Ocular counter-roll is less affected in experienced versus novice space crew after long-duration spaceflight.
Journal
NPJ microgravity
ISSN: 2373-8065
Titre abrégé: NPJ Microgravity
Pays: United States
ID NLM: 101703605
Informations de publication
Date de publication:
20 Jul 2022
20 Jul 2022
Historique:
received:
29
09
2021
accepted:
22
06
2022
entrez:
20
7
2022
pubmed:
21
7
2022
medline:
21
7
2022
Statut:
epublish
Résumé
Otoliths are the primary gravity sensors of the vestibular system and are responsible for the ocular counter-roll (OCR). This compensatory eye torsion ensures gaze stabilization and is sensitive to a head roll with respect to gravity and the Gravito-Inertial Acceleration vector during, e.g., centrifugation. To measure the effect of prolonged spaceflight on the otoliths, we quantified the OCR induced by off-axis centrifugation in a group of 27 cosmonauts in an upright position before and after their 6-month space mission to the International Space Station. We observed a significant decrease in OCR early postflight, larger for first-time compared to experienced flyers. We also found a significantly larger torsion for the inner eye, the eye closest to the rotation axis. Our results suggest that experienced cosmonauts have acquired the ability to adapt faster after G-transitions. These data provide a scientific basis for sending experienced cosmonauts on challenging missions that include multiple g-level transitions.
Identifiants
pubmed: 35858981
doi: 10.1038/s41526-022-00208-5
pii: 10.1038/s41526-022-00208-5
pmc: PMC9300597
doi:
Types de publication
Journal Article
Langues
eng
Pagination
27Informations de copyright
© 2022. The Author(s).
Références
Angelaki, D. E. & Cullen, K. E. Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125–150 (2008).
pubmed: 18338968
doi: 10.1146/annurev.neuro.31.060407.125555
Macdougall, H. G., Curthoys, I. S., Betts, G. A., Burgess, A. M. & Halmagyi, G. M. Human ocular counterrolling during roll-tilt and centrifugation. Ann. N. Y. Acad. Sci. 871, 173–180 (1999).
Miller, E. F. II & Graybiel, A. Effect of gravitoinertial force on ocular counterrolling. J. Appl. Physiol. 31, 697–700 (1971).
pubmed: 5117183
doi: 10.1152/jappl.1971.31.5.697
Moore, S. T., Clement, G., Raphan, T. & Cohen, B. Ocular counterrolling induced by centrifugation during orbital spaceflight. Exp. Brain Res. 137, 323–335 (2001).
pubmed: 11355379
doi: 10.1007/s002210000669
Imai, T., Moore, S. T., Raphan, T. & Cohen, B. Interaction of the body, head, and eyes during walking and turning. Exp. Brain Res. 136, 1–18 (2001).
pubmed: 11204402
doi: 10.1007/s002210000533
Hallgren, E. et al. Decreased otolith-mediated vestibular response in 25 astronauts induced by long-duration spaceflight. J. Neurophysiol. 115, 3045–3051 (2016).
pubmed: 27009158
pmcid: 4922620
doi: 10.1152/jn.00065.2016
Clarke, A. H., Grigull, J., Mueller, R. & Scherer, H. The three-dimensional vestibulo-ocular reflex during prolonged microgravity. Exp. Brain Res. 134, 322–334 (2000).
pubmed: 11045357
doi: 10.1007/s002210000476
Hallgren, E. et al. Dysfunctional vestibular system causes a blood pressure drop in astronauts returning from space. Sci. Rep. 16(5), 17627 (2015).
doi: 10.1038/srep17627
Clement, G., Reschke, M. & Wood, S. Neurovestibular and sensorimotor studies in space and Earth benefits. Curr. Pharm. Biotechnol. 6, 267–283 (2005).
pubmed: 16101466
doi: 10.2174/1389201054553716
Arrott, A. P. & Young, L. R. M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 6. Vestibular reactions to lateral acceleration following ten days of weightlessness. Exp. Brain Res. 64, 347–357 (1986).
pubmed: 3492387
doi: 10.1007/BF00237751
Diamond, S. G. & Markham, C. H. Changes in gravitational state cause changes in ocular torsion. J. Gravit. Physiol. 5, P109–P110 (1998).
