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Review Article
Review on the impact of spaceflight stressors on the vestibular system: beyond microgravity to space radiation
Hui Ho Vanessa Chang1orcid, Kyu-Sung Kim1,2orcid
Research in Vestibular Science 2024;23(3):71-78.
DOI: https://doi.org/10.21790/rvs.2024.013
Published online: September 15, 2024

1Research Institute for Aerospace Medicine, Inha University, Incheon, Korea

2Department of Otolaryngology-Head and Neck Surgery, Inha University Hospital, Incheon, Korea

Corresponding author: Kyu-Sung Kim Department of Otolaryngology-Head and Neck Surgery, Inha University Hospital, 27 Inhang-ro, Jung-gu, Incheon 22332, Korea. E-mail: stedman@inha.ac.kr
• Received: July 25, 2024   • Revised: August 20, 2024   • Accepted: August 20, 2024

© 2024 The Korean Balance Society

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Understanding the effects of microgravity on the vestibular system has been a primary focus of space research, driven by the need to counteract the often-debilitating impacts of altered gravity environments and maintain operational performance in space. Research using both space-based and ground-based models has identified structural and functional changes in the vestibular system, highlighting its significant capacity for sensorimotor adaptation. As human space exploration progresses towards missions beyond low Earth orbit for extended periods, additional stressors, such as space radiation, may impact the vestibular system. Early studies on space radiation using animal models and insights from radiotherapy have shown that the vestibular system is more vulnerable to radiation than previously understood. This paper provides a brief review of (1) dysfunctions in spatial orientation, gaze stabilization, posture, and locomotion observed in astronauts; (2) ground-based experiments on animals that likely explain these vestibular and sensorimotor dysfunctions; and (3) studies examining the effects of radiation on the vestibular system and its implications for vestibular function in space.
  • Keywords: Vestibular system; Space flight; Radiation; Weightlessness; Space medicine
Space is a complex environment posing several hazardous stressors, such as space radiation, isolation and confinement, distance from Earth, gravity fields, and hostile/closed environments (Fig. 1). These spaceflight hazards substantially impact the human body, prompting rigorous attempts to characterize the biological effects of these stressors, understand their mechanisms, and develop corresponding countermeasures. One stressor that has been relatively more extensively studied is the effect of microgravity on our bodies, as it represents a major environmental shift from Earth with almost immediate effects on motor control and perception.
Indeed, during our everyday activities on Earth, gravity acts as a world-based reference for controlling gaze, posture, and maintaining balance and perceiving spatial orientation [1]. However, during space exploration missions, astronauts are exposed to varying levels of gravity. This leads to significant changes in sensory input, especially from the vestibular system, which causes a mismatch between what the brain, hard-wired to the force of gravity, expects and the actual sensory inputs [2]. This mismatch causes astronauts to experience impaired balance and gait, gaze and eye-head coordination, and motion sickness, but astronauts show robust sensorimotor adaptation in the days following such changes in gravity [3].
However, exposure to changes in gravity is not the sole stressor in space. As exploration campaigns increasingly target missions beyond low Earth orbit (LEO) and for longer durations, the health risks associated with the mentioned space stressors are expected to increase, especially concerning space radiation. It remains unclear how space radiation will affect the health and operation of astronaut crews during spaceflight, as exposure to space radiation affects multiple organs and physiological systems in complex ways. To date, it is believed that the temporal bone is resistant to radiation and its effects on the structure and functions of the vestibular system are not significant enough to warrant the same level of attention as the effects of microgravity. However, radiotherapy studies targeting the head-neck area and early animal studies using high-energy protons indicate potential harm to both the structure and the peripheral and central processing of the vestibular system [4-7].
The objective of this paper is to review how space stressors can affect the vestibular system. We first consider space-based studies examining dysfunctions in gaze stabilization, postural control, and perception reported by astronauts, as well as ground-based models that have advanced our understanding of the neural mechanisms underlying sensory adaptation. Then, we will consider the potential effects of space radiation on the vestibular system, drawing insights from radiotherapy and early animal studies to understand the implications of radiation exposure following long-duration space missions.
An altered gravitational environment in space leads to changes in vestibular input, particularly from the otolith organs of the vestibular system. In microgravity, the otoliths are unloaded and no longer function as gravireceptors, thus failing to provide useful information about static head orientation (i.e., tilt). This change in input disrupts orientation, gaze, balance, and locomotion, requiring the central nervous system (CNS) to recalibrate and adapt. Indeed, after a few days, these functional disturbances typically return to baseline following a robust exponential recovery curve [8,9]. However, the longer the duration of space travel, the more intense the sensorimotor disturbances become, and the time required for complete recovery may extend to weeks or months [10].
Spatial Orientation
