Healthy VolunteersNeuroimaging & Brain MeasuresPsilocybin

Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin

Using arterial spin labelling and BOLD fMRI in healthy volunteers, intravenous psilocybin produced widespread decreases in cerebral blood flow and BOLD signal that were maximal in hub regions (thalamus, ACC, PCC and mPFC), with reduced mPFC activity predicting the intensity of subjective effects. The drug also decreased functional coupling between mPFC and PCC, suggesting psychedelic phenomenology arises from diminished activity and connectivity of key network hubs, permitting a state of unconstrained cognition.

Authors

  • Robin Carhart-Harris
  • David Nutt
  • David Erritzoe

Published

PNAS
individual Study

Abstract

Psychedelic drugs have a long history of use in healing ceremonies, but despite renewed interest in their therapeutic potential, we continue to know very little about how they work in the brain. Here we used psilocybin, a classic psychedelic found in magic mushrooms, and a task-free functional MRI (fMRI) protocol designed to capture the transition from normal waking consciousness to the psychedelic state. Arterial spin labeling perfusion and blood-oxygen level-dependent (BOLD) fMRI were used to map cerebral blood flow and changes in venous oxygenation before and after intravenous infusions of placebo and psilocybin. Fifteen healthy volunteers were scanned with arterial spin labeling and a separate 15 with BOLD. As predicted, profound changes in consciousness were observed after psilocybin, but surprisingly, only decreases in cerebral blood flow and BOLD signal were seen, and these were maximal in hub regions, such as the thalamus and anterior and posterior cingulate cortex (ACC and PCC). Decreased activity in the ACC/medial prefrontal cortex (mPFC) was a consistent finding and the magnitude of this decrease predicted the intensity of the subjective effects. Based on these results, a seed-based pharmaco-physiological interaction/functional connectivity analysis was performed using a medial prefrontal seed. Psilocybin caused a significant decrease in the positive coupling between the mPFC and PCC. These results strongly imply that the subjective effects of psychedelic drugs are caused by decreased activity and connectivity in the brain's key connector hubs, enabling a state of unconstrained cognition.

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Research Summary of 'Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin'

Introduction

Psychedelic drugs such as psilocybin have a long history of ritual and therapeutic use, yet their neural mechanisms remain poorly understood. Earlier work has characterised the phenomenology of psilocybin and implicated serotonergic (particularly 5-HT2A) receptors, but direct, high-resolution imaging of the transition from normal waking consciousness into the psychedelic state has been lacking. Carhart-Harris and colleagues set out to characterise the neural correlates of the acute psychedelic state using task-free functional MRI. They combined arterial spin labelling (ASL) perfusion and blood-oxygen-level-dependent (BOLD) fMRI to map cerebral blood flow (CBF) and BOLD changes before and after intravenous infusions of placebo and psilocybin, aiming to capture short‑latency, phasic effects produced by a 2 mg i.v. dose that begins acting within seconds and peaks within minutes. The study focused on resting-state activity and connectivity, with particular attention to high-level association regions and connector hubs such as the medial prefrontal cortex (mPFC), anterior cingulate cortex (ACC), posterior cingulate cortex (PCC) and thalamus.

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References (9)

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Hallucinogens in Mental Health: Preclinical and Clinical Studies on LSD, Psilocybin, MDMA, and Ketamine

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Pivotal Mental States

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Turn On, Tune In, Drop In: Psychedelics, Creativity and Entrepreneurship

Silver, L. S. · American Journal of Management (2020)

Serotonergic psychedelics LSD & psilocybin increase the fractal dimension of cortical brain activity in spatial and temporal domains

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Hallucinations Under Psychedelics and in the Schizophrenia Spectrum: An Interdisciplinary and Multiscale Comparison

Leptourgos, P., Fortier-Davy, M., Carhart-Harris, R. L. et al. · Schizophrenia Bulletin (2020)

Classic Psychedelics as a Psychotherapeutic Aid in the Treatment of Stimulant Use Disorder: a Case Report

Johnson, S., Black, Q. C. · International Journal of Mental Health and Addiction (2020)

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Vollenweider, F. X., Preller, K. H. · Nature Reviews Neuroscience (2020)

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A potential role for psilocybin in the treatment of obsessive-compulsive disorder

