Research Article
Enhanced repertoire of brain dynamical states during the psychedelic experience
Abstract
The study of rapid changes in brain dynamics and functional connectivity (FC) is of increasing interest in neuroimaging. Brain states departing from normal waking consciousness are expected to be accompanied by alterations in the aforementioned dynamics. In particular, the psychedelic experience produced by psilocybin (a substance found in “magic mushrooms”) is characterized by unconstrained cognition and profound alterations in the perception of time, space and selfhood. Considering the spontaneous and subjective manifestation of these effects, we hypothesize that neural correlates of the psychedelic experience can be found in the dynamics and variability of spontaneous brain activity fluctuations and connectivity, measurable with functional Magnetic Resonance Imaging (fMRI). Fifteen healthy subjects were scanned before, during and after intravenous infusion of psilocybin and an inert placebo. Blood‐Oxygen Level Dependent (BOLD) temporal variability was assessed computing the variance and total spectral power, resulting in increased signal variability bilaterally in the hippocampi and anterior cingulate cortex. Changes in BOLD signal spectral behavior (including spectral scaling exponents) affected exclusively higher brain systems such as the default mode, executive control, and dorsal attention networks. A novel framework enabled us to track different connectivity states explored by the brain during rest. This approach revealed a wider repertoire of connectivity states post‐psilocybin than during control conditions. Together, the present results provide a comprehensive account of the effects of psilocybin on dynamical behavior in the human brain at a macroscopic level and may have implications for our understanding of the unconstrained, hyper‐associative quality of consciousness in the psychedelic state. Hum Brain Mapp 35:5442–5456, 2014. © 2014 Wiley Periodicals, Inc.
Citing Literature
Number of times cited: 57
- Franz X. Vollenweider and Katrin H. Preller, Neurobiologische Grundlagen der Wirkung von Psychedelika, Handbuch Psychoaktive Substanzen, 10.1007/978-3-642-55125-3_70, (423-436), (2017).
- Rainer Kraehenmann, Dan Pokorny, Leonie Vollenweider, Katrin H. Preller, Thomas Pokorny, Erich Seifritz and Franz X. Vollenweider, Dreamlike effects of LSD on waking imagery in humans depend on serotonin 2A receptor activation, Psychopharmacology, 10.1007/s00213-017-4610-0, 234, 13, (2031-2046), (2017).
- Franz X. Vollenweider and Katrin H. Preller, Neurobiologische Grundlagen der Wirkung von Psychedelika, Handbuch Psychoaktive Substanzen, 10.1007/978-3-642-55214-4_70-1, (1-18), (2017).
- A. Viol, Fernanda Palhano-Fontes, Heloisa Onias, Draulio B. de Araujo and G. M. Viswanathan, Shannon entropy of brain functional complex networks under the influence of the psychedelic Ayahuasca, Scientific Reports, 10.1038/s41598-017-06854-0, 7, 1, (2017).
- Michael P. Bogenschutz and Alyssa A. Forcehimes, Development of a Psychotherapeutic Model for Psilocybin-Assisted Treatment of Alcoholism, Journal of Humanistic Psychology, 57, 4, (389), (2017).
- Aaron Kucyi, Just a thought: How mind-wandering is represented in dynamic brain connectivity, NeuroImage, 10.1016/j.neuroimage.2017.07.001, (2017).
- Michael M. Schartner, Robin L. Carhart-Harris, Adam B. Barrett, Anil K. Seth and Suresh D. Muthukumaraswamy, Increased spontaneous MEG signal diversity for psychoactive doses of ketamine, LSD and psilocybin, Scientific Reports, 7, (46421), (2017).
- Selen Atasoy, Leor Roseman, Mendel Kaelen, Morten L. Kringelbach, Gustavo Deco and Robin L. Carhart-Harris, Connectome-harmonic decomposition of human brain activity reveals dynamical repertoire re-organization under LSD, Scientific Reports, 7, 1, (2017).
- Frederick S. Barrett and Roland R. Griffiths, Classic Hallucinogens and Mystical Experiences: Phenomenology and Neural Correlates, , 10.1007/7854_2017_474, (2017).
- RL Carhart-Harris and DJ Nutt, Serotonin and brain function: a tale of two receptors, Journal of Psychopharmacology, 10.1177/0269881117725915, 31, 9, (1091-1120), (2017).
- Cherise Rosen, Nev Jones, Kayla A. Chase, Jennifer K. Melbourne, Linda S. Grossman and Rajiv P. Sharma, Immersion in altered experience: An investigation of the relationship between absorption and psychopathology, Consciousness and Cognition, 49, (215), (2017).
