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Current Pathobiology Reports

, Volume 6, Issue 3, pp 177–183 | Cite as

Vestibular and Sensorimotor Dysfunction During Space Flight

  • Millard F. Reschke
  • Gilles Clément
Effects of the Space Environment on Human Pathobiology (R Kerschmann, Section Editor)
  • 70 Downloads
Part of the following topical collections:
  1. Topical Collection on Effects of the Space Environment on Human Pathobiology

Abstract

Purpose of Review

This paper aims to review dysfunctions in spatial orientation, cognition, gaze stabilization, and posture and locomotor control recently documented in astronauts during and immediately after both short- and long-duration space flights.

Recent Findings

The spatial disorientation and cognitive deficits experienced by astronauts in microgravity are similar to those observed in individuals with vestibular disorders on Earth. After space flight, astronauts take more time to acquire visual targets while moving their head. Balance and locomotion control are impaired for approximately 15 days after long-duration space flight. Altered vestibular and proprioceptive inputs and changes in cortical sensory motor maps are presumed to be responsible for these deficits.

Summary

Illusions of motion, underestimation of distance, delay in acquiring visual targets, and impairments in locomotion are potentially dangerous during operation of the spacecraft, especially during long-duration missions involving transitions between gravitational levels, and during landing when accurate manual and locomotor control is critical.

Keywords

Vestibular system Otoliths Microgravity Eye-head coordination Posture Locomotion Adaptation 

Notes

Acknowledgements

This work was supported by NASA. The authors thank Kerry George for editing the manuscript.

Compliance with Ethical Standards

Conflict of Interest

Millard Reschke and Gilles Clément declare that they have no conflict of interest.