Jacobs, E. · Journal of Psychedelic Studies (2020)

Updating the dynamic framework of thought: Creativity and psychedelics

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Broadening Your Mind to Include Others: The relationship between serotonergic psychedelic experiences and maladaptive narcissism

Van Mulukom, V., Patterson, R. E., Van Elk, M. · Psychopharmacology (2020)

Ethics and ego dissolution: the case of psilocybin

Smith, W. R., Sisti, D. · Journal of Medical Ethics (2020)

Me, myself, bye: regional alterations in glutamate and the experience of ego dissolution with psilocybin

Mason, N. L., Kuypers, K. P. C., Reckweg, J. et al. · Neuropsychopharmacology (2020)

Psilocybin: from ancient magic to modern medicine

Nichols, D. E. · Journal of Antibiotics (2020)

Chronic pain and psychedelics: a review and proposed mechanism of action

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LSD flattens the functional hierarchy of the human brain

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Isness: Using Multi-Person VR to Design Peak Mystical Type Experiences Comparable to Psychedelics

Glowacki, D. R., Wonnacott, M. D., Freire, R. et al. · Association for Computing Machinery (2020)

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Subacute Effects of the Psychedelic Ayahuasca on the Salience and Default Mode Networks

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A single psilocybin dose is associated with long-term increased mindfulness, preceded by a proportional change in neocortical 5-HT2A receptor binding

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Decreased directed functional connectivity in the psychedelic state

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Natural Psychoplastogens As Antidepressant Agents

Benko, J., Vranková, S. · Molecules (2020)

Psychedelics and Psychedelic-Assisted Psychotherapy

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Emotions and brain function are altered up to one month after a single high dose of psilocybin

Barrett, F. S., Doss, M. K., Sepeda, N. D. et al. · Scientific Reports (2020)

Therapeutic Use of LSD in Psychiatry: A Systematic Review of Randomized-Controlled Clinical Trials

Fuentes, J. J., Fonseca, F., Elices, M. et al. · Frontiers in Psychiatry (2020)

Therapeutic mechanisms of psilocybin: Changes in amygdala and prefrontal functional connectivity during emotional processing after psilocybin for treatment-resistant depression

Mertens, L. J., Wall, M. B., Roseman, L. et al. · Journal of Psychopharmacology (2020)

155 cited
Long-term follow-up of psilocybin-assisted psychotherapy for psychiatric and existential distress in patients with life-threatening cancer

Agin-Liebes, G. I., Malone, T., Yalch, M. M. et al. · Journal of Psychopharmacology (2020)

292 cited
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Ho, J. T., Preller, K. H., Lenggenhager, B. · Neuroscience and Biobehavioral Reviews (2020)

Therapeutic use of serotoninergic hallucinogens: A review of the evidence and of the biological and psychological mechanisms

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Embedding existential psychology within psychedelic science: reduced death anxiety as a mediator of the therapeutic effects of psychedelics.

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

Lord, L. D., Expert, P., Atasoy, S. et al. · NeuroImage (2019)

183 cited
Spectral signatures of serotonergic psychedelics and glutamatergic dissociatives

Pallavicini, C., Vilas, M. G., Villarreal, M. et al. · NeuroImage (2019)

51 cited
Psilocybin-assisted mindfulness training modulates self-consciousness and brain default mode network connectivity with lasting effects

Smigielski, L., Scheidegger, M., Kometer, M. et al. · NeuroImage (2019)

REBUS and the Anarchic Brain: Toward a Unified Model of the Brain Action of Psychedelics

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Psychedelic drugs-a new era in psychiatry?

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Cessation and reduction in alcohol consumption and misuse after psychedelic use

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Kuypers, K. P. C. · Medical Hypotheses (2019)

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Russ, S. L., Carhart-Harris, R. L., Maruyama, G. et al. · Psychology of Consciousness Theory Research and Practice (2019)

Sub-Acute Effects of Psilocybin on Empathy, Creative Thinking, and Subjective Well-Being

Mason, N. L., Mischler, E., Uthaug, M. V. et al. · Journal of Psychoactive Drugs (2019)

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Psychedelic effects of psilocybin correlate with serotonin 2A receptor occupancy and plasma psilocin levels

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Psychiatry might need some psychedelic therapy

Johnson, M. W. · International Review of Psychiatry (2018)

