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Neurovestibular and Sensorimotor Studies in Space and Earth Benefits

This review summarizes what has been learned from studies of human neurovestibular system in weightless conditions, including balance and locomotion, gaze control, vestibular-autonomic function and spatial orientation, and gives some examples of the potential Earth benefits of this research. Results show that when astronauts and cosmonauts return from space flight, both the peripheral and central neural processes are physiologically and functionally altered. There are clear distinctions between the virtually immediate adaptive compensations to weightlessness and those that require longer periods of time to adapt. However, little is known to date about the adaptation of sensory-motor functions to long-duration space missions in weightlessness and to the transitions between various reduced gravitational levels, such as on the Moon and Mars. Results from neurovestibular research in space have substantially enhanced our understanding of the mechanisms and characteristics of postural, gaze, and spatial orientation deficits, analogous to clinical cases of labyrinthine-defective function. Also, space neurosciences research has participated in the development and application of significant new technologies, such as video recording and processing of three-dimensional eye movements and posture, hardware for the unencumbered measurement of head and body movement, and procedures for investigating otolith function on Earth. In particular, devices such as centrifugation or off-vertical axis rotation could enhance clinical neurological testing because it provides linear acceleration which specifically stimulates the otolith organs in a frequency range close to natural head and body movement.

Clement, Gilles↗

Sensorimotor Adaptation Following Exposure to Ambiguous Inertial Motion Cues

The central nervous system must resolve the ambiguity of inertial motion sensory cues in order to derive accurate spatial orientation awareness. Our general hypothesis is that the central nervous system utilizes both multi-sensory integration and frequency segregation as neural strategies to resolve the ambiguity of tilt and translation stimuli. Movement in an altered gravity environment, such as weightlessness without a stable gravity reference, results in new patterns of sensory cues. For example, the semicircular canals, vision and neck proprioception provide information about head tilt on orbit without the normal otolith head-tilt position that is omnipresent on Earth. Adaptive changes in how inertial cues from the otolith system are integrated with other sensory information lead to perceptual and postural disturbances upon return to Earth's gravity. The primary goals of this ground-based research investigation are to explore physiological mechanisms and operational implications of disorientation and tilt-translation disturbances reported by crewmembers during and following re-entry, and to evaluate a tactile prosthesis as a countermeasure for improving control of whole-body orientation during tilt and translation motion.

Wood, S. J.↗

Sensorimotor Adaptation Following Exposure to Ambiguous Inertial Motion Cues

The central nervous system must resolve the ambiguity of inertial motion sensory cues in order to derive accurate spatial orientation awareness. Our general hypothesis is that the central nervous system utilizes both multi-sensory integration and frequency segregation as neural strategies to resolve the ambiguity of tilt and translation stimuli. Movement in an altered gravity environment, such as weightlessness without a stable gravity reference, results in new patterns of sensory cues. For example, the semicircular canals, vision and neck proprioception provide information about head tilt on orbit without the normal otolith head-tilt position that is omnipresent on Earth. Adaptive changes in how inertial cues from the otolith system are integrated with other sensory information lead to perceptual and postural disturbances upon return to Earth s gravity. The primary goals of this ground-based research investigation are to explore physiological mechanisms and operational implications of disorientation and tilt-translation disturbances reported by crewmembers during and following re-entry, and to evaluate a tactile prosthesis as a countermeasure for improving control of whole-body orientation during tilt and translation motion.

