Spaceflight-Associated Brain White Matter Microstructural Changes and Intracranial Fluid Redistribution

Abstract

How is spaceflight associated with human brain white matter and extracellular fluid distribution? In this longitudinal analysis, increased extracellular fluid was observed in widespread areas at the base of the cerebrum and decreases along the posterior aspect of the vertex following spaceflight. After adjusting for extracellular fluid, there was altered white matter microstructure in areas encompassing the superior and inferior longitudinal fasciculi, the inferior fronto-occipital fasciculus, and the corticospinal tract following spaceflight. Spaceflight is associated with redistribution of brain extracellular fluids; white matter changes occur throughout the brain and, in some cases, are significantly associated with mission duration and postflight declines in balance. Spaceflight results in transient balance declines and brain morphologic changes; to our knowledge, the effect on brain white matter as measured by diffusion magnetic resonance imaging (dMRI), after correcting for extracellular fluid shifts, has not been examined. To map spaceflight-induced intracranial extracellular free water (FW) shifts and to evaluate changes in brain white matter diffusion measures in astronauts. We performed retrospective, longitudinal analyses on dMRI data collected between 2010 and 2015. Of the 26 astronauts’ dMRI scans released by the National Aeronautics and Space Administration Lifetime Surveillance of Astronaut Health, 15 had both preflight and postflight dMRI scans and were included in the final analyses. Data were analyzed between 2015 and 2018. Seven astronauts completed a space shuttle mission (≤30 days) and 8 completed a long-duration International Space Station mission (≤200 days). The dMRI scans were acquired for clinical monitoring; in this retrospective analysis, we analyzed brain FW and white matter diffusion metrics corrected for FW. We also obtained scores from computerized dynamic posturography tests of balance to assess brain-behavior associations. Of the 15 astronauts included, the median (SD) age was 47.2 (1.5) years; 12 were men, and 3 were women. We found a significant, widespread increase in FW volume in the frontal, temporal, and occipital lobes from before spaceflight to after spaceflight. There was also a significant decrease in FW in the posterior aspect of the vertex. All FW changes were significant and ranged from approximately 2.5% to 4.0% across brain regions. We observed white matter changes in the right superior and inferior longitudinal fasciculi, the corticospinal tract, and cerebellar peduncles. All white matter changes were significant and ranged from approximately 0.75% to 1.25%. Spaceflight mission duration was associated with cerebellar white matter change, and white matter changes in the superior longitudinal fasciculus were associated with the balance changes seen in the astronauts from before spaceflight to after spaceflight. Free water redistribution with spaceflight likely reflects headward fluid shifts occurring in microgravity as well as an upward shift of the brain within the skull. White matter changes were of a greater magnitude than those typically seen during the same period with healthy aging. Future, prospective assessments are required to better understand the recovery time and behavioral consequences of these brain changes. This study maps spaceflight-induced intracranial extracellular free water (FW) shifts and evaluates changes in brain white matter diffusion measures in astronauts following spaceflight.