Human and Animal Rights and Informed Content

All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major Importance

  1. 1.
    Goldberg JM, Wilson VJ, Cullen KE, Angelaki DE, Broussard AM, Büttner-Ennever J, et al. The vestibular system: a sixth sense. New York, NY: Oxford University Press; 2002.Google Scholar
  2. 2.
    Clément G, Reschke MF. Neuroscience in Space. New York, NY: Springer; 2008.CrossRefGoogle Scholar
  3. 3.
    • Paloski WH, Oman CM, Bloomberg JJ, Reschke MF, Wood SJ, Harm DL, et al. Risk of sensory-motor performance failures affecting vehicle control during space missions: a review of the evidence. J Gravit Physiol. 2008;15:1–29. This is a comprehensive review of the research and operational evidence that demonstrate decreased visual acuity, eye-hand coordination, spatial and geographical orientation perception, and cognitive function during and after spaceflight. Google Scholar
  4. 4.
    Oman C. Spatial orientation and navigation in microgravity. In: Mast FW, Jäncke L, editors. Spatial processing in navigation, imagery, and perception. New York, NY: Springer; 2010. p. 209–48.Google Scholar
  5. 5.
    Harm DL, Parker DE. Perceived self-orientation and self-motion in microgravity, after landing and during preflight adaptation training. J Vestib Res. 1993;3:297–305.PubMedGoogle Scholar
  6. 6.
    Mittelstaedt H, Glasauer S. Crucial effects of weightlessness on human orientation. J Vestib Res. 1993;3:307–14.PubMedGoogle Scholar
  7. 7.
    McIntyre J, Zago M, Berthoz A, Lacquaniti F. Does the brain model Newton’s laws? Nature Neurosci. 2001;4:693–5.CrossRefPubMedGoogle Scholar
  8. 8.
    Lathan CE, Wang Z, Clément G. Changes in the vertical size of a three-dimensional object drawn in weightlessness by astronauts. Neurosci Lett. 2000;295:37–40.CrossRefPubMedGoogle Scholar
  9. 9.
    Clément G, Skinner A, Richard G, Lathan C. Geometric illusions in astronauts during long-duration spaceflight. NeuroReport. 2012;23:894–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Clément G, Skinner A, Lathan CE. Distance and size perception in astronauts during long-duration spaceflight. Life. 2013;3:524–37.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Clément G, Allaway HCM, Demel M, Golemis A, Kindrat AN, Melinyshyn AN, et al. Long-duration spaceflight increases depth ambiguity of reversible perspective figures. PLoS One. 2015;10(7):e0132317.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Harris LR, Jenkin M, Jenkin H, Zacher JE, Dyde RT. The effect of long-term exposure to microgravity on the perception of upright. npj Microgravity. 2017;3:3.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Clément G, Wood SJ. Eye movements and motion perception during off-vertical axis rotation after spaceflight. J Vestib Res. 2013;23:13–22.PubMedGoogle Scholar
  14. 14.
    Hallgren E, Kornilova L, Fransen E, Glukhikh D, Moore S, Clément G, et al. Decreased otolith function in 25 astronauts induced by long-duration spaceflight. J Neurophysiol. 2016;115:3045–51.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Kanas N, Manzey D. Space Psychology and Psychiatry. El Segundo, CA: Microcosm Press; New York, NY: Springer; 2008.Google Scholar
  16. 16.
    Jones PM, Fiedler E. Human performance in space. Rev Hum Fact Ergon. 2010;6:172–97.CrossRefGoogle Scholar
  17. 17.
    Manzey D, Lorenz B. Mental performance during short-term and long-term spaceflight. Brain Res Rev. 1998;28:215–21.CrossRefPubMedGoogle Scholar
  18. 18.
    Welch RB, Hoover M, Southward EF. Cognitive performance during prismatic displacement as a partial analogue of “space fog”. Aviat Space Environ Med. 2009;80:771–80.CrossRefPubMedGoogle Scholar
  19. 19.
    Smith PF, Zheng Y, Horii A, Darlington CL. Does vestibular damage cause cognitive dysfunction in humans? J Vestib Res. 2005;15:1–9.PubMedGoogle Scholar
  20. 20.
    Hanes DA, McCollum G. Cognitive-vestibular interactions: a review of patient difficulties and possible mechanisms. J Vestib Res. 2006;95:343–8.Google Scholar
  21. 21.
    Clément G, Fraysse MJ, Deguine O. Mental representation of space in vestibular patients with otolithic or rotatory vertigo. NeuroReport. 2009;20:457–61.CrossRefPubMedGoogle Scholar
  22. 22.