In the absence of gravity, our brain cannot determine our head and body orientation relative to gravity using vestibular and other sensory information such as proprioception [11]. As a result, astronauts tend to rely on visual cues. While they may be aware of their position relative to their surroundings, they still experience sensations of inversion, tilt, and various combinations of body and vehicle orientation [12-15]. These illusions can occur immediately after transitioning into microgravity but tend to diminish as astronauts adapt to the new environment [12]. Approximately 80% of astronauts report experiencing such illusory sensations of self and surroundings [13], which seem to be limited to those with appropriate vestibular function and are not observed in those with vestibular areflexia [14]. It is important to note that impaired perception during gravitational transitions compromises an astronaut’s ability to control the spacecraft itself [10]. Tactile aids, such as small tactors attached to the torso that vibrate when the body tilts relative to gravity, could alleviate spatial disorientation and destabilizing sensations. Indeed, such tactile feedback has been shown to restore early postflight performance to pre-mission levels [10].
Gaze Stabilization
Substantial evidence exists that spaceflight induces changes in the control of oculomotor responses. In microgravity, the vestibulo-ocular reflex (VOR) in the yaw axis does not change, indicating that semicircular canal-mediated responses are not affected [16,17]. However, the time constant of horizontal nystagmus decay is shorter in microgravity [18]. In contrast, both the gain and the time constant of the VOR in response to pitch and roll head movements are lower in microgravity, indicating decreased contributions from otolith inputs [19]. Indeed, otolith-mediated responses such as ocular counter-roll (OCR) are absent in microgravity [20] and reduced after spaceflight [21]. OCR can take several weeks to recover but eventually returns to pre-flight baseline [21-25]. Additionally, significant deficits in other domains of eye-head coordination, such as the generation of saccades, smooth pursuits, and gaze fixation, are found in microgravity conditions [22,26]. Upon returning to Earth, astronauts exhibit slowed eye and head movement velocities and increased latency when trying to acquire visual targets, relying heavily on saccadic eye movements to manage smooth pursuit stimuli [27-29].
Posture and Locomotion
Postural instability is frequently reported after spaceflight, with effects becoming more pronounced following longer mission durations [30]. Astronauts often struggle to maintain their posture when their eyes are closed and/or under disrupted somatosensory conditions, suggesting that balance control after spaceflight relies heavily on sensory reweighting [30,31]. Changes in the otolith-spinal reflex (the Hoffmann reflex) may also contribute to postural decrements after spaceflight. Muscle activity associated with the Hoffmann reflex decreased after seven days in space [32,33]. Locomotion is also significantly affected, with changes in step-cycle, walking speed, and head movement during walking being reported [34,35]. For short-duration missions, gait changes return to normal relatively quickly (within 12 hours), but it can take weeks for gait to return to normal after long-duration missions [36].
Ground-Based Animal Studies in Understanding the Effect of Microgravity on Vestibular Functions
Extensive research has investigated how the vestibular system responds and adapts to microgravity, aiming to understand the underlying mechanisms. Early experiments in rats and frogs suggested that this unloading increases the mass of the otoconia after relatively short 7-day microgravity exposure [37-39]. Conversely, in hypergravity conditions, a decrease in otoconial mass has been observed [1].
In addition to structural changes, microgravity induces changes in peripheral vestibular processing. Initially, after entering microgravity, both the baseline activities and sensitivities of otolith afferents substantially increase [3]. This hypersensitivity then returns to baseline levels after approximately five days and/or 24 hours post-return to Earth [40,41].
Expectedly, changes in central vestibular processing involving the integration of inputs from both otolith and canal afferents by neurons in the vestibular nuclei were also reported. Single-unit recordings from rhesus monkeys on several Russian “Cosmos/Bion” missions showed increases in vestibular nuclei neuron sensitivities to both linear and rotational head motion during the first days of spaceflight, with a subsequent return to normal baseline (reviewed in [42]). This adaptation over time likely contributes to the changes in utricular function observed in astronauts immediately after returning from spaceflight [20,21].
The effect of microgravity on vestibular nuclei activity has also been studied by quantifying the expression of the early gene c-fos, a neural activity marker. Ground-based models show that galvanic stimulation and centripetal acceleration increase Fos immunoreactivity in the vestibular nuclei [42-44]. Space experiments have similarly reported increased Fos expression in the vestibular nuclei of rats 24 hours postlaunch, with levels returning to baseline after 13 days postlaunch and postlanding, indicating adaptation over time in response to altered gravity [45]. Additionally, changes in the number of N-methyl-D-aspartate receptors, an indicator of neural plasticity, in the vestibular nuclei were reported following centrifugation [46].
Taken together, exposure to microgravity leads to significant alterations in vestibular function, impacting spatial orientation, gaze stabilization, and postural control. These disturbances primarily result from the unloading of otolith organs, which disrupts the CNS’s ability to process gravitational cues. While initial disturbances in vestibular function generally diminish over time as the body adapts, prolonged exposure to microgravity can extend recovery periods, emphasizing the need for further research on long-term adaptation mechanisms. Ground-based and space-based animal studies have provided valuable insights into the neural adaptations that occur in response to these changes, highlighting the complex interplay between peripheral and central vestibular processing in maintaining sensorimotor stability in altered gravity environments. It has been suggested that the increased sensitivity of otolith afferents induced by microgravity results from presynaptic adjustments in synaptic strength within hair cells, likely due to changes in otoconial mass, which in turn affects central vestibular functions. However, it remains unknown whether vestibular afferent sensitivities change during the first days of spaceflight in mammals, leaving open the question of how microgravity influences vestibular functions.