Wood, S. J.↗

Human Perception of Ambiguous Inertial Motion Cues

Human daily activities on Earth involve motions that elicit both tilt and translation components of the head (i.e. gazing and locomotion). With otolith cues alone, tilt and translation can be ambiguous since both motions can potentially displace the otolithic membrane by the same magnitude and direction. Transitions between gravity environments (i.e. Earth, microgravity and lunar) have demonstrated to alter the functions of the vestibular system and exacerbate the ambiguity between tilt and translational motion cues. Symptoms of motion sickness and spatial disorientation can impair human performances during critical mission phases. Specifically, Space Shuttle landing records show that particular cases of tilt-translation illusions have impaired the performance of seasoned commanders. This sensorimotor condition is one of many operational risks that may have dire implications on future human space exploration missions. The neural strategy with which the human central nervous system distinguishes ambiguous inertial motion cues remains the subject of intense research. A prevailing theory in the neuroscience field proposes that the human brain is able to formulate a neural internal model of ambiguous motion cues such that tilt and translation components can be perceptually decomposed in order to elicit the appropriate bodily response. The present work uses this theory, known as the GIF resolution hypothesis, as the framework for experimental hypothesis. Specifically, two novel motion paradigms are employed to validate the neural capacity of ambiguous inertial motion decomposition in ground-based human subjects. The experimental setup involves the Tilt-Translation Sled at Neuroscience Laboratory of NASA JSC. This two degree-of-freedom motion system is able to tilt subjects in the pitch plane and translate the subject along the fore-aft axis. Perception data will be gathered through subject verbal reports. Preliminary analysis of perceptual data does not indicate that the GIF resolution hypothesis is completely valid for non-rotational periodic motions. Additionally, human perception of translation is impaired without visual or spatial reference. The performance of ground-base subjects in estimating tilt after brief training is comparable with that of crewmembers without training.

Zhang, Guan-Lu↗

Neurophysiology Summary

The terrestrial gravitational field serves as an important orientation reference for human perception and movement, being continually monitored by sensory receptors in the skin, muscles, joints, and vestibular otolith organs. Cues from these graviceptors are used by the brain to estimate spatial orientation and to control balance and movement. Changes in these cues associated with the tonic changes in gravity (gravito-inertial force),during the launch and entry phases of space flight missions result in altered perceptions, degraded motor control performance, and in some cases, "motion" sickness during, and for a period of time after, the g-transitions. In response to these transitions, however, physiological and behavioral response mechanisms are triggered to compensate for altered graviceptor cues and/or to adapt to the new sensory environment. Basic research in the neurophysiology discipline is focused on understanding the characteristic features of and the underlying mechanisms for the normal human response to tonic changes in the gravito-inertial force environment. These studies address fundamental questions regarding the role of graviceptors in orientation and movement in the terrestrial environment, as well as the capacity, specificity, and modes for neural plasticity in the sensory-motor and perceptual systems of the brain. At the 2001 workshop basic research studies were presented addressing: neuroanatomical responses to altered gravity environments, the neural mechanisms for resolving the ambiguity between tilting and translational stimuli in otolith organ sensory input, interactions between the vestibular system and the autonomic nervous system , the roles of haptic and visual cues in spatial orientation, mechanisms for training environment-appropriate sensorimotor responses triggered by environment-specific context cues, and studies of sensori-motor control of posture and locomotion in the terrestrial environment with and without recent exposure to space flight. Building on these basic research studies are more applied studies focused on the development of countermeasures to the untoward neurophysiological responses to space flight. At the 2001 workshop, applied research studies were presented addressing issues related to the use of rotational artificial gravity (centripetal acceleration) as a multisystem (bone, muscle, cardiovascular, and, perhaps, neurovestibular) countermeasure. Also presented was a clinical study reporting on a new rating system for clinical evaluation of postflight functional neurological status.

Paloski, William H.↗

Influence of Vibrotactile Feedback on Controlling Tilt Motion After Spaceflight

We hypothesize that adaptive changes in how inertial cues from the vestibular system are integrated with other sensory information leads to perceptual disturbances and impaired manual control following transitions between gravity environments. The primary goals of this ongoing post-flight investigation are to quantify decrements in manual control of tilt motion following short-duration spaceflight and to evaluate vibrotactile feedback of tilt as a sensorimotor countermeasure. METHODS. Data is currently being collected on 9 astronaut subjects during 3 preflight sessions and during the first 8 days after Shuttle landings. Variable radius centrifugation (216 deg/s, <20 cm radius) in a darkened room is utilized to elicit otolith reflexes in the lateral plane without concordant canal or visual cues. A Tilt-Translation Sled (TTS) is capable of synchronizing pitch tilt with fore-aft translation to align the resultant gravitoinertial vector with the longitudinal body axis, thereby eliciting canal reflexes without concordant otolith or visual cues. A simple 4 tactor system was implemented to provide feedback when tilt position exceeded predetermined levels in either device. Closed-loop nulling tasks are performed during random tilt steps or sum-of-sines (TTS only) with and without vibrotactile feedback of chair position. RESULTS. On landing day the manual control performance without vibrotactile feedback was reduced by >30% based on the gain or the amount of tilt disturbance successfully nulled. Manual control performance tended to return to baseline levels within 1-2 days following landing. Root-mean-square position error and tilt velocity were significantly reduced with vibrotactile feedback. CONCLUSIONS. These preliminary results are consistent with our hypothesis that adaptive changes in vestibular processing corresponds to reduced manual control performance following G-transitions. A simple vibrotactile prosthesis improves the ability to null out tilt motion within a limited range of motion disturbances.

