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      Spontaneous electrical low-frequency oscillations: a possible role in Hydra and all living systems

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          Abstract

          As one of the first model systems in biology, the basal metazoan Hydra has been revealing fundamental features of living systems since it was first discovered by Antonie van Leeuwenhoek in the early eighteenth century. While it has become well-established within cell and developmental biology, this tiny freshwater polyp is only now being re-introduced to modern neuroscience where it has already produced a curious finding: the presence of low-frequency spontaneous neural oscillations at the same frequency as those found in the default mode network in the human brain. Surprisingly, increasing evidence suggests such spontaneous electrical low-frequency oscillations (SELFOs) are found across the wide diversity of life on Earth, from bacteria to humans. This paper reviews the evidence for SELFOs in diverse phyla, beginning with the importance of their discovery in Hydra, and hypothesizes a potential role as electrical organism organizers, which supports a growing literature on the role of bioelectricity as a ‘template’ for developmental memory in organism regeneration.

          This article is part of the theme issue ‘Basal cognition: conceptual tools and the view from the single cell’.

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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 free-energy principle: a unified brain theory?

            A free-energy principle has been proposed recently that accounts for action, perception and learning. This Review looks at some key brain theories in the biological (for example, neural Darwinism) and physical (for example, information theory and optimal control theory) sciences from the free-energy perspective. Crucially, one key theme runs through each of these theories - optimization. Furthermore, if we look closely at what is optimized, the same quantity keeps emerging, namely value (expected reward, expected utility) or its complement, surprise (prediction error, expected cost). This is the quantity that is optimized under the free-energy principle, which suggests that several global brain theories might be unified within a free-energy framework.
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              The brain's default mode network.

              The brain's default mode network consists of discrete, bilateral and symmetrical cortical areas, in the medial and lateral parietal, medial prefrontal, and medial and lateral temporal cortices of the human, nonhuman primate, cat, and rodent brains. Its discovery was an unexpected consequence of brain-imaging studies first performed with positron emission tomography in which various novel, attention-demanding, and non-self-referential tasks were compared with quiet repose either with eyes closed or with simple visual fixation. The default mode network consistently decreases its activity when compared with activity during these relaxed nontask states. The discovery of the default mode network reignited a longstanding interest in the significance of the brain's ongoing or intrinsic activity. Presently, studies of the brain's intrinsic activity, popularly referred to as resting-state studies, have come to play a major role in studies of the human brain in health and disease. The brain's default mode network plays a central role in this work.
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                Author and article information

                Contributors
                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                March 15, 2021
                January 25, 2021
                January 25, 2021
                : 376
                : 1820 , Theme issue ‘Basal cognition: conceptual tools and the view from the single cell’ compiled and edited by Pamela Lyon, Fred Keijzer, Detlev Arendt and Michael Levin
                : 20190763
                Affiliations
                [ 1 ]Neurotechnology Center, Department of Biological Sciences, Columbia University , New York, NY, USA
                [ 2 ]Department of Psychiatry, New York State Psychiatric Institute, Columbia University , New York, NY, USA
                Author notes

                One contribution of 8 to a theme issue ‘ Basal cognition: conceptual tools and the view from the single cell’.

                Author information
                http://orcid.org/0000-0002-9498-1238
                Article
                rstb20190763
                10.1098/rstb.2019.0763
                7934974
                33487108
                76a2fd4a-0697-4907-8360-5955866e06db
                © 2021 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : November 17, 2020
                Funding
                Funded by: Training in Schizophrenia and Psychotic Disorders: From Animal Models to Patients;
                Award ID: T32MH018870
                Categories
                1001
                133
                70
                58
                Part I: Conceptual Tools and Organizing Principles
                Review Articles
                Custom metadata
                March 15, 2021

                Philosophy of science
                hydra,spontaneous electrical low-frequency oscillations,default mode network,integration,self,organism organizer

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