Olga Kuldavletova, Paola Kola, Mikaël Naveau, Tianyi Wang, Thomas Caille, Gaëlle Quarck, Alexander Stahn, Scott Wood, Pierre Denise, Rachael D. Seidler, Olivier Etard
Abstract The hippocampus is a particularly plastic and vulnerable brain structure. Given the modulatory role of the vestibular system on hippocampal function, we hypothesized that altered vestibular stimulation associated with prolonged spaceflight could lead to similar hippocampal volume changes in astronauts after long-duration spaceflight and in individuals with bilateral vestibulopathy (BV), as a ground analog of spaceflight. We quantified hippocampal volumes using magnetic resonance imaging (MRI) in astronauts before and after spaceflight and in BV patients relative to matched healthy controls. MRI analyses revealed a significant decrease in the left hippocampal volume (-2%) and an increase in the total volume of the ventricles (+ 11%) postflight in astronauts. The variations in volume of right and left hippocampus and ventricles were not correlated with each other, suggesting that the cerebrospinal fluid redistribution that occurs with spaceflight does not contribute to hippocampal volume changes. BV patients exhibited reduced hippocampal volumes compared to matched controls (-6% left and − 4% right), suggesting that reduction of vestibular inputs, due either to microgravity or a disease, may contribute to hippocampal atrophy. Furthermore, in both astronauts and BV patients, hippocampal volume correlated negatively with age, suggesting increased vulnerability of older individuals to vestibular-related neurodegeneration. Overall, our findings suggest that hippocampal atrophy in astronauts is not driven by mechanical compression, but it may be affected by reduced vestibular input, aligning with observations in terrestrial vestibular loss.