Dynamical exploration of the repertoire of brain networks at rest is modulated by psilocybin

Louis David Lord, Paul Expert, Selen Atasoy, Leor Roseman, Kristina Rapuano, Renaud Lambiotte, David J. Nutt, Gustavo Deco, Robin L. Carhart-Harris, Morten L. Kringelbach, Joana Cabral

Research output: Contribution to journalArticle

Abstract

Growing evidence from the dynamical analysis of functional neuroimaging data suggests that brain function can be understood as the exploration of a repertoire of metastable connectivity patterns (‘functional brain networks’), which potentially underlie different mental processes. The present study characterizes how the brain's dynamical exploration of resting-state networks is rapidly modulated by intravenous infusion of psilocybin, a tryptamine psychedelic found in “magic mushrooms”. We employed a data-driven approach to characterize recurrent functional connectivity patterns by focusing on the leading eigenvector of BOLD phase coherence at single-TR resolution. Recurrent BOLD phase-locking patterns (PL states) were assessed and statistically compared pre- and post-infusion of psilocybin in terms of their probability of occurrence and transition profiles. Results were validated using a placebo session. Recurrent BOLD PL states revealed high spatial overlap with canonical resting-state networks. Notably, a PL state forming a frontoparietal subsystem was strongly destabilized after psilocybin injection, with a concomitant increase in the probability of occurrence of another PL state characterized by global BOLD phase coherence. These findings provide evidence of network-specific neuromodulation by psilocybin and represent one of the first attempts at bridging molecular pharmacodynamics and whole-brain network dynamics.

Original languageEnglish
Pages (from-to)127-142
Number of pages16
JournalNeuroImage
Volume199
DOIs
Publication statusPublished - 1 Oct 2019

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Psilocybin
Brain
Mental Processes
Hallucinogens
Functional Neuroimaging
Magic
Agaricales
Intravenous Infusions
Placebos
Injections

Cite this

Lord, Louis David ; Expert, Paul ; Atasoy, Selen ; Roseman, Leor ; Rapuano, Kristina ; Lambiotte, Renaud ; Nutt, David J. ; Deco, Gustavo ; Carhart-Harris, Robin L. ; Kringelbach, Morten L. ; Cabral, Joana. / Dynamical exploration of the repertoire of brain networks at rest is modulated by psilocybin. In: NeuroImage. 2019 ; Vol. 199. pp. 127-142.
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abstract = "Growing evidence from the dynamical analysis of functional neuroimaging data suggests that brain function can be understood as the exploration of a repertoire of metastable connectivity patterns (‘functional brain networks’), which potentially underlie different mental processes. The present study characterizes how the brain's dynamical exploration of resting-state networks is rapidly modulated by intravenous infusion of psilocybin, a tryptamine psychedelic found in “magic mushrooms”. We employed a data-driven approach to characterize recurrent functional connectivity patterns by focusing on the leading eigenvector of BOLD phase coherence at single-TR resolution. Recurrent BOLD phase-locking patterns (PL states) were assessed and statistically compared pre- and post-infusion of psilocybin in terms of their probability of occurrence and transition profiles. Results were validated using a placebo session. Recurrent BOLD PL states revealed high spatial overlap with canonical resting-state networks. Notably, a PL state forming a frontoparietal subsystem was strongly destabilized after psilocybin injection, with a concomitant increase in the probability of occurrence of another PL state characterized by global BOLD phase coherence. These findings provide evidence of network-specific neuromodulation by psilocybin and represent one of the first attempts at bridging molecular pharmacodynamics and whole-brain network dynamics.",
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Lord, LD, Expert, P, Atasoy, S, Roseman, L, Rapuano, K, Lambiotte, R, Nutt, DJ, Deco, G, Carhart-Harris, RL, Kringelbach, ML & Cabral, J 2019, 'Dynamical exploration of the repertoire of brain networks at rest is modulated by psilocybin', NeuroImage, vol. 199, pp. 127-142. https://doi.org/10.1016/j.neuroimage.2019.05.060

Dynamical exploration of the repertoire of brain networks at rest is modulated by psilocybin. / Lord, Louis David; Expert, Paul; Atasoy, Selen; Roseman, Leor; Rapuano, Kristina; Lambiotte, Renaud; Nutt, David J.; Deco, Gustavo; Carhart-Harris, Robin L.; Kringelbach, Morten L.; Cabral, Joana.

In: NeuroImage, Vol. 199, 01.10.2019, p. 127-142.

Research output: Contribution to journalArticle

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AU - Lambiotte, Renaud

AU - Nutt, David J.

AU - Deco, Gustavo

AU - Carhart-Harris, Robin L.

AU - Kringelbach, Morten L.

AU - Cabral, Joana

N1 - Copyright © 2019 Elsevier Inc. All rights reserved.

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N2 - Growing evidence from the dynamical analysis of functional neuroimaging data suggests that brain function can be understood as the exploration of a repertoire of metastable connectivity patterns (‘functional brain networks’), which potentially underlie different mental processes. The present study characterizes how the brain's dynamical exploration of resting-state networks is rapidly modulated by intravenous infusion of psilocybin, a tryptamine psychedelic found in “magic mushrooms”. We employed a data-driven approach to characterize recurrent functional connectivity patterns by focusing on the leading eigenvector of BOLD phase coherence at single-TR resolution. Recurrent BOLD phase-locking patterns (PL states) were assessed and statistically compared pre- and post-infusion of psilocybin in terms of their probability of occurrence and transition profiles. Results were validated using a placebo session. Recurrent BOLD PL states revealed high spatial overlap with canonical resting-state networks. Notably, a PL state forming a frontoparietal subsystem was strongly destabilized after psilocybin injection, with a concomitant increase in the probability of occurrence of another PL state characterized by global BOLD phase coherence. These findings provide evidence of network-specific neuromodulation by psilocybin and represent one of the first attempts at bridging molecular pharmacodynamics and whole-brain network dynamics.

AB - Growing evidence from the dynamical analysis of functional neuroimaging data suggests that brain function can be understood as the exploration of a repertoire of metastable connectivity patterns (‘functional brain networks’), which potentially underlie different mental processes. The present study characterizes how the brain's dynamical exploration of resting-state networks is rapidly modulated by intravenous infusion of psilocybin, a tryptamine psychedelic found in “magic mushrooms”. We employed a data-driven approach to characterize recurrent functional connectivity patterns by focusing on the leading eigenvector of BOLD phase coherence at single-TR resolution. Recurrent BOLD phase-locking patterns (PL states) were assessed and statistically compared pre- and post-infusion of psilocybin in terms of their probability of occurrence and transition profiles. Results were validated using a placebo session. Recurrent BOLD PL states revealed high spatial overlap with canonical resting-state networks. Notably, a PL state forming a frontoparietal subsystem was strongly destabilized after psilocybin injection, with a concomitant increase in the probability of occurrence of another PL state characterized by global BOLD phase coherence. These findings provide evidence of network-specific neuromodulation by psilocybin and represent one of the first attempts at bridging molecular pharmacodynamics and whole-brain network dynamics.

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