The flattening of spacetime hierarchy of the -dimethyltryptamine brain state is characterized by harmonic decomposition of spacetime (HADES) framework.

Jakub Vohryzek, Joana Cabral, Christopher Timmermann, Selen Atasoy, Leor Roseman, David J Nutt, Robin L Carhart-Harris, Gustavo Deco, Morten L Kringelbach
Author Information
  1. Jakub Vohryzek: Centre for Eudaimonia and Human Flourishing, Linacre College, Department of Psychiatry, University of Oxford, Oxford OX3 9BX, UK. ORCID
  2. Joana Cabral: Centre for Eudaimonia and Human Flourishing, Linacre College, Department of Psychiatry, University of Oxford, Oxford OX3 9BX, UK.
  3. Christopher Timmermann: Centre for Psychedelic Research, Department of Brain Sciences, Imperial College London, London SW7 2AZ, UK. ORCID
  4. Selen Atasoy: Centre for Eudaimonia and Human Flourishing, Linacre College, Department of Psychiatry, University of Oxford, Oxford OX3 9BX, UK.
  5. Leor Roseman: Centre for Psychedelic Research, Department of Brain Sciences, Imperial College London, London SW7 2AZ, UK.
  6. David J Nutt: Centre for Psychedelic Research, Department of Brain Sciences, Imperial College London, London SW7 2AZ, UK.
  7. Robin L Carhart-Harris: Centre for Psychedelic Research, Department of Brain Sciences, Imperial College London, London SW7 2AZ, UK.
  8. Gustavo Deco: Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona 08005, Spain.
  9. Morten L Kringelbach: Centre for Eudaimonia and Human Flourishing, Linacre College, Department of Psychiatry, University of Oxford, Oxford OX3 9BX, UK. ORCID

Abstract

The human brain is a complex system, whose activity exhibits flexible and continuous reorganization across space and time. The decomposition of whole-brain recordings into harmonic modes has revealed a repertoire of gradient-like activity patterns associated with distinct brain functions. However, the way these activity patterns are expressed over time with their changes in various brain states remains unclear. Here, we investigate healthy participants taking the serotonergic psychedelic -dimethyltryptamine (DMT) with the Harmonic Decomposition of Spacetime (HADES) framework that can characterize how different harmonic modes defined in space are expressed over time. HADES demonstrates significant decreases in contributions across most low-frequency harmonic modes in the DMT-induced brain state. When normalizing the contributions by condition (DMT and non-DMT), we detect a decrease specifically in the second functional harmonic, which represents the uni- to transmodal functional hierarchy of the brain, supporting the leading hypothesis that functional hierarchy is changed in psychedelics. Moreover, HADES' dynamic spacetime measures of fractional occupancy, life time and latent space provide a precise description of the significant changes of the spacetime hierarchical organization of brain activity in the psychedelic state.

