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      Combined Exposure to Simulated Microgravity and Acute or Chronic Radiation Reduces Neuronal Network Integrity and Survival

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          Abstract

          During orbital or interplanetary space flights, astronauts are exposed to cosmic radiations and microgravity. However, most earth-based studies on the potential health risks of space conditions have investigated the effects of these two conditions separately. This study aimed at assessing the combined effect of radiation exposure and microgravity on neuronal morphology and survival in vitro. In particular, we investigated the effects of simulated microgravity after acute (X-rays) or during chronic (Californium-252) exposure to ionizing radiation using mouse mature neuron cultures. Acute exposure to low (0.1 Gy) doses of X-rays caused a delay in neurite outgrowth and a reduction in soma size, while only the high dose impaired neuronal survival. Of interest, the strongest effect on neuronal morphology and survival was evident in cells exposed to microgravity and in particular in cells exposed to both microgravity and radiation. Removal of neurons from simulated microgravity for a period of 24 h was not sufficient to recover neurite length, whereas the soma size showed a clear re-adaptation to normal ground conditions. Genome-wide gene expression analysis confirmed a modulation of genes involved in neurite extension, cell survival and synaptic communication, suggesting that these changes might be responsible for the observed morphological effects. In general, the observed synergistic changes in neuronal network integrity and cell survival induced by simulated space conditions might help to better evaluate the astronaut's health risks and underline the importance of investigating the central nervous system and long-term cognition during and after a space flight.

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          Most cited references60

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          Measurements of energetic particle radiation in transit to Mars on the Mars Science Laboratory.

          The Mars Science Laboratory spacecraft, containing the Curiosity rover, was launched to Mars on 26 November 2011, and for most of the 253-day, 560-million-kilometer cruise to Mars, the Radiation Assessment Detector made detailed measurements of the energetic particle radiation environment inside the spacecraft. These data provide insights into the radiation hazards that would be associated with a human mission to Mars. We report measurements of the radiation dose, dose equivalent, and linear energy transfer spectra. The dose equivalent for even the shortest round-trip with current propulsion systems and comparable shielding is found to be 0.66 ± 0.12 sievert.
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            Dynamics and effective topology underlying synchronization in networks of cortical neurons.

            Cognitive processes depend on synchronization and propagation of electrical activity within and between neuronal assemblies. In vivo measurements show that the size of individual assemblies depends on their function and varies considerably, but the timescale of assembly activation is in the range of 0.1-0.2 s and is primarily independent of assembly size. Here we use an in vitro experimental model of cortical assemblies to characterize the process underlying the timescale of synchronization, its relationship to the effective topology of connectivity within an assembly, and its impact on propagation of activity within and between assemblies. We show that the basic mode of assembly activation, "network spike," is a threshold-governed, synchronized population event of 0.1-0.2 s duration and follows the logistics of neuronal recruitment in an effectively scale-free connected network. Accordingly, the sequence of neuronal activation within a network spike is nonrandom and hierarchical; a small subset of neurons is consistently recruited tens of milliseconds before others. Theory predicts that scale-free topology allows for synchronization time that does not increase markedly with network size; our experiments with networks of different densities support this prediction. The activity of early-to-fire neurons reliably forecasts an upcoming network spike and provides means for expedited propagation between assemblies. We demonstrate this capacity by observing the dynamics of two artificially coupled assemblies in vitro, using neuronal activity of one as a trigger for electrical stimulation of the other.
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              Characterizing brain cortical plasticity and network dynamics across the age-span in health and disease with TMS-EEG and TMS-fMRI.

              Brain plasticity can be conceptualized as nature's invention to overcome limitations of the genome and adapt to a rapidly changing environment. As such, plasticity is an intrinsic property of the brain across the lifespan. However, mechanisms of plasticity may vary with age. The combination of transcranial magnetic stimulation (TMS) with electroencephalography (EEG) or functional magnetic resonance imaging (fMRI) enables clinicians and researchers to directly study local and network cortical plasticity, in humans in vivo, and characterize their changes across the age-span. Parallel, translational studies in animals can provide mechanistic insights. Here, we argue that, for each individual, the efficiency of neuronal plasticity declines throughout the age-span and may do so more or less prominently depending on variable 'starting-points' and different 'slopes of change' defined by genetic, biological, and environmental factors. Furthermore, aberrant, excessive, insufficient, or mistimed plasticity may represent the proximal pathogenic cause of neurodevelopmental and neurodegenerative disorders such as autism spectrum disorders or Alzheimer's disease.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                20 May 2016
                2016
                : 11
                : 5
                : e0155260
                Affiliations
                [1 ]Radiobiology Unit, Laboratory of Molecular and Cellular Biology, Institute for Environment, Health and Safety, Belgian Nuclear Research Centre, SCK•CEN, Mol, Belgium
                [2 ]Cell Systems and Imaging Research Group (CSI), Department of Molecular Biotechnology, Ghent University, Ghent, Belgium
                [3 ]Laboratory of Membrane Biochemistry and Applied Nutrition, Department of Pharmacology and Bio-molecular Sciences (DiSFeB), Università degli Studi di Milano, Milano, Italy
                University of Louisville, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GP MV RQ PvO SB MB. Performed the experiments: GP MV RQ NS LD. Analyzed the data: GP MV RQ. Wrote the paper: GP MV RQ.

                Article
                PONE-D-16-01283
                10.1371/journal.pone.0155260
                4874625
                27203085
                ac57c5a5-953f-4081-9b47-2c182362e80b
                © 2016 Pani 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.

                History
                : 11 January 2016
                : 26 April 2016
                Page count
                Figures: 6, Tables: 0, Pages: 19
                Funding
                Funded by: Prodex/ESA
                Award ID: C90-303
                Award Recipient :
                Funded by: Prodex/ESA
                Award ID: C90-391
                Award Recipient :
                Funded by: Prodex/ESA
                Award ID: C0-90-11-2801-02
                Award Recipient :
                Funded by: Sardinian government
                Award ID: AF-DR-A2008-67
                Award Recipient :
                Funded by PRODEX/ESA: C90-303, C90-391, C0-90-11-2801-02, Sardinian government: EF-DR-A2008-67. 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
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Death
                Apoptosis
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Neuronal Dendrites
                Neurites
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Neuronal Dendrites
                Neurites
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neuronal Morphology
                Physical Sciences
                Physics
                Gravitation
                Artificial Gravity
                Biology and Life Sciences
                Genetics
                Gene Expression
                Physical Sciences
                Physics
                Nuclear Physics
                Nucleons
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Death
                Neuronal Death
                Custom metadata
                All relevant data are within the paper.

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