    Gurvich C, Maller JJ, Lithgow B, Haghgooied S, Kulkarnia J. Vestibular insights into cognition and psychiatry. Brain Res. 2013;1537:244–59.CrossRefPubMedGoogle Scholar
  23. 23.
    Brandt T, Schautzer F, Hamilton DA, Brüning R, Markowitsch HJ, Kalla R, et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain. 2005;28:2732–41.CrossRefGoogle Scholar
  24. 24.
    Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Res Rev. 2011;67:119–46.CrossRefPubMedGoogle Scholar
  25. 25.
    Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F. Representation of visual gravitational motion in the human vestibular cortex. Science. 2005;308:416–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Previc FH. The neuropsychology of 3-D space. Psychol Bull. 1998;124:123–64.CrossRefPubMedGoogle Scholar
  27. 27.
    Previc FH. Vestibular loss as a contributor to Alzheimer’s disease. Med Hypotheses. 2013;80:360–7.CrossRefPubMedGoogle Scholar
  28. 28.
    Balaban CD. Projections from the parabrachial nucleus to the vestibular nuclei: potential substrates for autonomic and limbic influences on vestibular responses. Brain Res. 2004;996:126–37.CrossRefPubMedGoogle Scholar
  29. 29.
    Brandt T, Strupp M, Dieterich M. Towards a concept of disorders of higher vestibular function. Front Integrat Neurosci. 2014;8(47):22–9.Google Scholar
  30. 30.
    Pelisson D, Prablanc C. Eye-hand coordination. In: Binder MD, Hirokawa N, Windhorst U, editors. Encyclopedia of neuroscience. Heidelberg: Springer; 2008. p. 1540–2.Google Scholar
  31. 31.
    Young LR, Oman CM, Watt DG, Money KE, Lichtenberg BK. Spatial orientation in weightlessness and readaptation to earth’s gravity. Science. 1984;225(4658):205–8.CrossRefPubMedGoogle Scholar
  32. 32.
    Benson AJ, Viéville T. European vestibular experiments on the Spacelab-1 mission: 6. Yaw axis vestibulo-ocular reflex. Exp Brain Res. 1986;64:279–83.PubMedGoogle Scholar
  33. 33.
    DiZio P, Lackner JR. The effects of gravitoinertial force level and head movements on post-rotational nystagmus and illusory after-rotation. Exp Brain Res. 1988;70:485–95.CrossRefPubMedGoogle Scholar
  34. 34.
    Oman CM, Kulbaski M. Space flight affects the 1-g postrotatory vestibulo-ocular reflex. Adv Otorhinolaryngol. 1988;42:5–8.PubMedGoogle Scholar
  35. 35.
    Raphan T, Dai MJ, The CB. Spatial orientation of the vestibular system. Ann N Y Acad Sci. 1992;56:140–57.CrossRefGoogle Scholar
  36. 36.
    • Reschke MF, Kolev OI, Clément G. Eye-head coordination in 31 space shuttle astronauts during visual target acquisition. Sci Rep. 2017;7:14283. This research study demonstrates a significant delay in acquiring visual targets after space flight, which is caused by a decrease in velocity and amplitude of both eye and head movements. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    André-Deshays C, Israël I, Charade O, Berthoz A, Popov K, Lipshits M. Gaze control in microgravity. 1. Saccades, pursuit, eye-head coordination. J Vestib Res. 1993;3:331–4.PubMedGoogle Scholar
  38. 38.
    Reschke MF, Kozlovskaya IB, Somers JT, Kornilova LN, Paloski WH, Berthoz A. Smooth pursuit deficits in space flights of variable length. J Gravit Physiol. 2002;9:133–6.Google Scholar
  39. 39.
    Paloski WH, Reschke MF, Black FO, Dow RS. Recovery of postural equilibrium control following space flight (DSO 605). In: Sawin CF, Taylor GR, Smith WL, editors. Extended duration orbiter medical project final report (1989–1995). NASA SP-1999-534. Houston: NASA Johnson Space Center; 5.4–1–5; 1999. p. 4–16.Google Scholar
  40. 40.
    Paloski WH, Black FO, Reschke MF, Calkins DS, Shupert C. Vestibular ataxia following shuttle flights: effects of microgravity on otolith-mediated sensorimotor control of posture. Am J Otol. 1993;14(1):9–17.PubMedGoogle Scholar
  41. 41.
    Kornilova LN. Vestibular function and sensory interaction in altered gravity. Adv Space Biol Med. 1997;6:275–313.CrossRefPubMedGoogle Scholar
  42. 42.
    Homick JL, Reschke MF. Postural equilibrium following exposure to weightless space flight. Acta Otolaryngol. 1977;83:455–64.CrossRefGoogle Scholar
  43. 43.
    Kozlovskaya IB, Kreidich Yu V, Oganov VS, Koserenko OP. Pathophysiology of motor functions in prolonged manned space flights. Acta Astronaut. 1981;8:1059–72.CrossRefPubMedGoogle Scholar
  44. 44.