Wood, S. J.↗

Straight Ahead in Microgravity

INTRODUCTION The subjective straight-ahead direction is a very basic perceptual reference for spatial orientation and locomotion. The perceived straight-ahead along the horizontal and vertical meridian is largely determined by both otolith and somatosensory inputs which are altered in microgravity. The Straight Ahead in Microgravity (SAM) experiment will be conducted on the International Space Station (ISS) to examine how this spatial processing changes as a function of spaceflight. METHODS Data will be collected before the flight, at one-month intervals during long-duration stay (180 days) on board ISS, and after return to Earth. Control studies will also be performed during parabolic flights. Three different protocols will be used in each test session: (1) Fixation: The subject will be asked to look at actual targets (normal vision) and then to imagine these same targets (occluded vision) in the straight-ahead direction. Targets will be located at near distance (arm s length, ~0.5m), medium distance (~1 m), and far distance (beyond 2 m). This task will be successively performed with subject s body aligned with the spacecraft interior, and with subject s body tilted forward and backward by an operator. (2) Saccades: The subject will be asked to make horizontal and vertical saccades, first relative to the spacecraft interior reference system, and then relative to the subject s head reference system. This task will be successively performed with subject s body aligned with the spacecraft interior, and with subject s body tilted in roll or in pitch by an operator. (3) Linear Vestibulo-Ocular Reflex (VOR): The subject will be asked to stare at actual visual targets (normal vision) at various distances (near, medium, far) in the straight-ahead direction. Vision will then be occluded, and the subject will be asked to continue staring at the same imagined targets while he/she is passively translated forward-backward, up-down, or side-to-side. The subject's body motion will be performed by the restrained operator while the subject is free-floating. EXPECTED RESULTS The coupling of downward gaze with vergence eye movements observed on Earth is expected to increase in microgravity. Saccadic eye movements made in darkness along perceived axes are expected to be more closely aligned with the body s longitudinal axis in 0g compared to 1g, as the reference system for spatial orientation moves from an allocentric (gravitational) to an egocentric (idiotropic) vector. Changes in the linear VOR will reflect adaptive changes in otolith-ocular reflex contributions to the perceived straight-ahead. DISCUSSION A change in an individual's egocentric reference might have negative consequences on evaluating the direction of an approaching object or on the accuracy of reaching movements or locomotion. Consequently, investigating how microgravity affects the egocenter is important for understanding the problems associated with long-term effects of microgravity on astronauts' and how they re-adapt to the return of gravitational forces on Earth or other planetary surfaces. This project therefore has theoretical, practical and even clinical implications for the sensorimotor research gap "What are the changes in sensorimotor function over the course of a mission?"

Clement, G.↗

Improving Early Adaptation Following Long Duration Spaceflight by Enhancing Vestibular Information