- Frederic Sampedro, Mario de la Fuente Revenga, Marta Valle, Natalia Roberto, Elisabet Domínguez-Clavé, Matilde Elices, Luís Eduardo Luna, José Alexandre S Crippa, Jaime E C Hallak, Draulio B de Araujo, Pablo Friedlander, Steven A Barker, Enrique Álvarez, Joaquim Soler, Juan C Pascual, Amanda Feilding and Jordi Riba, Assessing the Psychedelic “After-Glow” in Ayahuasca Users: Post-Acute Neurometabolic and Functional Connectivity Changes Are Associated with Enhanced Mindfulness Capacities, International Journal of Neuropsychopharmacology, 10.1093/ijnp/pyx036, 20, 9, (698-711), (2017).
- Garth J. Thompson, Neural and metabolic basis of dynamic resting state fMRI, NeuroImage, 10.1016/j.neuroimage.2017.09.010, (2017).
- Evan J. Kyzar, Charles D. Nichols, Raul R. Gainetdinov, David E. Nichols and Allan V. Kalueff, Psychedelic Drugs in Biomedicine, Trends in Pharmacological Sciences, 10.1016/j.tips.2017.08.003, 38, 11, (992-1005), (2017).
- Peter Csermely, The Network Concept of Creativity and Deep Thinking: Applications to Social Opinion Formation and Talent Support, Gifted Child Quarterly, 61, 3, (194), (2017).
- James W.B. Elsey, Psychedelic drug use in healthy individuals: A review of benefits, costs, and implications for drug policy, Drug Science, Policy and Law, 3, (205032451772323), (2017).
- Maria Giulia Preti, Thomas AW Bolton and Dimitri Van De Ville, The dynamic functional connectome: State-of-the-art and perspectives, NeuroImage, 160, (41), (2017).
- Federico Cavanna, Martina G. Vilas, Matías Palmucci and Enzo Tagliazucchi, Dynamic functional connectivity and brain metastability during altered states of consciousness, NeuroImage, 10.1016/j.neuroimage.2017.09.065, (2017).
- A.V. Lebedev, M. Kaelen, M. Lövdén, J. Nilsson, A. Feilding, D.J. Nutt and R.L. Carhart‐Harris, LSD‐induced entropic brain activity predicts subsequent personality change, Human Brain Mapping, 37, 9, (3203-3213), (2016).
- José Carlos Bouso, Eduardo José Pedrero‐Pérez, Sam Gandy and Miguel Ángel Alcázar‐Córcoles, Measuring the subjective: revisiting the psychometric properties of three rating scales that assess the acute effects of hallucinogens, Human Psychopharmacology: Clinical and Experimental, 31, 5, (356-372), (2016).
- Anna Abraham, The imaginative mind, Human Brain Mapping, 37, 11, (4197-4211), (2016).
- Michael P. Bogenschutz and Matthew W. Johnson, Classic hallucinogens in the treatment of addictions, Progress in Neuro-Psychopharmacology and Biological Psychiatry, 64, (250), (2016).
- Chris Letheby, The epistemic innocence of psychedelic states, Consciousness and Cognition, 39, (28), (2016).
- Michael P. Bogenschutz and Stephen Ross, Therapeutic Applications of Classic Hallucinogens, , 10.1007/7854_2016_464, (2017).
- Robin L. Carhart-Harris, Suresh Muthukumaraswamy, Leor Roseman, Mendel Kaelen, Wouter Droog, Kevin Murphy, Enzo Tagliazucchi, Eduardo E. Schenberg, Timothy Nest, Csaba Orban, Robert Leech, Luke T. Williams, Tim M. Williams, Mark Bolstridge, Ben Sessa, John McGonigle, Martin I. Sereno, David Nichols, Peter J. Hellyer, Peter Hobden, John Evans, Krish D. Singh, Richard G. Wise, H. Valerie Curran, Amanda Feilding and David J. Nutt, Neural correlates of the LSD experience revealed by multimodal neuroimaging, Proceedings of the National Academy of Sciences, 10.1073/pnas.1518377113, 113, 17, (4853-4858), (2016).
- L.F. Tófoli and D.B. de Araujo, Treating Addiction, Imaging the Addicted Brain, 10.1016/bs.irn.2016.06.005, (157-185), (2016).
- Katrin H. Preller and Franz X. Vollenweider, Phenomenology, Structure, and Dynamic of Psychedelic States, , 10.1007/7854_2016_459, (2016).
- Charlotte Walsh, Psychedelics and cognitive liberty: Reimagining drug policy through the prism of human rights, International Journal of Drug Policy, 29, (80), (2016).