    Baumgarten v RJ. European experiments in the spacelab mission 1. Overview Exp Brain Res. 1986;64:239–46.CrossRefGoogle Scholar
  45. 45.
    Jain V, Wood SJ, Feiveson AH, Black FO, Paloski WH. Diagnostic accuracy of dynamic posturography testing after short-duration spaceflight. Aviat Space Environ Med. 2010;81:625–31.CrossRefPubMedGoogle Scholar
  46. 46••.
    Wood SJ, Paloski WH, Clark JB. Assessing sensorimotor function on ISS with computerized dynamic posturography. Aerosp Med Hum Perform. 2015;86(Suppl 12):A1–9. This study reports the decrements in postural control performance during standardized sensory organization tests in 26 astronauts following long-duration missions on board the ISS. Google Scholar
  47. 47.
    Paloski WH, Wood SJ, Feiveson AH, Black FO, Hwang EY, Reschke MF. Destabilization of human balance control by static and dynamic head tilts. Gait Posture. 2006;23:315–23.CrossRefPubMedGoogle Scholar
  48. 48.
    Bloomberg JJ, Peters BT, Smith SL, Huebner WP, Reschke MF. Locomotor head-trunk coordination strategies following space flight. J Vestib Res. 1997;7:161–77.CrossRefPubMedGoogle Scholar
  49. 49.
    Black FO, Paloski WH, Reschke MF, Igarashi M, Guedry F, Anderson DJ. Disruption of postural readaptation by inertial stimuli following space flight. J Vestib Res. 1999;9:369–78.PubMedGoogle Scholar
  50. 50.
    McDonald PV, Basdogan C, Bloomberg JJ, Layne CS. Lower limb kinematics during treadmill walking after space flight: implications for gaze stabilization. Exp Brain Res. 1996;112:325–34.CrossRefPubMedGoogle Scholar
  51. 51.
    Newman DJ, Jackson DK, Bloomberg BJJ. Altered astronaut lower limb and mass center kinematics in downward jumping following space flight. Exp Brain Res. 1997;117:30–42.CrossRefPubMedGoogle Scholar
  52. 52.
    Layne CS, Mulavara AP, McDonald PV, Pruett CJ, Kozlovskaya IB, Bloomberg JJ. The effects of long-duration spaceflight during self-generated perturbations. J Appl Physiol. 2001(1985);90:997–1006.CrossRefPubMedGoogle Scholar
  53. 53.
    Courtine G, Pozzo T. Recovery of the locomotor function after prolonged microgravity exposure. I. Head-trunk movement and locomotor equilibrium during various tasks. Exp Brain Res. 2004;158:86–99.CrossRefPubMedGoogle Scholar
  54. 54.
    Miller CA, Peters BT, Brady RR, Richards JR, Ploutz-Snyder RJ, Mulavara AP, et al. Changes in toe clearance during treadmill walking after long-duration spaceflight. Aviat Space Environ Med. 2010;81:919–28.CrossRefPubMedGoogle Scholar
  55. 55.
    Peters BT, Miller CA, Brady RA, Richards JT, Mulavara AP, Bloomberg JJ. Dynamic visual acuity during walking after long-duration spaceflight. Aviat Space Environ Med. 2011;82:463–6.CrossRefPubMedGoogle Scholar
  56. 56••.
    Mulavara AP, Feiveson A, Feidler J, Cohen HS, Peters BT, Miller CA, et al. Locomotor function after long-duration space flight: effects and motor learning during recovery. Exp Brain Res. 2010;202:649–59. This study on 18 astronauts demonstrated that the time to walk an obstacle course increased by 48% after long-duration spaceflight, and returned to preflight level at approximately 15 days post-flight. CrossRefPubMedGoogle Scholar
  57. 57.
    Reschke MF, Good EF, Clément G. Vestibular symptoms in astronauts following space shuttle and international Space Station missions. Otolaryngol Head Neck Surg. 2017;1:1–8.Google Scholar
  58. 58.
    Fitts RH, Riley DR, Widrick JJ. Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol. 2001;204:3201–8.PubMedGoogle Scholar
  59. 59.
    D'Amelio F, Fox RA, Wu LC, Daunton NG, Corcoran ML. Effects of microgravity on muscle and cerebral cortex: a suggested interaction. Adv Space Res. 1998;22:235–44.CrossRefPubMedGoogle Scholar
  60. 60.
    Reschke MF, Bloomberg JJ, Harm DL, Huebner WP, Krnavek J, Paloski WH, et al. Visual-vestibular integration as a function of adaptation to space flight and return to earth. In: SaWin CF, Taylor GR, Smith WL, editors. Extended duration orbiter medical project. Final report (1989–1995). NASA SP-1999-534. Houston: NASA Johnson Space Center; 5.3–1–5; 1999. p. 3–41.Google Scholar
  61. 61.
    Wood SJ, Loehr JA, Guilliams ME. Sensorimotor reconditioning during and after spaceflight. NeuroRehabilitation. 2011;29:185–95.PubMedGoogle Scholar
  62. 62.