Crewmember adapted to the microgravity state may need to egress the vehicle within a few minutes for safety and operational reasons after g-transitions. The transition from one sensorimotor state to another consists of two main mechanisms: strategic and plastic-adaptive and have been demonstrated in astronauts returning after long duration space flight. Strategic modifications represent "early adaptation" -immediate and transitory changes in control that are employed to deal with short-term changes in the environment. If these modifications are prolonged then plastic-adaptive changes are evoked that modify central nervous system function, automating new behavioral responses. More importantly, this longer term adaptive recovery mechanism was significantly associated with their strategic ability to recover on the first day after return to Earth G. We are developing a method based on stochastic resonance (SR) to enhance information transfer by improving the brain's ability to detect vestibular signals especially when combined with balance training exercises for rapid improvement in functional skill, for standing and mobility. The countermeasure to improve post-flight balance and locomotor disturbances is a stimulus delivery system that is wearable/portable providing low imperceptible levels of white noise based binaural bipolar electrical stimulation of the vestibular system (stochastic vestibular stimulation, SVS). The techniques for improving signal detection using SVS may thus provide additional information to improve such strategic abilities and thus help in significantly reducing the number of days required to recover functional performance to preflight levels after long duration space flight. We have conducted a series of studies to document the efficacy of SVS stimulation on balance/locomotion tasks on unstable surfaces and motion tracking tasks during intra-vestibular system conflicts. In an initial study, we showed that SVS improved overall balance performance while standing on an unstable surface indicating that SVS may be sufficient to provide a comprehensive countermeasure approach for improving postural stability. In a second study, we showed that SVS improved locomotor performance on a treadmill mounted on an oscillating platform indicating that SVS may also be used to maximize locomotor performance during walking in unstable environments. In a third study, SVS was evaluated during an otolith-canal conflict scenario in a variable radius centrifuge at low frequency of oscillation (0.1 Hz) on both eye movements and perceptual responses (using a joystick) to track imposed oscillations. The variable radius centrifuge provides a selective tilting sensation that is detectable only by the otolith organs providing conflicting information from the canal organs of the vestibular system (intra-vestibular conflict). Results show that SVS significantly reduced the timing difference between both the eye movement responses as well as the perceptual tracking responses with respect to the imposed tilt sensations. These results indicate that SVS can improve performance in sensory conflict scenarios like that experienced during space flight. Such a SR countermeasure will act synergistically along with the pre-and in-flight adaptability training protocols providing an integrated, multi-disciplinary countermeasure capable of fulfilling multiple requirements making it a comprehensive and cost effective countermeasure approach to enhance sensorimotor capabilities following long-duration space flight.

Mulavara, Ajitkumar↗

Functional Imaging of Human Vestibular Cortex Activity Elicited by Skull Tap and Auditory Tone Burst

The aim of the current study was to characterize the brain activation in response to two modes of vestibular stimulation: skull tap and auditory tone burst. The auditory tone burst has been used in previous studies to elicit saccular Vestibular Evoked Myogenic Potentials (VEMP) (Colebatch & Halmagyi 1992; Colebatch et al. 1994). Some researchers have reported that airconducted skull tap elicits both saccular and utricle VEMPs, while being faster and less irritating for the subjects (Curthoys et al. 2009, Wackym et al., 2012). However, it is not clear whether the skull tap and auditory tone burst elicit the same pattern of cortical activity. Both forms of stimulation target the otolith response, which provides a measurement of vestibular function independent from semicircular canals. This is of high importance for studying the vestibular disorders related to otolith deficits. Previous imaging studies have documented activity in the anterior and posterior insula, superior temporal gyrus, inferior parietal lobule, pre and post central gyri, inferior frontal gyrus, and the anterior cingulate cortex in response to different modes of vestibular stimulation (Bottini et al., 1994; Dieterich et al., 2003; Emri et al., 2003; Schlindwein et al., 2008; Janzen et al., 2008). Here we hypothesized that the skull tap elicits the similar pattern of cortical activity as the auditory tone burst. Subjects put on a set of MR compatible skull tappers and headphones inside the 3T GE scanner, while lying in supine position, with eyes closed. All subjects received both forms of the stimulation, however, the order of stimulation with auditory tone burst and air-conducted skull tap was counterbalanced across subjects. Pneumatically powered skull tappers were placed bilaterally on the cheekbones. The vibration of the cheekbone was transmitted to the vestibular cortex, resulting in vestibular response (Halmagyi et al., 1995). Auditory tone bursts were also delivered for comparison. To validate our stimulation method, we measured the ocular VEMP outside of the scanner. This measurement showed that both skull tap and auditory tone burst elicited vestibular evoked activation, indicated by eye muscle response. Our preliminary analyses showed that the skull tap elicited activation in medial frontal gyrus, superior temporal gyrus, postcentral gyrus, transverse temporal gyrus, anterior cingulate, and putamen. The auditory tone bursts elicited activation in medial frontal gyrus, superior temporal gyrus, superior frontal gyrus, precentral gyrus, inferior and superior parietal lobules. In line with our hypothesis, skull taps elicited a pattern of cortical activity closely similar to one elicited by auditory tone bursts. Further analysis will determine the extent to which the skull taps can replace the auditory tone stimulation in clinical and basic science vestibular assessments.

