Ocular counter-roll is less affected in experienced versus novice space crew after long-duration spaceflight.

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.

The Role of Different Afferent Systems in the Modulation of the Otolith-Ocular Reflex After Long-Term Space Flights.

Background: The vestibular (otolith) function is highly suppressed during space flight (SF) and the study of these changes is very important for the safety of the space crew during SF missions. The vestibular function (particularly, otolith-ocular reflex-OOcR) in clinical and space medicine is studied using different methodologies. However, different methods and methodologies can influence the outcome results. Objective: The current study addresses the question of whether the OOcR results obtained by different methods are different, and what the role is of the different afferent systems in the modulation of the OOcR. Methods: A total of 25 Russian cosmonauts voluntarily took part in our study. They are crewmembers of long duration space missions on the International Space Station (ISS). Cosmonauts were examined in pre- and post-flight "Sensory Adaptation" and "Gaze Spin" experiments, twice before (preflight) and three times after SF (post-flight). We used two different video oculography (VOG) systems for the recording of the OOcR obtained in each experiment. Results: Comparison of the two VOG systems didn't result into significant and systematic differences in the OOcR measurements. Analysis of the static torsion otolith-ocular reflex (OOR), static torsion otolith-cervical-ocular reflex (OCOR) and static torsion otolith-ocular reflex during eccentric centrifugation (OOREC) shows that the OOREC results in a lower OOcR response compared to the OOR and OCOR (before flight and late post-flight). However, all OOcRs were significantly decreased in all cosmonauts early post-flight. Conclusion: Analysis of the results of ocular counter rolling (OCR) obtained by different methods (OOR, OCOR, and OOREC) showed that different afferent systems (tactile-proprioception, neck-cervical, visual and vestibular afferent input) have an impact on the OOcR.

Alterations of Functional Brain Connectivity After Long-Duration Spaceflight as Revealed by fMRI.

The present study reports alterations of task-based functional brain connectivity in a group of 11 cosmonauts after a long-duration spaceflight, compared to a healthy control group not involved in the space program. To elicit the postural and locomotor sensorimotor mechanisms that are usually most significantly impaired when space travelers return to Earth, a plantar stimulation paradigm was used in a block design fMRI study. The motor control system activated by the plantar stimulation involved the pre-central and post-central gyri, SMA, SII/operculum, and, to a lesser degree, the insular cortex and cerebellum. While no post-flight alterations were observed in terms of activation, the network-based statistics approach revealed task-specific functional connectivity modifications within a broader set of regions involving the activation sites along with other parts of the sensorimotor neural network and the visual, proprioceptive, and vestibular systems. The most notable findings included a post-flight increase in the stimulation-specific connectivity of the right posterior supramarginal gyrus with the rest of the brain; a strengthening of connections between the left and right insulae; decreased connectivity of the vestibular nuclei, right inferior parietal cortex (BA40) and cerebellum with areas associated with motor, visual, vestibular, and proprioception functions; and decreased coupling of the cerebellum with the visual cortex and the right inferior parietal cortex. The severity of space motion sickness symptoms was found to correlate with a post- to pre-flight difference in connectivity between the right supramarginal gyrus and the left anterior insula. Due to the complex nature and rapid dynamics of adaptation to gravity alterations, the post-flight findings might be attributed to both the long-term microgravity exposure and to the readaptation to Earth's gravity that took place between the landing and post-flight MRI session. Nevertheless, the results have implications for the multisensory reweighting and gravitational motor system theories, generating hypotheses to be tested in future research.

Decreased otolith-mediated vestibular response in 25 astronauts induced by long-duration spaceflight.

The information coming from the vestibular otolith organs is important for the brain when reflexively making appropriate visual and spinal corrections to maintain balance. Symptoms related to failed balance control and navigation are commonly observed in astronauts returning from space. To investigate the effect of microgravity exposure on the otoliths, we studied the otolith-mediated responses elicited by centrifugation in a group of 25 astronauts before and after 6 mo of spaceflight. Ocular counterrolling (OCR) is an otolith-driven reflex that is sensitive to head tilt with regard to gravity and tilts of the gravito-inertial acceleration vector during centrifugation. When comparing pre- and postflight OCR, we found a statistically significant decrease of the OCR response upon return. Nine days after return, the OCR was back at preflight level, indicating a full recovery. Our large study sample allows for more general physiological conclusions about the effect of prolonged microgravity on the otolith system. A deconditioned otolith system is thought to be the cause of several of the negative effects seen in returning astronauts, such as spatial disorientation and orthostatic intolerance. This knowledge should be taken into account for future long-term space missions.

Dysfunctional vestibular system causes a blood pressure drop in astronauts returning from space.

