Astronauts; Brain/diagnostic imaging/pathology; Humans; Space Flight; Weightlessness; White Matter/diagnostic imaging/pathology; International Space Station (ISS); magnetic resonance imaging (MRI); microgravity; neuroplasticity; neuroscience; spaceflight; tractography
Abstract :
[en] Humans undergo extreme physiological changes when subjected to long periods of weightlessness, and as we continue to become a space-faring species, it is imperative that we fully understand the physiological changes that occur in the human body, including the brain. In this study, we present findings of brain structural changes associated with long-duration spaceflight based on diffusion magnetic resonance imaging (dMRI) data. Twelve cosmonauts who spent an average of six months aboard the International Space Station (ISS) were scanned in an MRI scanner pre-flight, ten days after flight, and at a follow-up time point seven months after flight. We performed differential tractography, a technique that confines white matter fiber tracking to voxels showing microstructural changes. We found significant microstructural changes in several large white matter tracts, such as the corpus callosum, arcuate fasciculus, corticospinal, corticostriatal, and cerebellar tracts. This is the first paper to use fiber tractography to investigate which specific tracts exhibit structural changes after long-duration spaceflight and may direct future research to investigate brain functional and behavioral changes associated with these white matter pathways.
Research center :
CHU de Liège-Centre du Cerveau² - ULiège [BE]
Disciplines :
Neurology
Author, co-author :
Doroshin, Andrei; Drexel University Neuroimaging Laboratory (DUN), Drexel University, Philadelphia,
Jillings, Steven ; Université de Liège - ULiège > GIGA ; Lab for Equilibrium Investigations and Aerospace, University of Antwerp, Antwerp,
Jeurissen, Ben; Imec-Vision Lab, University of Antwerp, Antwerp, Belgium.
Tomilovskaya, Elena; State Scientific Center of the Russian Federation - Institute for Biomedical
Pechenkova, Ekaterina; Laboratory for Cognitive Research, HSE University, Moscow, Russia.
Nosikova, Inna; State Scientific Center of the Russian Federation - Institute for Biomedical
Rumshiskaya, Alena; Radiology Department, National Medical Research Treatment and Rehabilitation
Litvinova, Liudmila; Radiology Department, National Medical Research Treatment and Rehabilitation
Rukavishnikov, Ilya; State Scientific Center of the Russian Federation - Institute for Biomedical
De Laet, Chloë; Lab for Equilibrium Investigations and Aerospace, University of Antwerp, Antwerp,
Schoenmaekers, Catho; Lab for Equilibrium Investigations and Aerospace, University of Antwerp, Antwerp,
Sijbers, Jan; Imec-Vision Lab, University of Antwerp, Antwerp, Belgium.
Laureys, Steven ; Centre Hospitalier Universitaire de Liège - CHU > > Centre du Cerveau²
Petrovichev, Victor; Radiology Department, National Medical Research Treatment and Rehabilitation
Van Ombergen, Angelique; Lab for Equilibrium Investigations and Aerospace, University of Antwerp, Antwerp, ; Department of Translational Neurosciences-ENT, University of Antwerp, Antwerp,
Annen, Jitka ; Université de Liège - ULiège > GIGA > GIGA Consciousness - Coma Science Group
Sunaert, Stefan; Department of Imaging & Pathology, Translational MRI, KU Leuven - University of
Parizel, Paul M; Department of Radiology, Royal Perth Hospital, University of Western Australia
Sinitsyn, Valentin; Faculty of Fundamental Medicine, Lomonosov Moscow State University, Moscow,
Zu Eulenburg, Peter; Institute for Neuroradiology, Ludwig-Maximilians-University Munich, Munich,
Osipowicz, Karol; Drexel University Neuroimaging Laboratory (DUN), Drexel University, Philadelphia,
Wuyts, Floris L; Lab for Equilibrium Investigations and Aerospace, University of Antwerp, Antwerp,
Andersson J. L. R. Skare S. Ashburner J. (2003). How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. NeuroImage 20 870–888. 10.1016/S1053-8119(03)00336-7 14568458
Andersson J. L. R. Sotiropoulos S. N. (2016). An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. NeuroImage 125 1063–1078. 10.1016/j.neuroimage.2015.10.019 26481672
Cieslak M. Cook P. A. He X. Yeh F. C. Dhollander T. Adebimpe A. et al. (2021). QSIPrep: an integrative platform for preprocessing and reconstructing diffusion MRI data. Nat. Methods 18 775–778. 10.1038/s41592-021-01185-5 34155395
Clément G. R. Bukley A. P. Paloski W. H. (2015). Artificial gravity as a countermeasure for mitigating physiological deconditioning during long-duration space missions. Front. Syst. Neurosci. 9:92. 10.3389/fnsys.2015.00092
Herbet G. Zemmoura I. Duffau H. (2018). Functional Anatomy of the Inferior Longitudinal Fasciculus: from Historical Reports to Current Hypotheses. Front. Neuroanat. 12:77. 10.3389/fnana.2018.00077
Holderman M. Henderson E. (2011). Nautilus-X Multi-Mission Space Exploration Vehicle. Houston: NASA Johnson Space Center.