Current perspectives on psychedelic therapy: use of serotonergic hallucinogens in clinical interventions

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Ketamine for the treatment of addiction: Evidence and potential mechanisms

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LSD modulates effective connectivity and neural adaptation mechanisms in an auditory oddball paradigm

Timmermann, C., Spriggs, M. J., Kaelen, M. et al. · Neuropharmacology (2018)

More realistic forecasting of future life events after psilocybin for treatment-resistant depression

Lyons, T., Carhart-Harris, R. L. · Frontiers in Psychology (2018)

49 cited
Psychedelics and music: neuroscience and therapeutic implications

Barrett, F. S., Preller, K. H., Kaelen, M. · International Review of Psychiatry (2018)

Psychedelics, meditation, and self-consciousness

Milliere, R., Carhart-Harris, R. L., Roseman, L. et al. · Frontiers in Psychology (2018)

Psychedelics as anti-inflammatory agents

Flanagan, T. W., Nichols, C. D. · International Review of Psychiatry (2018)

N, N-Dimethyltryptamine (DMT), an Endogenous Hallucinogen: Past, Present, and Future Research to Determine Its Role and Function

Barker, S. · Frontiers in Neuroscience (2018)

DARK Classics in Chemical Neuroscience: Psilocybin

Geiger, H. A., Wurst, M. G., Daniels, R. N. · ACS Chemical Neuroscience (2018)

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Out of the box: A psychedelic model to study the creative mind

Kuypers, K. P. C. · Medical Hypotheses (2018)

Psilocybin modulates functional connectivity of the amygdala during emotional face discrimination

Grimm, O., Kraehenmann, R., Preller, K. H. et al. · European Neuropsychopharmacology (2018)

Integrating Psychedelic Medicines and Psychiatry: Theory and Methods of a Model Clinic

Sloshower, J. A. · Plant Medicines Healing and Psychedelic Science (2018)

The Use of Salvia divinorum from a Mazatec Perspective

Maqueda, A. E. · Plant Medicines Healing and Psychedelic Science (2018)

Unifying theories of psychedelic drug effects

Swanson, L. R. · Frontiers in Pharmacology (2018)

Neuroendocrine Associations Underlying the Persistent Therapeutic Effects of Classic Serotonergic Psychedelics

Schindler, E. A. D., Wallace, R. M., Sloshower, J. A. et al. · Frontiers in Pharmacology (2018)

The psychedelic debriefing in alcohol dependence treatment: illustrating key change phenomena through qualitative content analysis of clinical sessions

Kraehenmann, R., Nielson, E. M., May, D. G. et al. · Frontiers in Pharmacology (2018)

The hidden therapist: evidence for a central role of music in psychedelic therapy

Kaelen, M., Giribaldi, B., Raine, J. et al. · Psychopharmacology (2018)

213 cited
The Experience Elicited by Hallucinogens Presents the Highest Similarity to Dreaming within a Large Database of Psychoactive Substance Reports

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Increased nature relatedness and decreased authoritarian political views after psilocybin for treatment-resistant depression

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Quality of acute psychedelic experience predicts therapeutic efficacy of psilocybin for treatment-resistant depression

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Implications for psychedelic-assisted psychotherapy: functional magnetic resonance imaging study with psilocybin

Carhart-Harris, R. L., Leech, R., Williams, T. M. et al. · British Journal of Psychiatry (2018)

202 cited
Psychiatry & the psychedelic drugs. Past, present & future

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Connectome-harmonic decomposition of human brain activity reveals dynamical repertoire re-organization under LSD

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The serotonin hallucinogen 5-MeO-DMT alters cortico-thalamic activity in freely moving mice: Regionally-selective involvement of 5-HT1A and 5-HT2A receptors

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LSD Increases Primary Process Thinking via Serotonin 2A Receptor Activation

Sumiyoshi, T., Kraehenmann, R., Pokorny, D. et al. · Frontiers in Pharmacology (2017)

Double-blind comparison of the two hallucinogens psilocybin and dextromethorphan: similarities and differences in subjective experiences

Carbonaro, T. M., Hurwitz, E., Johnson, M. W. · Psychopharmacology (2017)

102 cited
Psilocybin for treatment-resistant depression: fMRI-measured brain mechanisms

