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

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      Abstract

      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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      A default mode of brain function.

      A baseline or control state is fundamental to the understanding of most complex systems. Defining a baseline state in the human brain, arguably our most complex system, poses a particular challenge. Many suspect that left unconstrained, its activity will vary unpredictably. Despite this prediction we identify a baseline state of the normal adult human brain in terms of the brain oxygen extraction fraction or OEF. The OEF is defined as the ratio of oxygen used by the brain to oxygen delivered by flowing blood and is remarkably uniform in the awake but resting state (e.g., lying quietly with eyes closed). Local deviations in the OEF represent the physiological basis of signals of changes in neuronal activity obtained with functional MRI during a wide variety of human behaviors. We used quantitative metabolic and circulatory measurements from positron-emission tomography to obtain the OEF regionally throughout the brain. Areas of activation were conspicuous by their absence. All significant deviations from the mean hemisphere OEF were increases, signifying deactivations, and resided almost exclusively in the visual system. Defining the baseline state of an area in this manner attaches meaning to a group of areas that consistently exhibit decreases from this baseline, during a wide variety of goal-directed behaviors monitored with positron-emission tomography and functional MRI. These decreases suggest the existence of an organized, baseline default mode of brain function that is suspended during specific goal-directed behaviors.
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        The human brain is intrinsically organized into dynamic, anticorrelated functional networks.

        During performance of attention-demanding cognitive tasks, certain regions of the brain routinely increase activity, whereas others routinely decrease activity. In this study, we investigate the extent to which this task-related dichotomy is represented intrinsically in the resting human brain through examination of spontaneous fluctuations in the functional MRI blood oxygen level-dependent signal. We identify two diametrically opposed, widely distributed brain networks on the basis of both spontaneous correlations within each network and anticorrelations between networks. One network consists of regions routinely exhibiting task-related activations and the other of regions routinely exhibiting task-related deactivations. This intrinsic organization, featuring the presence of anticorrelated networks in the absence of overt task performance, provides a critical context in which to understand brain function. We suggest that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain.
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          Self-organized criticality: An explanation of the 1/fnoise

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            Author and article information

            Affiliations
            1Division of Brain Sciences, Department of Medicine, Centre for Neuropsychopharmacology, Imperial College London London, UK
            2C3NL, Division of Brain Sciences, Department of Medicine, Imperial College London London, UK
            3Department of Computing, Imperial College London London, UK
            4The Beckley Foundation, Beckley Park Oxford, UK
            5Neurology Department and Brain Imaging Center, Goethe University Frankfurt am Main, Germany
            6Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET) Buenos Aires, Argentina
            Author notes

            Edited by: Nikolai Axmacher, University of Bonn, Germany

            Reviewed by: Samantha J. Brooks, Uppsala University, Sweden; Katherine MacLean, Johns Hopkins University School of Medicine, USA

            *Correspondence: Robin L. Carhart-Harris, Division of Brain Sciences, Department of Medicine, Centre for Neuropsychopharmacology, Imperial College London, Burlington Danes building, Du Cane Rd., W12 0NN London, UK e-mail: r.carhart-harris@ 123456imperial.ac.uk

            This article was submitted to the journal Frontiers in Human Neuroscience.

            Journal
            Front Hum Neurosci
            Front Hum Neurosci
            Front. Hum. Neurosci.
            Frontiers in Human Neuroscience
            Frontiers Media S.A.
            1662-5161
            03 February 2014
            2014
            : 8
            3909994
            10.3389/fnhum.2014.00020
            Copyright © 2014 Carhart-Harris, Leech, Hellyer, Shanahan, Feilding, Tagliazucchi, Chialvo and Nutt.

            This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

            Counts
            Figures: 8, Tables: 0, Equations: 0, References: 218, Pages: 22, Words: 20470
            Categories
            Neuroscience
            Hypothesis and Theory Article

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