Jeurissen B. Tournier J. D. Dhollander T. Connelly A. Sijbers J. (2014). Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. NeuroImage 103 411–426. 10.1016/j.neuroimage.2014.07.061 25109526
Jillings S. Van Ombergen A. Tomilovskaya E. Rumshiskaya A. Litvinova L. Nosikova I. et al. (2020). Macro- and microstructural changes in cosmonauts’ brains after long-duration spaceflight. Sci. Adv. 6:eaaz9488. 10.1126/sciadv.aaz9488
Koppelmans V. Bloomberg J. J. Mulavara A. P. Seidler R. D. (2016). Brain structural plasticity with spaceflight. NPJ Microgravity 2:2.
Kramer L. A. Hasan K. M. Stenger M. B. Sargsyan A. Laurie S. S. Otto C. et al. (2020). Intracranial Effects of Microgravity: a Prospective Longitudinal MRI Study. Radiology 295 640–648. 10.1148/radiol.2020191413 32286194
Laitinen T. Sierra A. Bolkvadze T. Pitkänen A. Gröhn O. (2015). Diffusion tensor imaging detects chronic microstructural changes in white and gray matter after traumatic brain injury in rat. Front. Neurosci. 9:128. 10.3389/fnins.2015.00128
Lee J. K. Koppelmans V. Riascos R. F. Hasan K. M. Pasternak O. Mulavara A. P. et al. (2019). Spaceflight-Associated Brain White Matter Microstructural Changes and Intracranial Fluid Redistribution. JAMA Neurol. 76 412–419. 10.1001/jamaneurol.2018.4882 30673793
Mamiya P. C. Richards T. L. Kuhl P. K. (2018). Right Forceps Minor and Anterior Thalamic Radiation Predict Executive Function Skills in Young Bilingual Adults. Front. Psychol. 9:118. 10.3389/fpsyg.2018.00118
McDonald S. Dalton K. I. Rushby J. A. Landin-Romero R. (2019). Loss of white matter connections after severe traumatic brain injury (TBI) and its relationship to social cognition. Brain Imaging Behav. 13 819–829. 10.1007/s11682-018-9906-0 29948905
Menegaux A. Meng C. Neitzel J. Bäuml J. G. Müller H. J. Bartmann P. et al. (2017). Impaired visual short-term memory capacity is distinctively associated with structural connectivity of the posterior thalamic radiation and the splenium of the corpus callosum in preterm-born adults. NeuroImage 150 68–76. 10.1016/j.neuroimage.2017.02.017 28188917
Nakajima R. Kinoshita M. Yahata T. Nakada M. (2019). Recovery time from supplementary motor area syndrome: relationship to postoperative day 7 paralysis and damage of the cingulum. J. Neurosurg. 132 865–874. 10.3171/2018.10.JNS182391 30738403
Oldfield R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9 97–113. 10.1016/0028-3932(71)90067-4 5146491
Pascual-Leone A. Amedi A. Fregni F. Merabet L. B. (2005). The plastic human brain cortex. Ann. Rev. Neurosci. 28 377–401. 10.1146/annurev.neuro.27.070203.144216
Petersen K. J. Reid J. A. Chakravorti S. Juttukonda M. R. Franco G. Trujillo P. et al. (2018). Structural and functional connectivity of the non-decussating dentato-rubro-thalamic tract. NeuroImage 176 364–371. 10.1093/brain/awab074 33889943
Reschke M. F. Bloomberg J. J. Harm D. L. Paloski W. H. Layne C. McDonald V. (1998). Posture, locomotion, spatial orientation, and motion sickness as a function of space flight. Brain Res. Rev. 28 102–117. 10.1016/s0165-0173(98)00031-9 9795167
Roberts D. R. Albrecht M. H. Collins H. R. Asemani D. Chatterjee A. R. Spampinato M. V. et al. (2017). Effects of Spaceflight on Astronaut Brain Structure as Indicated on MRI. N. Engl. J. Med. 377 1746–1753. 10.1056/NEJMoa1705129 29091569
Roberts D. R. Stahn A. C. Seidler R. D. Wuyts F. L. (2020). Towards understanding the effects of spaceflight on the brain. Lancet Neurol. 19:808. 10.1016/S1474-4422(20)30304-5 32949538
Schilling K. G. Daducci A. Maier-Hein K. Poupon C. Houde J.-C. Nath V. et al. (2019). Challenges in diffusion MRI tractography - Lessons learned from international benchmark competitions. Magn. Reson. Imaging 57 194–209. 10.1016/j.mri.2018.11.014 30503948
Seiler S. Pirpamer L. Gesierich B. Hofer E. Duering M. Pinter D. et al. (2017). Lower Magnetization Transfer Ratio in the Forceps Minor Is Associated with Poorer Gait Velocity in Older Adults. Am. J. Neuroradiol. 38 500–506. 10.3174/ajnr.A5036 27979793
Stein T. P. (2013). Weight, muscle and bone loss during space flight: another perspective. Eur. J. Appl. Physiol. 113 2171–2181. 10.1007/s00421-012-2548-9
Tajmar M. Plesescu F. Marhold K. De Matos C. J. (2006). Experimental Detection of the Gravitomagnetic London Moment. arXiv:gr-qc/0603033v1 [preprint].