Keywords

References

  1. Nat Neurosci. 2018 Sep;21(9):1251-1259 [PMID: 30082915]
  2. Proc Natl Acad Sci U S A. 2016 Apr 26;113(17):4853-8 [PMID: 27071089]
  3. Phys Life Rev. 2010 Jun;7(2):195-249 [PMID: 20417160]
  4. Hum Brain Mapp. 2005 Feb;24(2):109-29 [PMID: 15468155]
  5. Front Hum Neurosci. 2014 Feb 03;8:20 [PMID: 24550805]
  6. Pharmacol Rev. 2016 Apr;68(2):264-355 [PMID: 26841800]
  7. Neuroimage. 2017 Oct 15;160:73-83 [PMID: 27845257]
  8. Neuroimage. 2019 Oct 1;199:127-142 [PMID: 31132450]
  9. Neuropharmacology. 2023 Mar 15;226:109398 [PMID: 36584883]
  10. J Neurosci. 2012 Mar 7;32(10):3366-75 [PMID: 22399758]
  11. Brain Commun. 2024 Feb 15;6(2):fcae049 [PMID: 38515439]
  12. Nature. 2020 Nov;587(7834):432-436 [PMID: 33029013]
  13. Proc Natl Acad Sci U S A. 2017 Nov 28;114(48):12827-12832 [PMID: 29087305]
  14. Neuroscientist. 2018 Jun;24(3):277-293 [PMID: 28863720]
  15. Elife. 2014 Mar 25;3:e01867 [PMID: 24668169]
  16. Commun Biol. 2020 Mar 5;3(1):103 [PMID: 32139786]
  17. Cereb Cortex. 1991 Jan-Feb;1(1):1-47 [PMID: 1822724]
  18. Nat Rev Neurosci. 2018 Nov;19(11):672-686 [PMID: 30305712]
  19. Prog Brain Res. 2018;242:97-120 [PMID: 30471684]
  20. Nat Rev Neurosci. 2021 Mar;22(3):181-192 [PMID: 33483717]
  21. Sci Adv. 2021 Jul 21;7(30): [PMID: 34290088]
  22. Proc Natl Acad Sci U S A. 2022 Feb 15;119(7): [PMID: 35145021]
  23. Front Syst Neurosci. 2016 Oct 07;10:81 [PMID: 27781035]
  24. Rev Neurosci. 2017 Apr 1;28(3):235-245 [PMID: 28107174]
  25. Neuron. 2017 Aug 2;95(3):709-721.e5 [PMID: 28772125]
  26. Science. 2001 Nov 9;294(5545):1350-4 [PMID: 11701930]
  27. Hum Brain Mapp. 2014 Nov;35(11):5442-56 [PMID: 24989126]
  28. Netw Neurosci. 2020 Feb 01;4(1):115-133 [PMID: 32043046]
  29. Pharmacol Rev. 2019 Jul;71(3):316-344 [PMID: 31221820]
  30. Behav Brain Res. 2022 Apr 29;424:113788 [PMID: 35149122]
  31. Brain Connect. 2017 Dec;7(10):661-670 [PMID: 28891322]
  32. Sci Rep. 2017 Dec 15;7(1):17661 [PMID: 29247209]
  33. Sci Rep. 2019 Nov 19;9(1):16324 [PMID: 31745107]
  34. Proc Natl Acad Sci U S A. 2010 Jul 20;107(29):13135-40 [PMID: 20624964]
  35. Front Psychol. 2018 Aug 15;9:1424 [PMID: 30174629]
  36. Trends Cogn Sci. 2014 Jan;18(1):46-55 [PMID: 24501779]
  37. Neuroimage. 2018 Apr 15;170:83-94 [PMID: 28666880]
  38. Neuroimage. 2017 Oct 15;160:41-54 [PMID: 28034766]
  39. Trends Cogn Sci. 2014 Sep;18(9):480-7 [PMID: 24788139]
  40. PLoS Biol. 2008 Jul 1;6(7):e159 [PMID: 18597554]
  41. Trends Cogn Sci. 2019 Jul;23(7):572-583 [PMID: 31076192]
  42. Nat Commun. 2016 Jan 21;7:10340 [PMID: 26792267]
  43. Trends Cogn Sci. 2022 Feb;26(2):159-173 [PMID: 34991988]
  44. Cereb Cortex. 2017 Feb 1;27(2):981-997 [PMID: 28184415]
  45. Front Syst Neurosci. 2020 Apr 17;14:20 [PMID: 32362815]
  46. J Physiol Paris. 2006 Jul-Sep;100(1-3):70-87 [PMID: 17097864]
  47. Entropy (Basel). 2024 Jan 22;26(1): [PMID: 38275498]
  48. Proc Natl Acad Sci U S A. 2014 Dec 9;111(49):17642-7 [PMID: 25422426]
  49. Commun Biol. 2023 Jan 28;6(1):117 [PMID: 36709401]
  50. Proc Natl Acad Sci U S A. 2016 Nov 1;113(44):12574-12579 [PMID: 27791099]
  51. Proc Natl Acad Sci U S A. 2005 Jul 5;102(27):9673-8 [PMID: 15976020]
  52. Psychol Med. 2019 Mar;49(4):655-663 [PMID: 29903051]
  53. Phys Rev Lett. 2020 Dec 4;125(23):238101 [PMID: 33337222]
  54. Front Physiol. 2012 Feb 08;3:15 [PMID: 22347863]
  55. Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):3131-6 [PMID: 22323591]
  56. Trends Cogn Sci. 2018 Jan;22(1):21-31 [PMID: 29203085]
  57. Neuroimage. 2017 Jul 15;155:490-502 [PMID: 28412440]
  58. Phys Life Rev. 2020 Jul;33:75-77 [PMID: 31624013]
  59. Proc Natl Acad Sci U S A. 2023 Mar 28;120(13):e2218949120 [PMID: 36940333]
  60. Cereb Cortex. 2015 Jan;25(1):147-60 [PMID: 23960207]
  61. Nat Neurosci. 2014 Nov;17(11):1500-9 [PMID: 25151264]
  62. Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9566-9576 [PMID: 32284420]
  63. Nature. 2023 Jun;618(7965):566-574 [PMID: 37258669]
  64. Philos Trans A Math Phys Eng Sci. 2022 Jul 11;380(2227):20210247 [PMID: 35599554]
  65. PLoS One. 2015 Feb 18;10(2):e0118143 [PMID: 25693169]
  66. Neuropharmacology. 2018 Nov;142:167-178 [PMID: 29548884]
  67. Commun Biol. 2021 Mar 4;4(1):277 [PMID: 33664456]
  68. Neuroimage. 2018 Apr 15;170:332-347 [PMID: 28219775]
  69. Commun Biol. 2021 Aug 16;4(1):970 [PMID: 34400800]
  70. Phys Life Rev. 2020 Jul;33:34-54 [PMID: 31221604]
  71. Trends Cogn Sci. 2013 Dec;17(12):648-65 [PMID: 24210963]
  72. Cereb Cortex. 2014 Mar;24(3):663-76 [PMID: 23146964]
  73. Nat Commun. 2015 Jul 16;6:7751 [PMID: 26178017]
  74. Cell Rep. 2021 Aug 24;36(8):109554 [PMID: 34433059]
  75. Sci Rep. 2017 Jul 11;7(1):5135 [PMID: 28698644]

Word Cloud

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