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

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          Abstract

          Recent studies have started to elucidate the effects of lysergic acid diethylamide (LSD) on the human brain but the underlying dynamics are not yet fully understood. Here we used ’connectome-harmonic decomposition’, a novel method to investigate the dynamical changes in brain states. We found that LSD alters the energy and the power of individual harmonic brain states in a frequency-selective manner. Remarkably, this leads to an expansion of the repertoire of active brain states, suggestive of a general re-organization of brain dynamics given the non-random increase in co-activation across frequencies. Interestingly, the frequency distribution of the active repertoire of brain states under LSD closely follows power-laws indicating a re-organization of the dynamics at the edge of criticality. Beyond the present findings, these methods open up for a better understanding of the complex brain dynamics in health and disease.

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

          Robin Carhart-Harris, Robert Leech, Peter Hellyer … (2014)
          Entropy is a dimensionless quantity that is used for measuring uncertainty about the state of a system but it can also imply physical qualities, where high entropy is synonymous with high disorder. Entropy is applied here in the context of states of consciousness and their associated neurodynamics, with a particular focus on the psychedelic state. The psychedelic state is considered an exemplar of a primitive or primary state of consciousness that preceded the development of modern, adult, human, normal waking consciousness. Based on neuroimaging data with psilocybin, a classic psychedelic drug, it is argued that the defining feature of “primary states” is elevated entropy in certain aspects of brain function, such as the repertoire of functional connectivity motifs that form and fragment across time. Indeed, since there is a greater repertoire of connectivity motifs in the psychedelic state than in normal waking consciousness, this implies that primary states may exhibit “criticality,” i.e., the property of being poised at a “critical” point in a transition zone between order and disorder where certain phenomena such as power-law scaling appear. Moreover, if primary states are critical, then this suggests that entropy is suppressed in normal waking consciousness, meaning that the brain operates just below criticality. It is argued that this entropy suppression furnishes normal waking consciousness with a constrained quality and associated metacognitive functions, including reality-testing and self-awareness. It is also proposed that entry into primary states depends on a collapse of the normally highly organized activity within the default-mode network (DMN) and a decoupling between the DMN and the medial temporal lobes (which are normally significantly coupled). These hypotheses can be tested by examining brain activity and associated cognition in other candidate primary states such as rapid eye movement (REM) sleep and early psychosis and comparing these with non-primary states such as normal waking consciousness and the anaesthetized state.
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            Long-range temporal correlations and scaling behavior in human brain oscillations.

            Klaus Linkenkaer-Hansen, Vadim V Nikouline, J Matias Palva … (2001)
            The human brain spontaneously generates neural oscillations with a large variability in frequency, amplitude, duration, and recurrence. Little, however, is known about the long-term spatiotemporal structure of the complex patterns of ongoing activity. A central unresolved issue is whether fluctuations in oscillatory activity reflect a memory of the dynamics of the system for more than a few seconds. We investigated the temporal correlations of network oscillations in the normal human brain at time scales ranging from a few seconds to several minutes. Ongoing activity during eyes-open and eyes-closed conditions was recorded with simultaneous magnetoencephalography and electroencephalography. Here we show that amplitude fluctuations of 10 and 20 Hz oscillations are correlated over thousands of oscillation cycles. Our analyses also indicated that these amplitude fluctuations obey power-law scaling behavior. The scaling exponents were highly invariant across subjects. We propose that the large variability, the long-range correlations, and the power-law scaling behavior of spontaneous oscillations find a unifying explanation within the theory of self-organized criticality, which offers a general mechanism for the emergence of correlations and complex dynamics in stochastic multiunit systems. The demonstrated scaling laws pose novel quantitative constraints on computational models of network oscillations. We argue that critical-state dynamics of spontaneous oscillations may lend neural networks capable of quick reorganization during processing demands.
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              Psilocybin induces schizophrenia-like psychosis in humans via a serotonin-2 agonist action.

              Franz X. Vollenweider, Margreet F. I. Vollenweider-Scherpenhuyzen, Andreas Bäbler … (1998)
              Psilocybin, an indoleamine hallucinogen, produces a psychosis-like syndrome in humans that resembles first episodes of schizophrenia. In healthy human volunteers, the psychotomimetic effects of psilocybin were blocked dose-dependently by the serotonin-2A antagonist ketanserin or the atypical antipsychotic risperidone, but were increased by the dopamine antagonist and typical antipsychotic haloperidol. These data are consistent with animal studies and provide the first evidence in humans that psilocybin-induced psychosis is due to serotonin-2A receptor activation, independently of dopamine stimulation. Thus, serotonin-2A overactivity may be involved in the pathophysiology of schizophrenia and serotonin-2A antagonism may contribute to therapeutic effects of antipsychotics.
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                Author and article information

                Contributors
                Selen Atasoy:
                ORCID: http://orcid.org/0000-0002-8213-8462
                selenatasoy@gmail.com
                Journal
                Journal ID (nlm-ta): Sci Rep
                Journal ID (iso-abbrev): Sci Rep
                Title: Scientific Reports
                Publisher: Nature Publishing Group UK (London )
                ISSN (Electronic): 2045-2322
                Publication date (Electronic): 15 December 2017
                Publication date PMC-release: 15 December 2017
                Publication date Collection: 2017
                Volume: 7
                Electronic Location Identifier: 17661
                Affiliations
                [1 ]ISNI 0000 0001 2172 2676, GRID grid.5612.0, Center of Brain and Cognition, , Computational Neuroscience Group, Universitat Pompeu Fabra, ; Barcelona, Spain
                [2 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Psychedelic Research Group, , Psychopharmacology Unit, Centre for Psychiatry, Department of Medicine, Imperial College London, ; London, UK
                [3 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Department of Psychiatry, , University of Oxford, ; Oxford, UK
                [4 ]ISNI 0000 0001 1956 2722, GRID grid.7048.b, Center for Music in the Brain, , Clinical Medicine, Aarhus University, ; Aarhus, Denmark
                [5 ]ISNI 0000 0000 9601 989X, GRID grid.425902.8, Institució Catalana de la Recerca i Estudis Avançats (ICREA), ; Barcelona, Spain
                [6 ]ISNI 0000 0001 0041 5028, GRID grid.419524.f, Department of Neuropsychology, , Max Planck Institute for Human Cognitive and Brain Sciences, ; Leipzig, Germany
                [7 ]ISNI 0000 0004 1936 7857, GRID grid.1002.3, School of Psychological Sciences, , Monash University, ; Melbourne, Australia
                Author information
                http://orcid.org/0000-0002-8213-8462
                Article
                Publisher ID: 17546
                DOI: 10.1038/s41598-017-17546-0
                PMC ID: 5732294
                PubMed ID: 29247209
                SO-VID: 0c7ff47b-5c16-46c6-b270-4ed04e1d3f7c
                Copyright © © The Author(s) 2017
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                Date received : 26 July 2017
                Date accepted : 24 November 2017
                Categories
                Subject: Article
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                issue-copyright-statement © The Author(s) 2017

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