Noohi, Fatemeh↗

Improving Sensorimotor Adaptation Following Long Duration Space Flight by Enhancing Vestibular Information Transfer

Crewmember adapted to the microgravity state may need to egress the vehicle within a few minutes for safety and operational reasons after gravitational transitions. The transition from one sensorimotor state to another consists of two main mechanisms: strategic and plastic-adaptive and have been demonstrated in astronauts returning after long duration space flight. Strategic modifications represent "early adaptation" - immediate and transitory changes in control that are employed to deal with short-term changes in the environment. If these modifications are prolonged then plastic-adaptive changes are evoked that modify central nervous system function, automating new behavioral responses. More importantly, this longer term adaptive recovery mechanism was significantly associated with their strategic ability to recover on the first day after return to Earth G. We are developing a method based on stochastic resonance to enhance information transfer by improving the brain's ability to detect vestibular signals (Vestibular Stochastic Resonance, VSR) especially when combined with balance training exercises such as sensorimotor adaptability (SA) training for rapid improvement in functional skill, for standing and mobility. This countermeasure to improve detection of vestibular signals is a stimulus delivery system that is wearable/portable providing low imperceptible levels of white noise based binaural bipolar electrical stimulation of the vestibular system (stochastic vestibular stimulation). To determine efficacy of vestibular stimulation on physiological and perceptual responses during otolith-canal conflicts and dynamic perturbations we have conducted a series of studies: We have shown that imperceptible binaural bipolar electrical stimulation of the vestibular system across the mastoids enhances balance performance in the mediolateral (ML) plane while standing on an unstable surface. We have followed up on the previous study showing VSR stimulation improved balance performance in both ML and anteroposterior planes while stimulating in the ML axis only. We have shown the efficacy of VSR stimulations on enhancing physiological and perceptual responses of whole-body orientation during low frequency perturbations (0.1 Hz) on the ocular motor system using a variable radius centrifuge on both physiological (using eye movements) and perceptual responses (using a joystick) to track imposed oscillations. The variable radius centrifuge provides a selective tilting sensation that is detectable only by the otolith organs providing conflicting information from the canal organs of the vestibular system (intra-vestibular conflict). These results indicate that VSR can improve performance in sensory conflict scenarios like that experienced during space flight. We have showed the efficacy of VSR stimulation to improve balance and locomotor control on subjects exposed to continuous, sinusoidal lateral motion of the support surface while walking on a treadmill while viewing perceptually matched linear optic flow. We have shown the safety of short term continuous use of up to 4 hours of VSR stimulation and its efficacy in improving balance and locomotor function in Parkinson's Disease patients. This technique for improving vestibular signal detection may thus provide additional information to improve strategic abilities. We hypothesize that VSR stimulation will act synergistically with SA training to improve adaptability by increased utilization of vestibular information and therefore serve to optimize and personalize the SA countermeasure prescription. This forms the basis of its usefulness both as a training modality and further help in significantly reducing the number of days required to recover functional performance to preflight levels after long duration space flight.