Iakovleva, I., Kornilova, L. N., Tarasov, I. K. & Alekseev, V. N. Results of a study of vestibular function and space perception in cosmonauts. Kosm. Biol. Aviakosm. Med. 16, 20–26 (1982).
pubmed: 6977677
Vogel, H. & Kass, J. R. European vestibular experiments on the Spacelab-1 mission: 7. Ocular counterrolling measurements pre- and postflight. Exp. Brain Res. 64, 284–290 (1986).
pubmed: 3803474
doi: 10.1007/BF00237745
Young, L. R. & Sinha, P. Spaceflight influences on ocular counterrolling and other neurovestibular reactions. Otolaryngol. Head Neck Surg. 118, S31–S34 (1998).
pubmed: 9525488
doi: 10.1016/S0194-59989870006-3
Clement, G., Denise, P., Reschke, M. F. & Wood, S. J. Human ocular counter-rolling and roll tilt perception during off-vertical axis rotation after spaceflight. J. Vestib. Res. 17, 209–215 (2007).
pubmed: 18626132
doi: 10.3233/VES-2007-175-602
Kornilova, L. N., Sagalovitch, S. V., Temnikova, V. V. & Yakushev, A. G. Static and dynamic vestibulo-cervico-ocular responses after prolonged exposure to microgravity. J. Vestib. Res. 17, 217–226 (2007).
pubmed: 18626133
doi: 10.3233/VES-2007-175-603
Collewijn, H., van der Steen, J., Ferman, L. & Jansen, T. C. Human ocular counterroll: assessment of static and dynamic properties from electromagnetic scleral coil recordings. Exp. Brain Res. 59, 185–196 (1985).
pubmed: 4018196
doi: 10.1007/BF00237678
Das, R., Banerjee, M., Nan, B. & Zheng, H. Fast estimation of regression parameters in a broken-stick model for longitudinal data. J. Am. Stat. Assoc. 111(515), 1132–1143 (2016).
pubmed: 28316356
pmcid: 5353362
doi: 10.1080/01621459.2015.1073154
Koppelmans, V. et al. Brain plasticity and sensorimotor deterioration as a function of 70 days head down tilt bed rest. PLoS One 12, e0182236 (2017).
Tays, G. D. et al. The effects of long duration spaceflight on sensorimotor control and cognition. Front. Neural Circuits 26(15), 723504 (2021).
doi: 10.3389/fncir.2021.723504
Dai, M., Mcgarvie, L., Kozlovskaya, I., Raphan, T. & Cohen, B. Effects of spaceflight on ocular counterrolling and the spatial orientation of the vestibular system. Exp. Brain Res. 102, 45–56 (1994).
pubmed: 7895798
doi: 10.1007/BF00232437
Homick, J. L. & Reschke, M. F. Postural equilibrium following exposure to weightless spaceflight. Acta Otolaryngol. 83, 45 5–64 (1977).
doi: 10.3109/00016487709128871
Kenyon, R. V. & Young, L. R. M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 5. Postural responses following exposure to weightlessness. Exp. Brain Res. 64, 335–346 (1986).
pubmed: 3492386
doi: 10.1007/BF00237750
Merfeld, D. M. Effect of spaceflight on ability to sense and control roll tilt: human neurovestibular studies on SLS-2. J. Appl. Physiol. 81, 50–57 (1996).
pubmed: 8828647
doi: 10.1152/jappl.1996.81.1.50
Reschke, M. F., Wood, S. J. & Clement, G. Ocular counter rolling in astronauts after short- and long-duration spaceflight. Sci. Rep. 8, 7747 (2018).
pubmed: 29773841
pmcid: 5958131
doi: 10.1038/s41598-018-26159-0
Young, L. R., Oman, C. M., Watt, D. G., Money, K. E. & Lichtenberg, B. K. Spatial orientation in weightlessness and readaptation to earth’s gravity. Science 225, 205–208 (1984).
pubmed: 6610215
doi: 10.1126/science.6610215
Seidler, R. D., Mulavara, A. P., Bloomberg, J. J. & Peters, B. T. Individual predictors of sensorimotor adaptability. Front. Syst. Neurosci. 9, 100 (2015).
pubmed: 26217197
pmcid: 4491631
doi: 10.3389/fnsys.2015.00100
Pechenkova, E. et al. Alterations of functional brain connectivity after long-duration spaceflight as revealed by fMRI. Front. Physiol. 4, 10:761 (2019).
