Neural Comput. 1999 Oct 1;11(7):1621-71 - PubMed
  10. Commun Biol. 2019 Nov 18;2:421 - PubMed
  11. Nat Rev Neurosci. 2007 Sep;8(9):700-11 - PubMed
  12. Science. 2019 Apr 19;364(6437):253 - PubMed
  13. Nat Neurosci. 2006 Jan;9(1):23-5 - PubMed
  14. J Neurosci. 1999 Jul 15;19(14):6191-9 - PubMed
  15. Neuroimage. 2018 Feb 15;167:297-308 - PubMed
  16. Neurochem Res. 2015 Dec;40(12):2583-99 - PubMed
  17. PLoS Comput Biol. 2017 May 24;13(5):e1005543 - PubMed
  18. J Neurosci. 2013 Nov 13;33(46):18190-9 - PubMed
  19. Neuron. 2018 Feb 21;97(4):940-952.e4 - PubMed
  20. Cereb Cortex. 2020 Sep 3;30(10):5242-5256 - PubMed
  21. Neuroimage. 2019 May 1;191:193-204 - PubMed
  22. Neuroimage. 2006 Jul 15;31(4):1536-48 - PubMed
  23. Curr Opin Neurobiol. 2006 Dec;16(6):710-5 - PubMed
  24. Neuron. 2020 Feb 5;105(3):549-561.e5 - PubMed
  25. Neuron. 1998 Nov;21(5):1123-8 - PubMed
  26. Electroencephalogr Clin Neurophysiol. 1965 Jul;19:25-33 - PubMed
  27. Nat Rev Neurol. 2010 Jan;6(1):15-28 - PubMed
  28. Science. 1982 Mar 5;215(4537):1237-9 - PubMed
  29. J Neurochem. 2017 Aug;142 Suppl 2:111-121 - PubMed
  30. Neuroscientist. 2019 Aug;25(4):298-313 - PubMed
  31. Mov Disord. 2021 Sep;36(9):2066-2076 - PubMed
  32. Arch Neurol. 1974 Feb;30(2):113-21 - PubMed
  33. Nat Commun. 2016 Nov 08;7:13289 - PubMed
  34. Neuron. 2014 Oct 22;84(2):355-62 - PubMed
  35. Neuroimage. 2017 Apr 15;150:213-229 - PubMed
  36. Exp Neurol. 2000 Jun;163(2):495-529 - PubMed
  37. Science. 2019 Nov 1;366(6465):628-631 - PubMed
  38. J Magn Reson Imaging. 2000 Apr;11(4):438-44 - PubMed
  39. Proc Natl Acad Sci U S A. 2020 Mar 24;117(12):6875-6882 - PubMed
  40. Proc Natl Acad Sci U S A. 2005 Jul 5;102(27):9673-8 - PubMed
  41. Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):2065-9 - PubMed
  42. Neuroimage. 2018 Aug 1;176:541-549 - PubMed
  43. Magn Reson Med. 1995 Oct;34(4):537-41 - PubMed
  44. J Theor Biol. 2006 Feb 21;238(4):962-74 - PubMed
  45. Cereb Cortex. 2021 Jul 29;31(9):3986-4005 - PubMed
  46. Cereb Cortex. 2021 Jan 1;31(1):324-340 - PubMed
  47. Neuroimage. 2009 Feb 1;44(3):857-69 - PubMed
  48. Fluids Barriers CNS. 2013 Dec 27;10(1):36 - PubMed
  49. Neuroimage. 2013 Dec;83:983-90 - PubMed
  50. Science. 2013 Oct 18;342(6156):373-7 - PubMed
  51. J Neurosci. 2013 Mar 13;33(11):4672-82 - PubMed
  52. Nat Commun. 2018 Jan 26;9(1):395 - PubMed
  53. Neuron. 2014 Jul 16;83(2):467-480 - PubMed
  54. Neuron. 2015 Jul 1;87(1):179-92 - PubMed
  55. Science. 2019 Apr 19;364(6437):255 - PubMed
  56. J Cereb Blood Flow Metab. 2019 Jun;39(6):1148-1160 - PubMed
  57. Science. 2019 Apr 19;364(6437): - PubMed

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