Mulavara, A. P.↗

Ocular Vestibular Evoked Myogenic Potentials Using Head Striker Stimulation

Introduction: Over the last two decades, several studies have been published on the impact of long-duration (i.e., 22 days or longer) spaceflight on the central nervous system (CNS). In consideration of the health and performance of crewmembers in flight and post-flight, we are conducting a controlled prospective longitudinal study to investigate the effects of spaceflight on the extent, longevity and neural bases of sensorimotor, cognitive, and neural changes. Multiple studies have demonstrated the effects of spaceflight on the vestibular system. One of the supporting tests conducted in this protocol is the Vestibular Evoked Myogenic Potential (VEMP) test that provides a unilateral measure of otolith (saccule and utricle) function. A different approach was taken for ocular VEMP (oVEMP) testing using a head striker system (Wackym et al. 2012). The oVEMP is generally considered to be a measure of utricle function. The the otolithic input to the inferior oblique muscle is predominately from the utricular macula. Thus, quantitatively, oVEMP tests utricular function. Another practical extension of these relationships is that the oVEMP reflects the superior vestibular nerve function. Methods: Ground testing was administered on 16 control subjects and for 8 subjects over four repeated sessions spanning 70 days. The oVEMP was elicitied via a hand held striker by a vibrotactile pulse presented at the rate of 1 Hz for 24 seconds on the side of the head as subjects lay supine on a gurney. Subjects were directed to gaze approximately 25 degrees above straight ahead in semi-darkness. For the oVEMP electromyograms will be recorded with active bipolar electrodes (Delsys Inc., Boston, MA) on the infra-orbital ridge 1 cm below the eyelid with a reference electrode on the below the knee cap. The EMG potentials were amplified; band-pass filtered using a BagnoliTM Desktop EMG System (Delsys Inc., Boston, MA, USA). This EMG signal is sampled at 10 kHz and the data stimulus onset to 100 MS was averaged over 24 trial repetitions for the vibrotactile VEMP. The typical oVEMP EMG response is an excitatory potential with first peak occurring at 11-12 ms and second peak at 18 ms. This requires a total recording time of approximately 29 seconds per trial which includes 5 seconds of no vibrotactile stimulation at the beginning of the protocol. The primary dependent measures consist of the latency and peak-to-peak amplitude from the EMG signals, which will be normalized to EMG levels at the beginning of the protocol. Data were collected for 3 repeated trials with striker stimulation on both the left and right side of the head Results: The oVEMP p1 range was observed at 3-14 ms and n1 at 7-19 ms. The striker system provided a consistent and rapid method for oVEMP testing. Discussion: Crew testing is in progress to determine changes in results between pre and post flight.

De Dios, Y. E.↗

Relationships Between Vestibular Measures as Potential Predictors for Spaceflight Sensorimotor Adaptation

Introduction: During space exploration missions astronauts are exposed to a series of novel sensorimotor environments, requiring sensorimotor adaptation. Until adaptation is complete, sensorimotor decrements occur, affecting critical tasks such as piloted landing or docking. Of particularly interest are locomotion tasks such as emergency vehicle egress or extra-vehicular activity. While nearly all astronauts eventually adapt sufficiently, it appears there are substantial individual differences in how quickly and effectively this adaptation occurs. These individual differences in capacity for sensorimotor adaptation are poorly understood. Broadly, we aim to identify measures that may serve as pre-flight predictors of and individual's adaptation capacity to spaceflight-induced sensorimotor changes. As a first step, since spaceflight is thought to involve a reinterpretation of graviceptor cues (e.g. otolith cues from the vestibular system) we investigate the relationships between various measures of vestibular function in humans. Methods: In a set of 15 ground-based control subjects, we quantified individual differences in vestibular function using three measures: 1) ocular vestibular evoked myogenic potential (oVEMP), 2) computerized dynamic posturography and 3) vestibular perceptual thresholds. oVEMP responses are elicited using a mechanical stimuli approach. Computerized dynamic posturography was used to quantify Sensory Organization Tests (SOTs), including SOT5M which involved performing pitching head movements while balancing on a sway-reference support surface with eyes closed. We implemented a vestibular perceptual threshold task using the tilt capabilities of the Tilt-Translation Sled (TTS) at JSC. On each trial, the subject was passively roll-tilted left ear down or right ear down in the dark and verbally provided a forced-choice response regarding which direction they felt tilted. The motion profile was a single-cycle sinusoid of angular acceleration with a duration of 5 seconds (frequency of 0.2 Hz), which was selected as it requires sensory integration of otolith and semicircular canal cues. Stimuli direction was randomized and magnitude was determined using an adaptive sampling procedure. One hundred trials were provided and each subject's responses were fit with a psychometric curve to estimate the subject's threshold. Results: Roll tilt perceptual thresholds at 0.2 Hz ranged from 0.5 degrees to 1.82 degrees across the 15 subjects (geometric mean of 1.04 degrees), consistent with previous studies. The inter-individual variability in thresholds may be able to help explain individual differences observed in sensorimotor adaptation to spaceflight. Analysis is ongoing for the oVEMPS and computerized dynamic posturography to identify relationships between the various vestibular measures. Discussion: Predicting individual differences in sensorimotor adaptation is critical both for the development of personalized countermeasures and mission planning. Here we aim to develop a basis of vestibular tests and parameters which may serve as predictors of individual differences in sensorimotor adaptability through studying the relationship between these measures.