Markham, C. H. & Diamond, S. G. Ocular counterrolling differs in dynamic and static stimulation. Acta Otolaryngol. Suppl. 545, 97–100 (2001).
pubmed: 11677754
Dai, M., Raphan, T., Kozlovskaya, I. & Cohen, B. Vestibular adaptation to space in monkeys. Otolaryngol. Head Neck Surg. 119, 65–77 (1998).
pubmed: 9674517
doi: 10.1016/S0194-5998(98)70175-5
Krejcova, H., Highstein, S. & Cohen, B. Labyrinthine and extra-labyrinthine effects on ocular counter-rolling. Acta Otolaryngol. 72, 165–171 (1971).
pubmed: 5000242
doi: 10.3109/00016487109122469
Yates, B. J., Jian, B. J., Cotter, L. A. & Cass, S. P. Responses of vestibular nucleus neurons to tilt following chronic bilateral removal of vestibular inputs. Exp. Brain Res. 130, 151–158 (2000).
pubmed: 10672468
doi: 10.1007/s002219900238
Diamond, S. G. & Markham, C. H. The effect of space missions on gravity-responsive torsional eye movements. J. Vestib. Res. 8, 217–231 (1998).
pubmed: 9626649
doi: 10.3233/VES-1998-8304
Young, L. R. et al. M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 1. Sensory adaptation to weightlessness and readaptation to one-g: an overview. Exp. Brain Res. 64, 291–298 (1986).
pubmed: 3492384
Hupfeld, K. E. et al. Brain and behavioral evidence for reweighting of vestibular inputs with long-duration spaceflight. Cereb. Cortex 32(4), 755–769 (2022).
pubmed: 34416764
doi: 10.1093/cercor/bhab239
Moore, S. T. et al. Artificial gravity: a possible countermeasure for postflight orthostatic intolerance. Acta Astronaut. 56, 867–876 (2005).
pubmed: 15835033
doi: 10.1016/j.actaastro.2005.01.012
Kornilova, L. N., Naumov, I. A., Azarov, K. A. & Sagalovitch, V. N. Gaze control and vestibular-cervical-ocular responses after prolonged exposure to microgravity. Aviat. Space Environ. Med. 83, 1123–1134 (2012).
pubmed: 23316540
doi: 10.3357/ASEM.3106.2012
Demertzi, A. et al. Cortical reorganization in an astronaut’s brain after long-duration spaceflight. Brain Struct. Funct. 221, 2873–2876 (2016).
pubmed: 25963710
doi: 10.1007/s00429-015-1054-3
Daddaoua, N., Dicke, P. W. & Thier, P. Non-human primates exhibit disconjugate ocular counterroll to head roll tilts. Vision Res. 51, 1986–1993 (2011).
pubmed: 21807017
doi: 10.1016/j.visres.2011.07.013
Palla, A., Bockisch, C. J., Bergamin, O. & Straumann, D. Dissociated hysteresis of static ocular counterroll in humans. J. Neurophysiol. 95, 2222–2232 (2006).
pubmed: 16338995
doi: 10.1152/jn.01014.2005
Pansell, T., Ygge, J. & Schworm, H. D. Conjugacy of torsional eye movements in response to a head tilt paradigm. Invest. Ophthalmol. Vis. Sci. 44, 2557–2564 (2003).
pubmed: 12766057
doi: 10.1167/iovs.02-0987
Diamond, S. G., Markham, C. H., Simpson, N. E. & Curthoys, I. S. Binocular counterrolling in humans during dynamic rotation. Acta Otolaryngol. 87, 490–498 (1979).
pubmed: 313656
doi: 10.3109/00016487909126457
Markham, C. H., Diamond, S. G. & Stoller, D. F. Parabolic flight reveals independent binocular control of otolith-induced eye torsion. Arch. Ital. Biol. 138, 73–86 (2000).
pubmed: 10604035
de Graaf, B., Bos, J. E. & Groen, E. Saccular impact on ocular torsion. Brain. Res. Bull. 40, 321–326; discussion 326–330 (1996).
Nowe, V. et al. The interutricular distance determined from external landmarks. J. Vestib. Res. 13, 17–23 (2003).
pubmed: 14646021
doi: 10.3233/VES-2003-13103
Moore, S. T. et al. Ocular and perceptual responses to linear acceleration in microgravity: alterations in otolith function on the COSMOS and Neurolab flights. J. Vestib. Res. 13(4–6), 377–393 (2003).
pubmed: 15096679
doi: 10.3233/VES-2003-134-620