4.8 Article

Receptor-informed network control theory links LSD and psilocybin to a flattening of the brain's control energy landscape

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NATURE COMMUNICATIONS
卷 13, 期 1, 页码 -

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NATURE PORTFOLIO
DOI: 10.1038/s41467-022-33578-1

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资金

  1. National Science Foundation Graduate Research Fellowship [DGE-1650441]
  2. Gates Cambridge Trust
  3. Alex Mosley Charitable Trust
  4. Centre for Psychedelic Research
  5. Crowd Funding Campaign
  6. Beckley Foundation, as part of the Beckley-Imperial Research Programme
  7. Spanish Ministry of Science and Innovation [BES-2017-080364]
  8. Edmond J. Safra Prof of Neuropsychopharmacology at Imperial College London
  9. Spanish Ministry of Science, Innovation and Universities (MCIU) [PID2019-105772GB-I00]
  10. State Research Agency (AEI)
  11. European Regional Development Funds (FEDER)
  12. HBP SGA3 Human Brain Project Specific Grant - EU H2020 FET Flagship program [945539]
  13. SGR Research Support Group support - Catalan Agency for Management of University and Research Grants (AGAUR) [2017 SGR 1545]
  14. Center for Music in the Brain - Danish National Research Foundation [DNRF117]
  15. Centre for Eudaimonia and Human Flourishing - Pettit Foundation
  16. Centre for Eudaimonia and Human Flourishing - Carlsberg Foundation
  17. Canadian Institute for Advanced Research (L'Institut Canadien de Recherches Avancees) [RCZB/072 RG93193]
  18. National Institutes of Health [RF1MH123232, R01NS102646, R21NS104634]
  19. Stephen Erskine Fellowship from Queens' College, Cambridge

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The authors used network control theory and functional MRI data to show that serotonergic psychedelic drugs like LSD and psilocybin flatten the dynamic landscape of the brain, allowing for easier state transitions and more diverse brain activity over time. These drugs alter subjective experience through serotonin 2a (5-HT2a) receptor agonism, which is associated with increased entropy in brain activity. This increase in entropy is hypothesized to be due to a flattening of the brain's control energy landscape, making transitions between brain states more energy efficient.
There are several models of how serotonergic psychedelic drugs affect brain activity. Here the authors use network control theory and functional MRI data to provide evidence that serotonin receptor agonists LSD and psilocybin flatten the brain's dynamic landscape, allowing for facile state transitions and more temporally diverse brain activity. Psychedelics including lysergic acid diethylamide (LSD) and psilocybin temporarily alter subjective experience through their neurochemical effects. Serotonin 2a (5-HT2a) receptor agonism by these compounds is associated with more diverse (entropic) brain activity. We postulate that this increase in entropy may arise in part from a flattening of the brain's control energy landscape, which can be observed using network control theory to quantify the energy required to transition between recurrent brain states. Using brain states derived from existing functional magnetic resonance imaging (fMRI) datasets, we show that LSD and psilocybin reduce control energy required for brain state transitions compared to placebo. Furthermore, across individuals, reduction in control energy correlates with more frequent state transitions and increased entropy of brain state dynamics. Through network control analysis that incorporates the spatial distribution of 5-HT2a receptors (obtained from publicly available positron emission tomography (PET) data under non-drug conditions), we demonstrate an association between the 5-HT2a receptor and reduced control energy. Our findings provide evidence that 5-HT2a receptor agonist compounds allow for more facile state transitions and more temporally diverse brain activity. More broadly, we demonstrate that receptor-informed network control theory can model the impact of neuropharmacological manipulation on brain activity dynamics.

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