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Otoconia Structure After Short- and Long-Duration Exposure to Altered Gravity

Abstract

Vertebrates use weight-lending otoconia in the inner ear otolith organs to enable detection of their translation during self or imposed movements and a change in their orientation with respect to gravity. In spaceflight, otoconia are near weightless. It has been hypothesized that otoconia undergo structural remodeling after exposure to weightlessness to restore normal sensation. A structural remodeling is reasoned to occur for hypergravity but in the opposite sense. We explored these hypotheses in several strains of mice within a Biospecimen Sharing Program in separate space- and ground-based projects. Mice were housed 90 days on the International Space Station, 13 days on two Shuttle Orbiter missions, or exposed to 90 days of hindlimb unloading or net 2.38 g via centrifugation. Corresponding flight habitat and standard cage vivarium controls were used. Utricular otoliths were visually analyzed using scanning electron microscopy and in selected samples before and after focused ion beam (FIB) milling. Results suggest a possible mass addition to the otoconia outer shell might occur after exposure to longer-duration spaceflight, but not short ones or hindlimb unloading. A destructive process is clearly seen after centrifugation: an ablation or thinning of the outer shell and cavitation of the inner core. This study provides a purely descriptive account of otoconia remodeling after exposures to altered gravity. The mechanism(s) underlying these processes must be identified and quantitatively validated to develop countermeasures to altered gravity levels during exploration missions.

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ACKNOWLEDGEMENTS

We gratefully acknowledge (1) the research team of Dr. R Cancedda of the Università degli Studi di Genova and Istituto Nazionale per la Ricerca sul Cancro, Genova, Italia; (2) ASI—Agenzia Spaziale Italiana, Roma, Italia; (3) Biospecimen Sharing Program of NASA STS-133 and -135; (4) Dr. Yoshinobu Ohira of the Graduate School of Medicine, Osaka University, Toyonaka City, Osaka 560-0043 and the Research Center for Adipocyte and Muscle Science, Doshisha University, Kyotanabe City, Kyoto 610-0394, Japan; and (5) Dr. Tom Yuzvinsky for his expertise in FIB milling and scanning electron microscopy and the W.M. Keck Center for Nanoscale Optofluidics at the University of California, Santa Cruz, USA, for providing the FEI Quanta 3D Dual beam microscope for use in portions of this study.

Funding

This work was supported by NASA funds for collaboration with the Italian Space Agency “Mouse Drawer System” and NASA Proposal “Inner Ear Otoconia Response in Mice to Micro- and Hyper-gravity” (no. 11-11_Omni_2-0002). Funding was also provided in part by the Human Research Program (Johnson Space Center, Houston TX USA) and Space Biology (Ames Research Center, Mountain View CA USA).

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Richard Boyle secured the resources, collected the samples at the multiple sites (Kennedy Space Center, Florida; Genova, Italy; Osaka, Japan), participated in FIB processing at University of California (Santa Cruz), interpreted the images, and drafted the manuscript. Joseph Varelas performed the critical technical preparation of the samples, imaged the samples, and participated in FIB processing.

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Correspondence to Richard Boyle.

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This study was conducted within Biospecimen Sharing Programs with “no interference” participation. All procedures of the principal investigations met the NIH guidelines for care and use of laboratory animals and were approved by the appropriate Animal Care and Use Committee at Kennedy Space Center (USA), Università di Genova (Italia), and Osaka University (Japan).

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Boyle, R., Varelas, J. Otoconia Structure After Short- and Long-Duration Exposure to Altered Gravity. JARO 22, 509–525 (2021). https://doi.org/10.1007/s10162-021-00791-6

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