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Two dose investigation of the 5-HT-agonist psilocybin on relative and global cerebral blood flow

Lewis, C. R., Preller, K. H., Kraehenmann, R. et al. · NeuroImage (2017)

74 cited
The Mechanisms of Psychedelic Visionary Experiences: Hypotheses from Evolutionary Psychology

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Psychedelic Drugs in Biomedicine

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Does psychedelic drug use reduce risk of suicidality? Evidence from a longitudinal community-based cohort of marginalised women in a Canadian setting

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Psychedelic pleasures: An affective understanding of the joys of tripping

Bøhling, F. · International Journal of Drug Policy (2017)

Serotonin and brain function: a tale of two receptors

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Shannon entropy of brain functional complex networks under the influence of the psychedelic Ayahuasca

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Psychedelic drug use in healthy individuals: A review of benefits, costs, and implications for drug policy

Elsey, J. W. B. · Drug Science Policy and Law (2017)

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Developing Guidelines and Competencies for the Training of Psychedelic Therapists

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Assessing the psychedelic “after-glow” in ayahuasca users: post-acute neurometabolic and functional connectivity changes are associated with enhanced mindfulness capacities

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Potential Therapeutic Effects of Psilocybin

Johnson, M. W., Griffiths, R. R. · Neurotherapeutics (2017)

Looking for the Self: Phenomenology, Neurophysiology and Philosophical Significance of Drug-induced Ego Dissolution

Millière, R. · Frontiers in Human Neuroscience (2017)

Psilocybin-Assisted Therapy: A Review of a Novel Treatment for Psychiatric Disorders

Thomas, K., Malcolm, B., Lastra, D. · Journal of Psychoactive Drugs (2017)

Modern clinical research on LSD

Liechti, M. E. · Neuropsychopharmacology (2017)

The therapeutic potential of psychedelic drugs: past, present, and future

Carhart-Harris, R. L., Goodwin, G. M. · Neuropsychopharmacology (2017)

The psychological and human brain effects of music in combination with psychedelic drugs

Kaelen, M. · Imperial College London (2017)

5-HT2A Agonists: A Novel Therapy for Functional Neurological Disorders?

Bryson, A., Carter, O., Norman, T. et al. · International Journal of Neuropsychopharmacology (2017)

18 cited
The fibrinolytic system: A new target for treatment of depression with psychedelics

Idell, R. D., Florova, G., Komissarov, A. A. et al. · Medical Hypotheses (2017)

An online survey of tobacco smoking cessation associated with naturalistic psychedelic use

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117 cited
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Psilocybin produces substantial and sustained decreases in depression and anxiety in patients with life-threatening cancer

Griffiths, R. R., Johnson, M. W. · Journal of Psychopharmacology (2016)

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Psychedelics in the treatment of unipolar mood disorders: a systematic review

Rucker, J., Young, A. H., Jelen, L. A. et al. · Journal of Psychopharmacology (2016)

Psychedelics as Medicines: An Emerging New Paradigm

Nichols, C. D., Nichols, D. E., Johnson, M. W. · Clinical Pharmacology and Therapeutics (2016)

Development of a Psychotherapeutic Model for Psilocybin-Assisted Treatment of Alcoholism

Bogenschutz, M. P., Forcehimes, A. A. · Journal of Humanistic Psychology (2016)

Psilocybin for treating substance use disorders?

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Clinical Applications of Hallucinogens: A Review

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174 cited
Measuring the subjective: revisiting the psychometric properties of three rating scales that assess the acute effects of hallucinogens

Bouso, J. C., Pedrero-Pérez, E. J., Gandy, S. · Human Psychopharmacology (2016)

42 cited
Treating Addiction: Perspectives from EEG and Imaging Studies on Psychedelics

Tófoli, L. F., De Araujo, D. B. · International Review of Neurobiology (2016)

A Model for the Application of Target-Controlled Intravenous Infusion for a Prolonged Immersive DMT Psychedelic Experience

Gallimore, A. R., Strassman, R. J. · Frontiers in Pharmacology (2016)

29 cited
LSD modulates music-induced imagery via changes in parahippocampal connectivity

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

Psilocybin with psychological support for treatment-resistant depression: an open-label feasibility study

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1174 cited
Ego-dissolution and psychedelics: validation of the ego-dissolution inventory (EDI)

