Journal Article

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

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

2019

Overview

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. [Display omitted] •Recurrent BOLD phase-locking (PL) states reveal canonical resting-state networks.•Psilocybin changes occupancy of two BOLD PL states compared to placebo.•Frontoparietal network occupancy negatively relates to subjective psychedelic scores.•The occurrence of all BOLD PL states is consistent at baseline over >1 week.•Results bridge molecular pharmacodynamics and whole-brain network dynamics.

• Publisher: Elsevier Inc,Elsevier Limited
• Subject: Adult / Brain research / Cerebral Cortex - diagnostic imaging / Cerebral Cortex - drug effects / Cerebral Cortex - physiology / Connectome / Datasets / Frequency dependence / Hallucinogens - administration & dosage / Hallucinogens - pharmacology / Humans / Image processing / Intravenous administration / Magnetic Resonance Imaging / Medical imaging / Nerve Net - diagnostic imaging / Nerve Net - drug effects / Nerve Net - physiology / Neural networks / Neuroimaging / Neuromodulation / Parietal Lobe / Partnership agreements / Pharmacodynamics / Prefrontal Cortex - diagnostic imaging / Prefrontal Cortex - drug effects / Prefrontal Cortex - physiology / Psilocybin / Psilocybin - administration & dosage / Psilocybin - pharmacology / Psychedelic drugs / Repertoire / Studies / Tryptamine / Young Adult