It is a challenge for the human body to maintain stable blood pressure while standing. The body's failure to do so can lead to dizziness or even fainting. For decades it has been postulated that the vestibular organ can prevent a drop in pressure during a position change--supposedly mediated by reflexes to the cardiovascular system. We show--for the first time--a significant correlation between decreased functionality of the vestibular otolith system and a decrease in the mean arterial pressure when a person stands up. Until now, no experiments on Earth could selectively suppress both otolith systems; astronauts returning from space are a unique group of subjects in this regard. Their otolith systems are being temporarily disturbed and at the same time they often suffer from blood pressure instability. In our study, we observed the functioning of both the otolith and the cardiovascular system of the astronauts before and after spaceflight. Our finding indicates that an intact otolith system plays an important role in preventing blood pressure instability during orthostatic challenges. Our finding not only has important implications for human space exploration; they may also improve the treatment of unstable blood pressure here on Earth.

Gaze control and vestibular-cervical-ocular responses after prolonged exposure to microgravity.

BACKGROUND: Microgravity does not affect visual function directly. However, because of the altered afferentation from vestibular, support, and tactile-proprioceptive systems, it could lead to disturbances in visual tracking and inhibit the cosmonaut's activity. Therefore, it is necessary to obtain quantitative evaluations of spaceflight effects upon gaze control and vestibular-cervical-ocular responses. METHODS: Examination of visual tracking with the head in a fixed position was performed in 26 Russian ISS cosmonauts before and after a prolonged spaceflight (129-215 d). As vestibular tests, we used several roll-tilts and yaw head rotations. Eye movements were recorded using both video-oculographic and electro-oculographic methods. RESULTS: It was shown that until 9 d after landing (R+9) spontaneous eye movements were increased (spontaneous nystagmus, gaze nystagmus, square wave jerks); otolith function was suppressed (inversion, absence, or significant decrease of the compensatory torsional ocular counter-rolling); vestibular reactivity was elevated (an increased intensity of the vestibular nystagmus during head yaw rotations); amplitude and velocity characteristics of gaze control (saccades, smooth pursuit, gaze holding) were significantly decreased; total reaction time was significantly increased up to 2-3 times; and gaze holding ability was degraded. For several cosmonauts, smooth pursuit was collapsed and their gaze approached the stimulus or pursued its motion utilizing a sequence of saccades at least until R+5. DISCUSSION: Prolonged exposure to microgravity considerably affects all forms of visual tracking. Revealed disturbances in precision of visual tracking and adoption of the new tracking strategy substantially prolong (up to 2-3 times) the period required to acquire, recognize, and to fixate gaze on the target.

Ocular torsion response to active head-roll movement under one-g and zero-g conditions.

Transitions to and from microgravity, as experienced during a spaceflight mission, radically alter the demands on sensorimotor coordination. In this contribution, attention is directed to the vestibulo-oculomotor response to active head roll-tilt, generally referred to as ocular counterroll (OCR). Results are presented from a single-case longitudinal study over a 435-day spaceflight and from three further subjects over a 30-day period in microgravity. 1. Under one-g test conditions, with the head initially in the comfortable-upright position, active head-to-trunk roll tilt elicits a combined canal- and otolith-mediated oculomotor response, which manifests as a volley of torsional nystagmus beats combined with a tonic OCR. In microgravity it appears that only the transitory canal-mediated torsional nystagmus response remains. In both conditions the initial nystagmus response commences with an anticompensatory torsional fast phase. 2. Under zero-g conditions the head movements were comparable to those under one-g conditions but a consistent reduction in head velocity was observed. Despite this, eye velocity and eye-head velocity gain for the torsional component were found to be enhanced by up to 50% over the first thirty days in prolonged microgravity. 3. The results obtained from the 435-day mission indicate that the initially enhanced response decreases--over the course of several months--to preflight baseline level. The findings indicate that otolith- and canal-ocular responses are not simply added linearly, but rather that the afferent otolith signal also plays an inhibitory, or stabilising role on the canal-mediated response. Further, presuming a re-weighting of otolithic afferent information during prolonged microgravity, it is proposed that a corollary inverse re-weighting of corollary neck-proprioceptive afferences provides an effective substitute. In contrast to the idea that the torsional VOR is an evolutionary relic, it is postulated from the above findings that the anticompensatory saccade and the inherent low gain of OCR result as a compromise between intended reorientation to a tilted visual field and VOR compensation.

Sensorimotor recovery following spaceflight may be due to frequent square-wave saccadic intrusions.

Square-wave jerks (SWJs) are small, involuntary saccades that disrupt steady fixation. We report the case of an astronaut (approximately 140 d on orbit) who showed frequent SWJs, especially postflight, but who showed no impairment of vision or decrement of postflight performance. These data support the view that SWJs do not impair vision because they are paired movements, consisting of a small saccade away from the fixation position followed, within 200 ms, by a corrective saccade that brings the eye back on target. Since many returning astronauts show a decrement of dynamic visual function during postflight locomotion, it seems possible that frequent SWJs improved this astronaut's visual function by providing postsaccadic enhancement of visual fixation, which aided postflight performance. Certainly, frequent SWJs did not impair performance in this astronaut, who had no other neurological disorder.