Brain; Diffusion in liquids; Image segmentation; Magnetic resonance imaging; Manned space flight; Neurophysiology; Brain structure; Cerebro spinal fluids; Diffusion magnetic resonance imaging; Long duration; Microstructural changes; Morphological changes; Neuroplasticity; Region of interest; Cerebrospinal fluid
Jillings, Steven ; Université de Liège - ULiège > Giga Consciousness-Coma Science Group
Van Ombergen, A.; Lab for Equilibrium Investigations and Aerospace, Department of Physics, University of Antwerp, Antwerp, Belgium, Department of Translational Neurosciences-ENT, University of Antwerp, Antwerp, Belgium
Tomilovskaya, E.; SSC RF - Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russian Federation
Rumshiskaya, A.; Radiology Department, National Medical Research Treatment and Rehabilitation Centre of the Ministry of Health of Russia, Moscow, Russian Federation
Litvinova, L.; Radiology Department, National Medical Research Treatment and Rehabilitation Centre of the Ministry of Health of Russia, Moscow, Russian Federation
Nosikova, I.; SSC RF - Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russian Federation
Pechenkova, E.; Laboratory for Cognitive Research, National Research University, Higher School of Economics, Moscow, Russian Federation
Rukavishnikov, I.; SSC RF - Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russian Federation
Kozlovskaya, I. B.; SSC RF - Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russian Federation
Manko, O.; SSC RF - Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russian Federation
Danilichev, S.; Gagarin Cosmonauts Training Center, Star City. Moscow Region, Russian Federation
Sunaert, S.; KU Leuven - University of Leuven, Department of Imaging and Pathology, Translational MRI, Leuven, Belgium
Parizel, P. M.; Department of Radiology, Royal Perth Hospital and University of Western Australia Medical School, Perth, WA, Australia
Sinitsyn, V.; Faculty of Fundamental Medicine, Lomonosov Moscow State University, Moscow, Russian Federation
Petrovichev, V.; Radiology Department, National Medical Research Treatment and Rehabilitation Centre of the Ministry of Health of Russia, Moscow, Russian Federation
Laureys, Steven ; Université de Liège - ULiège > Giga Consciousness-Coma Science Group
Eulenburg, P.; Institute for Neuroradiology, Ludwig-Maximilians- University Munich, Munich, Germany
Sijbers, J.; imec-Vision Lab, Department of Physics, University of Antwerp, Antwerp, Belgium
Wuyts, F. L.; Lab for Equilibrium Investigations and Aerospace, Department of Physics, University of Antwerp, Antwerp, Belgium
Jeurissen, B.; imec-Vision Lab, Department of Physics, University of Antwerp, Antwerp, Belgium
Macro- And microstructural changes in cosmonauts' brains after long-duration spaceflight
Publication date :
2020
Journal title :
Science Advances
eISSN :
2375-2548
Publisher :
American Association for the Advancement of Science
Volume :
6
Issue :
36
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Prodex
Funders :
RAS - Russian Academy of Sciences BELSPO - Belgian Science Policy Office FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen French-Speaking Community of Belgium BMBF - Federal Ministry of Education and Research
Funding number :
ESA Grant ISLRA 2009-1062; Russian Academy of Sciences (grant number 63.1); French Speaking Community Concerted Research Action Grant ARC06/11-340; German Federal Ministry of Education and Research Grant 01 EO 0901 (to P.z.E.); Zonta International Amelia Earhart Fellowship 2016−2017 (to A.V.O.)
G. Clément, Fundamentals of Space Medicine (Springer, ed. 2, 2011).
P.-M. Lledo, M. Alonso, M. S. Grubb, Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179-193 (2006).
A. Van Ombergen, S. Laureys, S. Sunaert, E. Tomilovskaya, P. M. Parizel, F. L. Wuyts, Spaceflight-induced neuroplasticity in humans as measured by MRI: What do we know so far? NPJ Microgravity 3, 2 (2017).
A. Van Ombergen, S. Jillings, B. Jeurissen, E. Tomilovskaya, R. M. Rühl, A. Rumshiskaya, I. Nosikova, L. Litvinova, J. Annen, E. V. Pechenkova, I. B. Kozlovskaya, S. Sunaert, P. M. Parizel, V. Sinitsyn, S. Laureys, J. Sijbers, P. Zu Eulenburg, F. L. Wuyts, Brain tissue-volume changes in cosmonauts. N. Engl. J. Med. 379, 1678-1680 (2018).
V. Koppelmans, J. J. Bloomberg, A. P. Mulavara, R. D. Seidler, Brain structural plasticity with spaceflight. NPJ Microgravity 2, 2 (2016).
J. K. Lee, V. Koppelmans, R. F. Riascos, K. M. Hasan, O. Pasternak, A. P. Mulavara, J. J. Bloomberg, R. D. Seidler, Spaceflight-associated brain white matter microstructural changes and intracranial fluid redistribution. JAMA Neurol. 76, 412-419 (2019).
