Neuroimaging & Brain MeasuresHealthy VolunteersPsilocybin

Broadband Cortical Desynchronization Underlies the Human Psychedelic State

Using MEG in healthy volunteers after intravenous psilocybin, the study shows broadband reductions in spontaneous cortical oscillatory power—especially in posterior association cortices and default‑mode network regions—while visually and motor‑induced gamma oscillations were preserved. Dynamic causal modelling indicates this desynchronisation is likely driven by 5‑HT2A‑mediated excitation of deep‑layer pyramidal neurons (notably in posterior cingulate cortex), linking cortical desynchronisation to the psychedelic state.

Authors

  • Suresh Muthukumaraswamy
  • Robin Carhart-Harris
  • David Nutt

Published

Journal of Neuroscience
individual Study

Abstract

Psychedelic drugs produce profound changes in consciousness, but the underlying neurobiological mechanisms for this remain unclear. Spontaneous and induced oscillatory activity was recorded in healthy human participants with magnetoencephalography after intravenous infusion of psilocybin—prodrug of the nonselective serotonin 2A receptor agonist and classic psychedelic psilocin. Psilocybin reduced spontaneous cortical oscillatory power from 1 to 50 Hz in posterior association cortices, and from 8 to 100 Hz in frontal association cortices. Large decreases in oscillatory power were seen in areas of the default-mode network. Independent component analysis was used to identify a number of resting-state networks, and activity in these was similarly decreased after psilocybin. Psilocybin had no effect on low-level visually induced and motor-induced gamma-band oscillations, suggesting that some basic elements of oscillatory brain activity are relatively preserved during the psychedelic experience. Dynamic causal modeling revealed that posterior cingulate cortex desynchronization can be explained by increased excitability of deep-layer pyramidal neurons, which are known to be rich in 5-HT2Areceptors. These findings suggest that the subjective effects of psychedelics result from a desynchronization of ongoing oscillatory rhythms in the cortex, likely triggered by 5-HT2Areceptor-mediated excitation of deep pyramidal cells.

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Research Summary of 'Broadband Cortical Desynchronization Underlies the Human Psychedelic State'

Introduction

Psychedelic drugs produce profound alterations of consciousness and have shown promise in a range of clinical and experimental settings, but the neural mechanisms that underlie these effects remain poorly understood. Previous human EEG studies and animal local field potential recordings have reported reduced cortical synchrony or high-frequency activity after psychedelic administration, and recent fMRI work has shown decreased blood flow in association cortices and subcortical structures after psilocybin. However, fMRI provides an indirect, slow measure of neural activity and EEG has limited spatial resolution and sensitivity to high-frequency components, leaving a gap in knowledge about broadband (1–100 Hz) electrophysiological changes during the acute psychedelic state. To address this gap, Muthukumaraswamy and colleagues used magnetoencephalography (MEG) to record spontaneous and stimulus-induced oscillatory activity in healthy volunteers during placebo and psilocybin infusion. The aims were to characterise broadband changes in oscillatory power and network-level activity, test whether low-level induced gamma responses were preserved, and use dynamic causal modelling (DCM) of source-level spectra to infer which cortical cell populations might mediate drug-induced desynchronization via 5-HT2A receptor mechanisms.

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Study Details

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Inhibition of alpha oscillations through serotonin-2A receptor activation underlies the visual effects of ayahuasca in humans

Valle, M., Maqueda, A. E., Rabella, M. et al. · European Neuropsychopharmacology (2016)

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LSD modulates music-induced imagery via changes in parahippocampal connectivity

Kaelen, M., Roseman, L., Kahan, J. et al. · European Neuropsychopharmacology (2016)

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The current state of research on ayahuasca: A systematic review of human studies assessing psychiatric symptoms, neuropsychological functioning, and neuroimaging

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LSD alters eyes-closed functional connectivity within the early visual cortex in a retinotopic fashion

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Neural correlates of the LSD experience revealed by multimodal neuroimaging

Carhart-Harris, R. L., Muthukumaraswamy, S., Roseman, L. et al. · PNAS (2016)

Increased global functional connectivity correlates with LSD-induced ego dissolution

Tagliazucchi, E., Roseman, L., Kaelen, M. et al. · Current Biology (2016)

Psychedelics

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The paradoxical psychological effects of lysergic acid diethylamide (LSD)

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The serotonergic hallucinogen 5-methoxy-N,N-dimethyltryptamine disrupts cortical activity in a regionally-selective manner via 5-HT1A and 5-HT2A receptors

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New World Tryptamine Hallucinogens and the Neuroscience of Ayahuasca

McKenna, D., Riba, J. · Current Topics in Behavioral Neurosciences (2016)

Serotonergic Hallucinogen-Induced Visual Perceptual Alterations

Kometer, M., Vollenweider, F. X. · Behavioral Neurobiology of Psychedelic Drugs (2016)

Acute Biphasic Effects of Ayahuasca

Schenberg, E. E., Alexandre, J. F. M., Filev, R. et al. · PLOS ONE (2015)

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Psilocybin-induced spiritual experiences and insightfulness are associated with synchronization of neuronal oscillations

Kometer, M., Pokorny, T., Seifritz, E. et al. · Psychopharmacology (2015)

Restructuring consciousness -the psychedelic state in light of integrated information theory

Gallimore, A. R. · Frontiers in Human Neuroscience (2015)

Finding the self by losing the self: Neural correlates of ego-dissolution under psilocybin

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Serotonergic psychedelics temporarily modify information transfer in humans

Alonso, J. N., Romero, S., Mañanas, M. A. et al. · International Journal of Neuropsychopharmacology (2015)

Long-term use of psychedelic drugs is associated with differences in brain structure and personality in humans

Rodríguez-Fornells, A., Ribeiro, S., Sanches, R. F. et al. · European Neuropsychopharmacology (2015)

Peak experiences and the afterglow phenomenon: when and how do therapeutic effects of hallucinogens depend on psychedelic experiences

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Classic psychedelic use is associated with reduced psychological distress and suicidality in the United States adult population

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Recent advances in the neuropsychopharmacology of serotonergic hallucinogens

Halberstadt, A. L. · Behavioural Brain Research (2014)

The effects of psilocybin and MDMA on between-network resting state functional connectivity in healthy volunteers

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The entropic brain: a theory of conscious states informed by neuroimaging research with psychedelic drugs

Carhart-Harris, R. L., Leech, R., Shanahan, M. et al. · Frontiers in Human Neuroscience (2014)

Psilocybin - Summary of knowledge and new perspectives

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