- Ralf-Peter Behrendt, Hallucinatory experience as aberrant event memory formation: Implications for the pathophysiology of schizophrenia, Progress in Neuro-Psychopharmacology and Biological Psychiatry, 71, (203), (2016).
- Enzo Tagliazucchi, Nicolas Crossley, Edward T. Bullmore and Helmut Laufs, Deep sleep divides the cortex into opposite modes of anatomical–functional coupling, Brain Structure and Function, 221, 8, (4221), (2016).
- Vince D. Calhoun and Tulay Adali, Time-Varying Brain Connectivity in fMRI Data: Whole-brain data-driven approaches for capturing and characterizing dynamic states, IEEE Signal Processing Magazine, 10.1109/MSP.2015.2478915, 33, 3, (52-66), (2016).
- Aaron Kucyi, Michael J. Hove, Michael Esterman, R. Matthew Hutchison and Eve M. Valera, Dynamic Brain Network Correlates of Spontaneous Fluctuations in Attention, Cerebral Cortex, (bhw029), (2016).
- Richard F. Betzel, Makoto Fukushima, Ye He, Xi-Nian Zuo and Olaf Sporns, Dynamic fluctuations coincide with periods of high and low modularity in resting-state functional brain networks, NeuroImage, 127, (287), (2016).
- Matthew M. Nour, Lisa Evans, David Nutt and Robin L. Carhart-Harris, Ego-Dissolution and Psychedelics: Validation of the Ego-Dissolution Inventory (EDI), Frontiers in Human Neuroscience, 10, (2016).
- Mendel Kaelen, Leor Roseman, Joshua Kahan, Andre Santos-Ribeiro, Csaba Orban, Romy Lorenz, Frederick S. Barrett, Mark Bolstridge, Tim Williams, Luke Williams, Matthew B. Wall, Amanda Feilding, Suresh Muthukumaraswamy, David J. Nutt and Robin Carhart-Harris, LSD modulates music-induced imagery via changes in parahippocampal connectivity, European Neuropsychopharmacology, 10.1016/j.euroneuro.2016.03.018, 26, 7, (1099-1109), (2016).
- R. L. Carhart-Harris, M. Kaelen, M. Bolstridge, T. M. Williams, L. T. Williams, R. Underwood, A. Feilding and D. J. Nutt, The paradoxical psychological effects of lysergic acid diethylamide (LSD), Psychological Medicine, 46, 07, (1379), (2016).
- Enzo Tagliazucchi, Leor Roseman, Mendel Kaelen, Csaba Orban, Suresh D. Muthukumaraswamy, Kevin Murphy, Helmut Laufs, Robert Leech, John McGonigle, Nicolas Crossley, Edward Bullmore, Tim Williams, Mark Bolstridge, Amanda Feilding, David J. Nutt and Robin Carhart-Harris, Increased Global Functional Connectivity Correlates with LSD-Induced Ego Dissolution, Current Biology, 26, 8, (1043), (2016).
- Andrew R. Gallimore and Rick J. Strassman, A Model for the Application of Target-Controlled Intravenous Infusion for a Prolonged Immersive DMT Psychedelic Experience, Frontiers in Pharmacology, 7, (2016).
- R. Matthew Hutchison and J. Bruce Morton, It's a matter of time: Reframing the development of cognitive control as a modification of the brain's temporal dynamics, Developmental Cognitive Neuroscience, 10.1016/j.dcn.2015.08.006, 18, (70-77), (2016).
- Rafael G. dos Santos, Flávia L. Osório, José Alexandre S. Crippa and Jaime E.C. Hallak, Classical hallucinogens and neuroimaging: A systematic review of human studies, Neuroscience & Biobehavioral Reviews, 10.1016/j.neubiorev.2016.10.026, 71, (715-728), (2016).
- Rafael G. dos Santos, Flávia L. Osório, José Alexandre S. Crippa, Jordi Riba, Antônio W. Zuardi and Jaime E. C. Hallak, 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, Therapeutic Advances in Psychopharmacology, 10.1177/2045125316638008, 6, 3, (193-213), (2016).
- Albert C. Yang, Chen‐Jee Hong, Yin‐Jay Liou, Kai‐Lin Huang, Chu‐Chung Huang, Mu‐En Liu, Men‐Tzung Lo, Norden E. Huang, Chung‐Kang Peng, Ching‐Po Lin and Shih‐Jen Tsai, Decreased resting‐state brain activity complexity in schizophrenia characterized by both increased regularity and randomness, Human Brain Mapping, 36, 6, (2174-2186), (2015).