A. Van Ombergen, S. Jillings, B. Jeurissen, E. Tomilovskaya, A. Rumshiskaya, L. Litvinova, I. Nosikova, E. Pechenkova, I. Rukavishnikov, O. Manko, S. Danylichev, R. M. Rühl, I. B. Kozlovskaya, S. Sunaert, P. M. Parizel, V. Sinitsyn, S. Laureys, J. Sijbers, P. Z. Eulenburg, F. L. Wuyts, Brain ventricular volume changes induced by long-duration spaceflight. Proc. Natl. Acad. Sci. U.S.A. 116, 10531-10536 (2019).
D. R. Roberts, M. H. Albrecht, H. R. Collins, D. Asemani, A. R. Chatterjee, M. V. Spampinato, X. Zhu, M. I. Chimowitz, M. U. Antonucci, Effects of spaceflight on astronaut brain structure as indicated on MRI. N. Engl. J. Med. 377, 1746-1753 (2017).
N. Alperin, A. M. Bagci, S. H. Lee, Spaceflight-induced changes in white matter hyperintensity burden in astronauts. Neurology 89, 2187-2191 (2017).
A. Demertzi, A. Van Ombergen, E. Tomilovskaya, B. Jeurissen, E. Pechenkova, C. Di Perri, L. Litvinova, E. Amico, A. Rumshiskaya, I. Rukavishnikov, J. Sijbers, V. Sinitsyn, I. B. Kozlovskaya, S. Sunaert, P. M. Parizel, P. H. Van de Heyning, S. Laureys, F. L. Wuyts, Cortical reorganization in an astronaut's brain after long-duration spaceflight. Brain Struct. Funct. 221, 2873-2876 (2016).
E. Pechenkova, I. Nosikova, A. Rumshiskaya, L. Litvinova, I. Rukavishnikov, E. Mershina, V. Sinitsyn, A. Van Ombergen, B. Jeurissen, S. Jillings, S. Laureys, J. Sijbers, A. Grishin, L. Chernikova, I. Naumov, L. Kornilova, F. L. Wuyts, E. Tomilovskaya, I. Kozlovskaya, Alterations of functional brain connectivity after long-duration spaceflight as revealed by fMRI. Front. Physiol. 10, 761 (2019).
T. H. Mader, C. R. Gibson, N. R. Miller, P. S. Subramanian, N. B. Patel, A. G. Lee, An overview of spaceflight-associated neuro-ocular syndrome (SANS). Neurol. India 67, S206-S211 (2019).
J. Ashburner, K. J. Friston, Voxel-Based Morphometry-The Methods. Neuroimage 11, 805-821 (2000).
D. A. Raffelt, J.-D. Tournier, R. E. Smith, D. N. Vaughan, G. Jackson, G. R. Ridgway, A. Connelly, Investigating white matter fibre density and morphology using fixel-based analysis. Neuroimage 144, 58-73 (2017).
B. Jeurissen, J.-D. Tournier, T. Dhollander, A. Connelly, J. Sijbers, Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. Neuroimage 103, 411-426 (2014).
D. R. Roberts, D. Asemani, P. J. Nietert, M. A. Eckert, D. C. Inglesby, J. J. Bloomberg, M. S. George, T. R. Brown, Prolonged microgravity affects human brain structure and function. AJNR Am. J. Neuroradiol. 40, 1878-1885 (2019).
Y. Sagi, I. Tavor, S. Hofstetter, S. Tzur-Moryosef, T. Blumenfeld-Katzir, Y. Assaf, Learning in the fast lane: New insights into neuroplasticity. Neuron 73, 1195-1203 (2012).
D. Manzoni, The cerebellum may implement the appropriate coupling of sensory inputs and motor responses: Evidence from vestibular physiology. Cerebellum 4, 178-188 (2005).
P. R. MacNeilage, S. Glasauer, Gravity perception: The role of the cerebellum. Curr. Biol. 28, R1296-R1298 (2018).
K. R. Bailey, R. G. Mair, The role of striatum in initiation and execution of learned action sequences in rats. J. Neurosci. 26, 1016-1025 (2006).
G. Courtine, T. Pozzo, Recovery of the locomotor function after prolonged microgravity exposure. I. Head-trunk movement and locomotor equilibrium during various tasks. Exp. Brain Res. 158, 86-99 (2004).
A. P. Mulavara, A. H. Feiveson, J. Fiedler, H. Cohen, B. T. Peters, C. Miller, R. Brady, J. J. Bloomberg, Locomotor function after long-duration space flight: Effects and motor learning during recovery. Exp. Brain Res. 202, 649-659 (2010).
E. Hallgren, L. Kornilova, E. Fransen, D. Glukhikh, S. T. Moore, G. Clément, A. Van Ombergen, H. MacDougall, I. Naumov, F. L. Wuyts, Decreased otolith-mediated vestibular response in 25 astronauts induced by long-duration spaceflight. J. Neurophysiol. 115, 3045-3051 (2016).