Clark, T. K.↗

Functional Imaging of Human Vestibular Cortex Activity Elicited by Skull Tap and Auditory Tone Burst

The current study characterizes brain activation in response to two modes of vestibular stimulation: skull tap and auditory tone burst. The auditory tone burst has been used in previous studies to elicit either the vestibulo-spinal reflex (saccular-mediated colic Vestibular Evoked Myogenic Potentials (cVEMP)), or the ocular muscle response (utricle-mediated ocular VEMP (oVEMP)). Some researchers have reported that air-conducted skull tap elicits both saccular and utricle-mediated VEMPs, while being faster and less irritating for the subjects. However, it is not clear whether the skull tap and auditory tone burst elicit the same pattern of cortical activity. Both forms of stimulation target the otolith response, which provides a measurement of vestibular function independent from semicircular canals. This is of high importance for studying otolith-specific deficits, including gait and balance problems that astronauts experience upon returning to earth. Previous imaging studies have documented activity in the anterior and posterior insula, superior temporal gyrus, inferior parietal lobule, inferior frontal gyrus, and the anterior cingulate cortex in response to different modes of vestibular stimulation. Here we hypothesized that skull taps elicit similar patterns of cortical activity as the auditory tone bursts, and previous vestibular imaging studies. Subjects wore bilateral MR compatible skull tappers and headphones inside the 3T GE scanner, while lying in the supine position, with eyes closed. Subjects received both forms of the stimulation in a counterbalanced fashion. Pneumatically powered skull tappers were placed bilaterally on the cheekbones. The vibration of the cheekbone was transmitted to the vestibular system, resulting in the vestibular cortical response. Auditory tone bursts were also delivered for comparison. To validate our stimulation method, we measured the ocular VEMP outside of the scanner. This measurement showed that both skull tap and auditory tone burst elicited vestibular evoked myogenic potentials, indicated by eye muscle responses. We further assessed subjects' postural control and its correlation with vestibular cortical activity. Our results provide the first evidence of using skull taps to elicit vestibular activity inside the MRI scanner. By conducting conjunction analyses we showed that skull taps elicit the same activation pattern as auditory tone bursts (superior temporal gyrus), and both modes of stimulation activate previously identified vestibular cortical regions. Additionally, we found that skull taps elicit more robust vestibular activity compared to auditory tone bursts, with less reported aversive effects. This further supports that the skull tap could replace auditory tone burst stimulation in clinical interventions and basic science research. Moreover, we observed that greater vestibular activation is associated with better balance control. We showed that not only the quality of balance (indicated by the amount of body sway) but also the ability to maintain balance for a longer time (indicated by the balance time) was associated with individuals' vestibular cortical excitability. Our findings support an association between vestibular cortical activity and individual differences in balance. In sum, we found that the skull tap stimulation results in activation of canonical vestibular cortex, suggesting an equally valid, but more tolerable stimulation method compared to auditory tone bursts. This is of high importance in longitudinal vestibular assessments, in which minimizing aversive effects may contribute to higher protocol adherence.

Noohi, F.↗

Neuro-Vestibular Examination During and Following Spaceflight (Vestibular Health)