Thomas S. L. Gorassini M. A. (2005). Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury. J. Neurophysiol. 94 2844–2855. 10.1152/jn.00532.2005 16000519
Tustison N. J. Avants B. B. Cook P. A. Zheng Y. Egan A. Yushkevich P. A. et al. (2010). N4ITK: improved N3 bias correction. IEEE Trans. Med. Imaging 29 1310–1320. 10.1109/TMI.2010.2046908 20378467
T͡Siolkovskiǐ K. Syers K. J. D. (1960). Beyond the Planet Earth: Translated from the Russian by Kenneth Syers. Oxford: Pergamon Press.
Van Ombergen A. Jillings S. Jeurissen B. Tomilovskaya E. Rühl R. M. Rumshiskaya A. et al. (2018). Brain Tissue–Volume Changes in Cosmonauts. N. Engl. J. Med. 379 1678–1680. 10.1056/NEJMc1809011 30354959
Van Ombergen A. Jillings S. Jeurissen B. Tomilovskaya E. Rumshiskaya A. Litvinova L. et al. (2019). Brain ventricular volume changes induced by long-duration spaceflight. Proc. Natl. Acad. Sci. 116 10531–10536. 10.1073/pnas.1820354116
Veraart J. Novikov D. S. Christiaens D. Ades-Aron B. Sijbers J. Fieremans E. (2016). Denoising of diffusion MRI using random matrix theory. NeuroImage 142 394–406. 10.1016/j.neuroimage.2016.08.016 27523449
Yeh F. C. Badre D. Verstynen T. (2016). Connectometry: a statistical approach harnessing the analytical potential of the local connectome. NeuroImage 125 162–171. 10.1016/j.neuroimage.2015.10.053 26499808
Yeh F. C. Liu L. Hitchens T. K. Wu Y. L. (2017). Mapping immune cell infiltration using restricted diffusion MRI. Magn. Reson. Med. 77 603–612. 10.1002/mrm.26143 26843524
Yeh F. C. Panesar S. Barrios J. Fernandes D. Abhinav K. Meola A. et al. (2019). Automatic Removal of False Connections in Diffusion MRI Tractography Using Topology-Informed Pruning (TIP). Neurotherapeutics 16 52–58. 10.1007/s13311-018-0663-y 30218214
Yeh F. C. Panesar S. Fernandes D. Meola A. Yoshino M. Fernandez-Miranda J. C. et al. (2018). Population-averaged atlas of the macroscale human structural connectome and its network topology. NeuroImage 178 57–68. 10.1016/j.neuroimage.2018.05.027 29758339
Yeh F. C. Tseng W.-Y. I. (2011). NTU-90: a high angular resolution brain atlas constructed by q-space diffeomorphic reconstruction. NeuroImage 58 91–99. 10.1016/j.neuroimage.2011.06.021 21704171
Yeh F. C. Verstynen T. D. Wang Y. Fernández-Miranda J. C. Tseng W.-Y. I. (2013). Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One 8:e80713. 10.1371/journal.pone.0080713
Yeh F. C. Wedeen V. J. Tseng W.-Y. I. (2010). Generalized q-sampling imaging. IEEE Trans. Med. Imaging 29 1626–1635. 10.1109/tmi.2010.2045126