Nour, M. R., Evans, J., Nutt, D. J. et al. · Frontiers in Human Neuroscience (2016)

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

Dos Santos, R. G., Balthazar, F. M., Bouso, J. C. et al. · Journal of Psychopharmacology (2016)

LSD-induced entropic brain activity predicts subsequent personality change

Lebedev, A. V., Kaelen, M., L€ Ovd En, M. et al. · Human Brain Mapping (2016)

292 cited
Effects of serotonin 2A/1A receptor stimulation on social exclusion processing

Preller, K. H., Pokorny, D., Hock, A. et al. · PNAS (2016)

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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)

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Antidepressive, anxiolytic, and antiaddictive effects of ayahuasca, psilocybin and lysergic acid diethylamide (LSD): a systematic review of clinical trials published in the last 25 years

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248 cited
Decreased mental time travel to the past correlates with default-mode network disintegration under lysergic acid diethylamide

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113 cited
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130 cited
The paradoxical psychological effects of lysergic acid diethylamide (LSD)

Carhart-Harris, R. L., Kaelen, M., Bolstridge, M. et al. · Psychological Medicine (2016)

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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)

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Psilocybin-induced decrease in amygdala reactivity correlates with enhanced positive mood in healthy volunteers

Kraehenmann, R., Preller, K. H., Scheidegger, M. et al. · Biological Psychiatry (2015)

LSD enhances the emotional response to music

Kaelen, M., Barrett, F. S., Roseman, L. et al. · Psychopharmacology (2015)

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

Lebedev, A. V., L€ Ovd En, M., Rosenthal, G. et al. · Human Brain Mapping (2015)

Serotonergic psychedelics temporarily modify information transfer in humans

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

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Psilocybin-occasioned mystical experiences in the treatment of tobacco addiction

Garcia-Romeu, A., Griffiths, R. R., Johnson, M. W. · Current Drug Abuse Reviews (2015)

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

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A qualitative report on the subjective experience of intravenous psilocybin administered in an FMRI environment

Nutt, D. J., Carhart-Harris, R. L. · Current Drug Abuse Reviews (2015)

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Hendricks, P. S., Thorne, C. B., Clark, B. et al. · Journal of Psychopharmacology (2015)

345 cited
Psilocybin-assisted treatment for alcohol dependence: a proof-of-concept study

Bogenschutz, M. P., Forcehimes, A. A., Pommy, J. A. et al. · Journal of Psychopharmacology (2015)

LSD-assisted psychotherapy for anxiety associated with a life-threatening disease: a qualitative study of acute and sustained subjective effects

Kirchner, K. · Journal of Psychopharmacology (2014)

389 cited
Drug models of schizophrenia

Steeds, H., Carhart-Harris, R. L., Stone, J. M. · Therapeutic Advances in Psychopharmacology (2014)

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Recent advances in the neuropsychopharmacology of serotonergic hallucinogens

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

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Pharmacology of Hallucinations: Several Mechanisms for One Single Symptom?

Rolland, B., Jardri, R., Amad, A. et al. · BioMed Research International (2014)

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

Roseman, L., Leech, R., Feilding, A. et al. · Frontiers in Human Neuroscience (2014)

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Classical hallucinogens as antidepressants? A review of pharmacodynamics and putative clinical roles

Tracy, D., Baumeister, D., Barnes, G. et al. · Therapeutic Advances in Psychopharmacology (2014)

Why Psychiatry Needs Psychedelics and Psychedelics Need Psychiatry

Sessa, B. · Journal of Psychoactive Drugs (2014)

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)

Hallucinogen use predicts reduced recidivism among substance-involved offenders under community corrections supervision

Hendricks, P. S., Clark, B., Johnson, M. W. et al. · Journal of Psychopharmacology (2014)

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Psilocybin - Summary of knowledge and new perspectives

Tylš, F., Páleníček, T., Horacek, J. · European Neuropsychopharmacology (2013)

Serotonergic hyperactivity as a potential factor in developmental, acquired and drug-induced synesthesia

Brogaard, B. · Frontiers in Human Neuroscience (2013)

Broadband Cortical Desynchronization Underlies the Human Psychedelic State

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Neural correlates of the psychedelic state as... — Research Summary & Context | Blossom