L. S. Popa, T. J. Ebner, Cerebellum, predictions and errors. Front. Cell. Neurosci. 12, 524 (2019).
A. Karabanov, S. Cervenka, O. de Manzano, H. Forssberg, L. Farde, F. Ullen, Dopamine D2 receptor density in the limbic striatum is related to implicit but not explicit movement sequence learning. Proc. Natl. Acad. Sci. U.S.A. 107, 7574-7579 (2010).
A. C. Bostan, P. L. Strick, The basal ganglia and the cerebellum: Nodes in an integrated network. Nat. Rev. Neurosci. 19, 338-350 (2018).
B. Jeurissen, A. Leemans, J.-D. Tournier, D. K. Jones, J. Sijbers, Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum. Brain Mapp. 34, 2747-2766 (2013).
P. Wostyn, T. H. Mader, C. R. Gibson, H. E. Killer, The escape of retrobulbar cerebrospinal fluid in the astronaut's eye: Mission impossible? Eye 33, 1519-1524 (2019).
A. Van Ombergen, S. Jillings, E. Tomilovskaya, F. L. Wuyts, P. Z. Eulenburg, Reply to Wostyn et al.: Investigating the spaceflight-associated neuro-ocular syndrome and the human brain in lockstep. Proc. Natl. Acad. Sci. U.S.A. 116, 15772-15773 (2019).
L. A. Kramer, K. M. Hasan, A. E. Sargsyan, J. S. Wolinsky, D. R. Hamilton, R. F. Riascos, W. K. Carson, J. Heimbigner, V. S. Patel, S. Romo, C. Otto, MR-derived cerebral spinal fluid hydrodynamics as a marker and a risk factor for intracranial hypertension in astronauts exposed to microgravity. J. Magn. Reson. Imaging 42, 1560-1571 (2015).
V. V. Bogomolov, M. P. Kuzmin, S. N. Danilichev, On the intracranial hypertension in astronauts during long-term microgravity. Aviakosm. Ekolog. Med. 49, 54-58 (2015).
R. C. Oldfield, The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9, 97-113 (1971).
J. L. R. Andersson, S. Skare, J. Ashburner, How to correct susceptibility distortions in spin-echo echo-planar images: Application to diffusion tensor imaging. Neuroimage 20, 870-888 (2003).
J.-D. Tournier, R. Smith, D. Raffelt, R. Tabbara, T. Dhollander, M. Pietsch, D. Christiaens, B. Jeurissen, C.-H. Yeh, A. Connelly, MRtrix3: A fast, flexible and open software framework for medical image processing and visualisation. Neuroimage 202, 116137 (2019).
B. Jeurissen, A. Leemans, J. Sijbers, Automated correction of improperly rotated diffusion gradient orientations in diffusion weighted MRI. Med. Image Anal. 18, 953-962 (2014).
M. Bastiani, M. Cottaar, S. P. Fitzgibbon, S. Suri, F. Alfaro-Almagro, S. N. Sotiropoulos, S. Jbabdi, J. L. R. Andersson, Automated quality control for within and between studies diffusion MRI data using a non-parametric framework for movement and distortion correction. Neuroimage 184, 801-812 (2019).
J. Veraart, D. S. Novikov, D. Christiaens, B. Ades-Aron, J. Sijbers, E. Fieremans, Denoising of diffusion MRI using random matrix theory. Neuroimage 142, 394-406 (2016).
E. Kellner, B. Dhital, V. G. Kiselev, M. Reisert, Gibbs-ringing artifact removal based on local subvoxel-shifts. Magn. Reson. Med. 76, 1574-1581 (2016).
J. L. R. Andersson, S. N. Sotiropoulos, An integrated approach to correction for offresonance effects and subject movement in diffusion MR imaging. Neuroimage 125, 1063-1078 (2016).
N. J. Tustison, B. B. Avants, P. A. Cook, Y. Zheng, A. Egan, P. A. Yushkevich, J. C. Gee, N4ITK: Improved N3 bias correction. IEEE Trans. Med. Imaging 29, 1310-1320 (2010).
D. Raffelt, J.-D. Tournier, J. Fripp, S. Crozier, A. Connelly, O. Salvado, Symmetric diffeomorphic registration of fibre orientation distributions. Neuroimage 56, 1171-1180 (2011).
M. Pietsch, D. Christiaens, J. Hutter, L. Cordero-Grande, A. N. Price, E. Hughes, A. D. Edwards, J. V. Hajnal, S. J. Counsell, J.-D. Tournier, A framework for multi-component analysis of diffusion MRI data over the neonatal period. Neuroimage 186, 321-337 (2019).
S. M. Smith, T. E. Nichols, Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44, 83-98 (2009).
T. E. Nichols, A. P. Holmes, Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum. Brain Mapp. 15, 1-25 (2002).