Exposure to varying levels of gravity significantly stresses the vestibular system, but it is not the only stressor in the complex environment of space. Space radiation also poses a primary, inevitable stressor with a considerable impact. Studies using accelerator-produced radiation sources have shown that space radiation affects multiple organs and physiological systems [47]. However, there has been limited research on its effects on the vestibular system, largely due to the more pronounced impact of microgravity on the system and the common belief that the inner ear, particularly the vestibular apparatus, is relatively resistant to radiation [48].
Despite the assumption that the vestibular system is relatively resistant to radiation, studies on the effects of radiation on the temporal bone have been conducted since the early 1900s, revealing that both the vestibular apparatus and the central vestibular pathways are susceptible to damage. Indeed, research in guinea pigs and chinchillas has documented degeneration in sensory cells after irradiation [48-50]. Functional testing, such as post-rotational and caloric nystagmus in dogs and rabbits, showed a decrease or loss of response [5,7].
Structural and functional changes in response to radiation have also been observed in humans, particularly in patients with brain tumors treated with doses of 50 to 60 Gy. For example, patients treated for parotid pleomorphic adenoma exhibited semicircular canal paresis [51]. Additionally, an autopsy study demonstrated the absence of the organ of Corti, macula of the utricle, and the cristae of the semicircular canals [52]. Functionally, patients often report symptoms like vertigo or dizziness following radiotherapy [53,54], and tests such as electronystagmography and calorimetry have shown abnormalities [54-57].
The cases and animal studies described illustrate vestibular dysfunction both peripherally and centrally due to radiation. However, the type of radiation we are exposed to on Earth is very different from that in space. The three primary radiation sources that make up the complex radiation environment in space are galactic cosmic rays (GCRs), solar particle events (SPEs), and trapped radiation within the Van Allen radiation belts, mostly consisting of high-energy protons [58] (Fig. 2). GCR originates from outside our solar system and produces high linear energy transfer radiation. GCR is comprised of 1% electrons, 85% to 90% protons, and 10% to 13% helium ions, with 1% heavier nuclei having charges ranging from Z=3 (lithium) to about Z=28 (nickel), known as high charge and energy particles [59]. Crews on the International Space Station (ISS) are exposed to high-energy radiation originating from GCRs and SPEs. Exposure doses in the ISS have been estimated to be about 0.5 mSv/day [60]. On a 6- to 12-month mission, radiation doses range from ~30 to 120 mGy, but the absorbed doses are expected to be significantly higher outside of LEO and Earth’s protective magnetic field. For instance, a 1-year stay on the lunar surface ranges from 100 to 120 mGy, and 300 to 450 mGy for a ~3-year Mars mission [61].
To date, most studies on the biological effects of space radiation have been conducted using monoenergetic beams and acute, single-ion exposures (i.e., proton, helium, or iron), often at substantially higher doses than those realistically encountered in space. Much attention has been focused on four major areas: acute radiation syndrome, carcinogenesis, degenerative tissue alterations, and CNS performance loss, with comparatively less research on the auditory and vestibular systems. However, one study examined the biological effect of protons with energies of 130 MeV on the vestibular apparatus [6]. Using dogs as their animal model, they investigated the threshold sensitivity and duration of nystagmus and found attenuation in their responses. While structural changes to the temporal bone mimicking space radiation have not been reported to date, the functional changes observed in some animal models suggest a possible impact of space radiation on central vestibular processing.
As human space exploration advances toward longer missions beyond LEO, the effects of space radiation on vestibular system must also be considered. A better understanding of how the vestibular and other sensorimotor systems adapt in space, and how to mitigate these effects, is crucial for the success of missions and the safety of astronauts.
Achieving a comprehensive understanding and developing mitigation strategies for vestibular dysfunctions in space presents significant challenges, particularly due to the complexities involved in replicating the space environment on Earth. Typically, altered gravitational fields are simulated on Earth using techniques like centrifugation and parabolic flights. However, these methods fall short of fully representing the conditions in space. For example, in space, astronauts are subjected to only brief exposures to hypergravity before transitioning into prolonged periods of microgravity. Studies that use centrifugation on Earth might not accurately represent this transition or the continuous microgravity environment astronauts face during space missions. Similarly, while parabolic flights provide a useful platform for microgravity research, the very short duration of microgravity exposure they offer—often just a few seconds at a time—limits their usefulness for long-term studies.
Compounding these challenges is the difficulty in accurately simulating the space radiation environment. There are currently no suitable accelerator-produced radiation sources that can replicate the spectrum of GCR encountered in space within terrestrial laboratories. Typically, these laboratories can only expose biological specimens to acute doses of single-energy accelerated ions, which does not mimic the continuous and varied radiation exposure in space.
Furthermore, the primary reliance on animal models—mostly rodents—for radiation risk assessment introduces additional complexities. Rodents exhibit high genetic instability, which may significantly differ from human responses, thus complicating the translation of these results to predict human outcomes.
To improve the fidelity of space environment simulations and the relevance of research findings, there is a pressing need to develop new methodologies and technologies. These advancements would better replicate the extended periods of microgravity and the complex radiation profiles astronauts experience. Enhancing our understanding of how the vestibular system and other sensorimotor systems respond to these unique conditions will be crucial for ensuring the health and safety of astronauts as they undertake longer and more distant missions beyond LEO.