- Alexander V. Lebedev, Martin Lövdén, Gidon Rosenthal, Amanda Feilding, David J. Nutt and Robin L. Carhart‐Harris, Finding the self by losing the self: Neural correlates of ego‐dissolution under psilocybin, Human Brain Mapping, 36, 8, (3137-3153), (2015).
- Amanda Elton and Wei Gao, Task‐related modulation of functional connectivity variability and its behavioral correlations, Human Brain Mapping, 36, 8, (3260-3272), (2015).
- Peter S Hendricks, Christopher B Thorne, C Brendan Clark, David W Coombs and Matthew W Johnson, Classic psychedelic use is associated with reduced psychological distress and suicidality in the United States adult population, Journal of Psychopharmacology, 10.1177/0269881114565653, 29, 3, (280-288), (2015).
- Ibai Diez, Asier Erramuzpe, Iñaki Escudero, Beatriz Mateos, Alberto Cabrera, Daniele Marinazzo, Ernesto J. Sanz-Arigita, Sebastiano Stramaglia and Jesus M. Cortes Diaz, Information Flow Between Resting-State Networks, Brain Connectivity, 10.1089/brain.2014.0337, 5, 9, (554-564), (2015).
- Andrew R. Gallimore, Restructuring consciousness –the psychedelic state in light of integrated information theory, Frontiers in Human Neuroscience, 9, (2015).
- Enzo Tagliazucchi and Helmut Laufs, Multimodal Imaging of Dynamic Functional Connectivity, Frontiers in Neurology, 6, (2015).
- Vince D. Calhoun, Robyn Miller, Godfrey Pearlson and Tulay Adalı, The Chronnectome: Time-Varying Connectivity Networks as the Next Frontier in fMRI Data Discovery, Neuron, 10.1016/j.neuron.2014.10.015, 84, 2, (262-274), (2014).
- Robyn L. Miller, Erik B. Erhardt, Oktay Agcaoglu, Elena A. Allen, Andrew M. Michael, Jessica A. Turner, Juan Bustillo, Judith M. Ford, Daniel H. Mathalon, Theo G. M. Van Erp, Steven Potkin, Adrian Preda, Godfrey Pearlson and Vince D. Calhoun, Multidimensional frequency domain analysis of full-volume fMRI reveals significant effects of age, gender, and mental illness on the spatiotemporal organization of resting-state brain activity, Frontiers in Neuroscience, 10.3389/fnins.2015.00203, 9, (2015).
- Selen Atasoy, Gustavo Deco, Morten L. Kringelbach and Joel Pearson, Harmonic Brain Modes: A Unifying Framework for Linking Space and Time in Brain Dynamics, The Neuroscientist, 10.1177/1073858417728032, (107385841772803), (2017).
- Enzo Tagliazucchi, Michael Siniatchkin, Helmut Laufs and Dante R. Chialvo, The Voxel-Wise Functional Connectome Can Be Efficiently Derived from Co-activations in a Sparse Spatio-Temporal Point-Process, Frontiers in Neuroscience, 10.3389/fnins.2016.00381, 10, (2016).
- Michael J. Winkelman, The Mechanisms of Psychedelic Visionary Experiences: Hypotheses from Evolutionary Psychology, Frontiers in Neuroscience, 10.3389/fnins.2017.00539, 11, (2017).
- Camila Sanz and Enzo Tagliazucchi, The Experience Elicited by Hallucinogens Presents the Highest Similarity to Dreaming within a Large Database of Psychoactive Substance Reports, Frontiers in Neuroscience, 10.3389/fnins.2018.00007, 12, (2018).
- Tomas Ros, Bernard J. Baars, Ruth A. Lanius and Patrik Vuilleumier, Tuning pathological brain oscillations with neurofeedback: a systems neuroscience framework, Frontiers in Human Neuroscience, 10.3389/fnhum.2014.01008, 8, (2014).
- Carmen Alonso-Montes, Ibai Diez, Lakhdar Remaki, Iñaki Escudero, Beatriz Mateos, Yves Rosseel, Daniele Marinazzo, Sebastiano Stramaglia and Jesus M. Cortes, Lagged and instantaneous dynamical influences related to brain structural connectivity, Frontiers in Psychology, 10.3389/fpsyg.2015.01024, 6, (2015).
- Helmut Laufs, Roman Rodionov, Rachel Thornton, John Sydney Duncan, Louis Lemieux and Enzo Tagliazucchi, Altered fMRI Connectivity Dynamics in Temporal Lobe Epilepsy Might Explain Seizure Semiology, Frontiers in Neurology, 10.3389/fneur.2014.00175, 5, (2014).
