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      Down-regulation of a cytokine secreted from peripheral fat bodies improves visual attention while reducing sleep in Drosophila

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Sleep is vital for survival. Yet under environmentally challenging conditions, such as starvation, animals suppress their need for sleep. Interestingly, starvation-induced sleep loss does not evoke a subsequent sleep rebound. Little is known about how starvation-induced sleep deprivation differs from other types of sleep loss, or why some sleep functions become dispensable during starvation. Here, we demonstrate that down-regulation of the secreted cytokine unpaired 2 ( upd2) in Drosophila flies may mimic a starved-like state. We used a genetic knockdown strategy to investigate the consequences of upd2 on visual attention and sleep in otherwise well-fed flies, thereby sidestepping the negative side effects of undernourishment. We find that knockdown of upd2 in the fat body (FB) is sufficient to suppress sleep and promote feeding-related behaviors while also improving selective visual attention. Furthermore, we show that this peripheral signal is integrated in the fly brain via insulin-expressing cells. Together, these findings identify a role for peripheral tissue-to-brain interactions in the simultaneous regulation of sleep quality and attention, to potentially promote adaptive behaviors necessary for survival in hungry animals.

          Abstract

          Hungry animals are often better off looking for food than sleeping. This study shows that attention is indeed sharpened while sleep is decreased in flies that have been genetically starved. This seems counterintuitive, because sleep deprivation normally impairs attention. A starvation cue from the peripheral fat stores to insulin-expressing cells in the brain seems responsible for sharpening attention in the face of decreased sleep.

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          Most cited references 81

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          Clues to the functions of mammalian sleep.

          The functions of mammalian sleep remain unclear. Most theories suggest a role for non-rapid eye movement (NREM) sleep in energy conservation and in nervous system recuperation. Theories of REM sleep have suggested a role for this state in periodic brain activation during sleep, in localized recuperative processes and in emotional regulation. Across mammals, the amount and nature of sleep are correlated with age, body size and ecological variables, such as whether the animals live in a terrestrial or an aquatic environment, their diet and the safety of their sleeping site. Sleep may be an efficient time for the completion of a number of functions, but variations in sleep expression indicate that these functions may differ across species.
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            A neural circuit mechanism integrating motivational state with memory expression in Drosophila.

            Behavioral expression of food-associated memory in fruit flies is constrained by satiety and promoted by hunger, suggesting an influence of motivational state. Here, we identify a neural mechanism that integrates the internal state of hunger and appetitive memory. We show that stimulation of neurons that express neuropeptide F (dNPF), an ortholog of mammalian NPY, mimics food deprivation and promotes memory performance in satiated flies. Robust appetitive memory performance requires the dNPF receptor in six dopaminergic neurons that innervate a distinct region of the mushroom bodies. Blocking these dopaminergic neurons releases memory performance in satiated flies, whereas stimulation suppresses memory performance in hungry flies. Therefore, dNPF and dopamine provide a motivational switch in the mushroom body that controls the output of appetitive memory.
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              • Record: found
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              Is Open Access

              A fractal approach to dynamic inference and distribution analysis

              Event-distributions inform scientists about the variability and dispersion of repeated measurements. This dispersion can be understood from a complex systems perspective, and quantified in terms of fractal geometry. The key premise is that a distribution's shape reveals information about the governing dynamics of the system that gave rise to the distribution. Two categories of characteristic dynamics are distinguished: additive systems governed by component-dominant dynamics and multiplicative or interdependent systems governed by interaction-dominant dynamics. A logic by which systems governed by interaction-dominant dynamics are expected to yield mixtures of lognormal and inverse power-law samples is discussed. These mixtures are described by a so-called cocktail model of response times derived from human cognitive performances. The overarching goals of this article are twofold: First, to offer readers an introduction to this theoretical perspective and second, to offer an overview of the related statistical methods.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: VisualizationRole: Writing – review & editing
                Role: Software
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                3 August 2020
                August 2020
                3 August 2020
                : 18
                : 8
                Affiliations
                Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia
                University of Pennsylvania, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PBIOLOGY-D-19-02915
                10.1371/journal.pbio.3000548
                7426065
                32745077
                © 2020 Ertekin et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 8, Tables: 0, Pages: 27
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Award ID: GNT1065713
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000025, National Institute of Mental Health;
                Award ID: R01 NS076980
                Award Recipient :
                This work was supported by two grants from the National Health and Medical Research Council of Australia ( https://www.nhmrc.gov.au/), GNT1065713 and GNT1164499, to BVS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Sleep
                Biology and Life Sciences
                Nutrition
                Diet
                Food
                Medicine and Health Sciences
                Nutrition
                Diet
                Food
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognitive Psychology
                Perception
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Cognitive Psychology
                Perception
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Cognitive Psychology
                Perception
                Sensory Perception
                Vision
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Behavior
                Social Sciences
                Psychology
                Behavior
                Biology and life sciences
                Genetics
                Epigenetics
                RNA interference
                Biology and life sciences
                Genetics
                Gene expression
                RNA interference
                Biology and life sciences
                Genetics
                Genetic interference
                RNA interference
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                RNA interference
                Biology and Life Sciences
                Genetics
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognitive Psychology
                Attention
                Biology and Life Sciences
                Psychology
                Cognitive Psychology
                Attention
                Social Sciences
                Psychology
                Cognitive Psychology
                Attention
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-08-13
                All relevant data are within the paper and in its Supporting Information files.

                Life sciences

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