Funding/Support

This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (No. 2018R1A6A1A03025523 and RS-2023-00266209).

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

Availability of Data and Materials

All data generated or analyzed during this study are included in this published article. For other data, these may be requested through the corresponding author.

Authors’ Contributions

Conceptualization: HHVC, KSK

Writing–original draft: HHVC, KSK

All authors read and approved the final manuscript.

Fig. 1.
The main hazards of future long-duration spaceflight are (1) radiation, (2) isolation and confinement, (3) distance from Earth, (4) altered gravity fields, and (5) hostile/closed environments.
rvs-2024-013f1.jpg
Fig. 2.
Types of radiation in space. The space radiation environment is comprised of three primary sources of ionizing radiation: galactic cosmic rays, energetic protons associated with a solar particle event, and trapped radiation within the Van Allen radiation belts.
rvs-2024-013f2.jpg
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        Review on the impact of spaceflight stressors on the vestibular system: beyond microgravity to space radiation
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      Review on the impact of spaceflight stressors on the vestibular system: beyond microgravity to space radiation
      Image Image
      Fig. 1. The main hazards of future long-duration spaceflight are (1) radiation, (2) isolation and confinement, (3) distance from Earth, (4) altered gravity fields, and (5) hostile/closed environments.
      Fig. 2. Types of radiation in space. The space radiation environment is comprised of three primary sources of ionizing radiation: galactic cosmic rays, energetic protons associated with a solar particle event, and trapped radiation within the Van Allen radiation belts.

      Fig. 1.

      Fig. 2.

      Review on the impact of spaceflight stressors on the vestibular system: beyond microgravity to space radiation
      Res Vestib Sci : Research in Vestibular Science
      © Korean Balance Society.
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