    Mulavara AP, Ruttley T, Cohen HS, Peters BT, Miller CA, Brady RR, et al. Vestibular-somatosensory convergence in head movement control during locomotion after long-duration space flight. J Vestib Res. 2012;22:153–66.PubMedGoogle Scholar
  63. 63.
    Ross MD. Morphological changes in rat vestibular system following weightlessness. J Vestib Res. 1993;3:241–51.PubMedGoogle Scholar
  64. 64.
    Ross MD. A spaceflight study of synaptic plasticity in adult rat vestibular maculas. Acta Otolaryngol Suppl. 1994;516:1–14.PubMedGoogle Scholar
  65. 65.
    Ross MD. Changes in ribbon synapses and rough endoplasmic reticulum of rat utricular macular hair cells in weightlessness. Acta Otolaryngol. 2000;120:490–9.CrossRefPubMedGoogle Scholar
  66. 66.
    Boyle R, Mensinger AF, Yoshida K, Usui S, Intravaia A, Tricas T, et al. Neural readaptation to Earth’s gravity following return from space. J Neurophysiol. 2001;86:2118–22.CrossRefPubMedGoogle Scholar
  67. 67.
    Correia MJ, Perachio AA, Dickman JD, Kozlovskaya IB, Sirota MG, Yakushin SB, et al. Changes in monkey horizontal semicircular afferent responses following space flight. J Appl Phys. 1992;73:121S–31S.Google Scholar
  68. 68.
    Balaban PM, Malyshev AY, Ierusalimsky VN, Aseyev N, Korshunova TA, Bravarenko NI, et al. Functional changes in the snail statocyst system elicited by microgravity. PLoS One. 2011;6:e17710.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69•.
    Aseyev N, Vinarskaya AK, Roshchin M, Korshunova TA, Malyshev AY, Zuzina AB, et al. Adaptive changes in the vestibular system of land snail to a 30-day spaceflight and readaptation on return to earth. Front Cell Neurosci. 2017;11(1):348. This study demonstrated hypersensitivity to tilt in the hair cells of the peripheral vestibular end organ of land snail after spaceflight, suggesting an upregulation of the graviceptor following adaptation to microgravity. CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Brandt T, Dieterich M, Strupp M. Vertigo and Dizziness. Common complaints. 2nd ed. New York, NY: Springer; 2013.CrossRefGoogle Scholar
  71. 71.
    Kass J. The reorganization of sensory and motor maps in adult animals. In: Gazzaniga MS, editor. The cognitive neurosciences. Cambridge, MA: MIT Press; 1995. p. 51–72.Google Scholar
  72. 72••.
    Koppelmans V, Bloomberg JJ, Mulavara AP, Seidler RD. Brain structural plasticity with spaceflight. npj Microgravity. 2016;2:2. This retrospective study showed an increase in gray matter volume in sensorimotor brain regions in astronauts after long-duration spaceflight. CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Koppelmans V, Erdeniz B, De Dios YE, Wood SJ, Reuter-Lorenz PA, Kofman I, et al. Study protocol to examine the effects of spaceflight and a spaceflight analog on neurocognitive performance: extent, longevity, and neural bases. BMC Neurol. 2013;13:205.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Roberts DR, Albrecht MH, Collins HR, Asemani D, Chatterjee AR, Spampinato MV, et al. Effects of spaceflight on astronaut brain structure as indicated on MRI. N Engl J Med. 2017;377:1746–53.CrossRefPubMedGoogle Scholar
  75. 75.
    Mader TH, Gibson CR, Pass AF, Kramer LA, Lee AG, Fogarty J, et al. Optic disc edema, globe flattening, choroidal folds, and hyperopic shifts observed in astronauts after long-duration space flight. Ophthalmology. 2011;118:2058–69.CrossRefPubMedGoogle Scholar
  76. 76.
    Mader T, Gibson C, Otto C, Sargsyan AE, Miller NR, Subramanian PS, et al. Persistent asymmetric optic disc swelling after long-duration space flight: implications for pathogenesis. J Neuroophthalmol. 2017;37:133–9.CrossRefPubMedGoogle Scholar
  77. 77.
    Lee AG, Tarver WJ, Mader TH, Gibson CR, Hart SF, Otto CA. Neuro-ophthalmology of space flight. J Neuroophthalmol. 2016;36:85–91.CrossRefPubMedGoogle Scholar
  78. 78.
    Reschke MF, Bloomberg JJ, Paloski WH, Mulavara AP, Feiveson AH, Harm DL. Postural reflexes, balance control, and functional mobility with long-duration head-down bed rest. Aviat Space Environ Med. 2009;80(Suppl 5):A45–54.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Neuroscience LaboratoriesNASA Johnson Space CenterHoustonUSA
  2. 2.KBRwyleHoustonUSA

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