BACKGROUND Adaptation to microgravity during spaceflight causes neurological disturbances that are either directly or indirectly mediated by the vestibular system. These disturbances could include space motion sickness, spatial disorientation, and cognitive impairment, as well as changes in head-eye coordination, vestibulo-ocular reflexes, and control of posture and locomotion. Otolith-mediated reflex gains appear to adapt rapidly during spaceflight and after landing. However, animal studies have shown that structural modifications of the vestibular sensory apparatus develop during long-duration spaceflight. To date, no studies have characterized the severity of vestibular syndromes experienced by astronauts as a function of the duration of spaceflight or whether the effects are caused by changes at the peripheral end organs, midbrain, cerebellum, or vestibular cortex. OBJECTIVES We will investigate temporal vestibular changes in crewmembers of short, 6-month, and one-year missions to identify trends in adaptation of vestibular health and performance in orbit and after landing. We will also determine whether the vestibular organs and/or the central vestibular system undergo structural changes during long-duration exposure to microgravity, which could cause vestibular disorders when transitioning to a different gravitational environment. METHODS Recordings of eye, head, and body movements, as well as subjective reports of perception of motion, will be used to determine the presence of abnormal eye movements, dysmetria, motion sickness symptoms, and illusions of motion during head or body movements. This includes characterization of temporal trends in central compensation for vestibular (otolith) asymmetry. Pre-flight data will be collected 90 days before the flight. In-flight tests will be performed early in the mission and once every one or two months thereafter. Post-flight examinations will be performed on the following days after return (R) from the mission: R+0, R+4, R+9, and R+30. Ground-based control tests will be performed on healthy volunteers in the laboratory to estimate mean normative responses. CONTROL RESULTS Thirty-two healthy (non-astronaut) control subjects performed the same ground test procedures as planned for crewmembers. In addition to establishing a normative database, these data were used to calculate vestibular asymmetries from perceptual reports during unilateral centrifugation, oculomotor responses during visual-alignment tasks, vestibulo-ocular reflex gain during head-impulse tests, and body rotation during stepping tests. A significant correlation was observed between asymmetries of subjective visual vertical and verbal report during unilateral centrifugation. Another significant correlation was observed between the asymmetries of ocular alignment, vestibulo-ocular reflex gain, and body rotation. These findings in a healthy cohort may help us better understand changes in vestibular asymmetries in crewmembers during and following spaceflight. RELEVANCE If the observed symptoms in crewmembers are more deleterious after the year-long missions than those documented after 6-month missions, then relevant countermeasures will be required to maintain the health and operational performance of astronauts during longer missions. Depending on the etiology of the vestibular syndrome revealed by these tests, countermeasures will be proposed based on vestibular rehabilitation therapies currently used in patients with vestibular disorders, such as habituation, gaze stabilization, and/or balance training exercises. ACKNOWLEDGEMENT This work is supported by the NASA’s Human Research Program Human Health Countermeasures Element.

T R Macaulay↗

Neuro-Vestibular Examination During and Following Spaceflight (Vestibular Health)

BACKGROUND Adaptation to microgravity during spaceflight causes neurological disturbances that are either directly or indirectly mediated by the vestibular system. These disturbances can include space motion sickness, spatial disorientation, and cognitive impairment, as well as changes in head-eye coordination, vestibulo-ocular reflexes, and control of posture and locomotion. Otolith-mediated reflex gains appear to adapt rapidly during spaceflight and after landing. However, animal studies have shown that structural modifications of the vestibular sensory apparatus develop during long-duration spaceflight. To date, no studies have characterized the severity of vestibular syndromes experienced by astronauts as a function of the duration of spaceflight or whether the effects are caused by changes at the peripheral end organs, midbrain, cerebellum, or vestibular cortex. OBJECTIVES We will investigate temporal vestibular changes in crewmembers of short, 6-month, and one-year missions to identify trends in adaptation of vestibular health and performance in orbit and after landing. We will also determine whether the vestibular organs and/or the central vestibular system undergo structural changes during long-duration exposure to microgravity, which could cause vestibular disorders when transitioning to a different gravitational environment. METHODS Recordings of eye, head, and body movements, as well as subjective reports of perception of motion, will be used to determine the presence of abnormal eye movements, dysmetria, motion sickness symptoms, and illusions of motion during head or body movements. This includes characterization of temporal trends in central compensation for vestibular (otolith) asymmetry. Pre-flight data will be collected 90 days before launch. In-flight examinations will be performed early in the mission (Flight Days 1 and 30) and once every two or three months thereafter. Post-flight examinations will be performed on the following days after return (R) from the mission: R+0, R+4, R+9, and R+30. Ground-based control tests have been performed on healthy volunteers in the laboratory to estimate mean normative responses. RESULTS Data collection for this study is ongoing. Data processing techniques are being refined. Our eye tracking method for measuring three-dimensional eye movement takes advantage of modern computer vision software (OpenCV) and advances in the field of iris recognition to improve measurement of ocular-counterolling. RELEVANCE If the observed symptoms in crewmembers are more deleterious after the year-long missions than those documented after 6-month missions, then relevant countermeasures will be required to maintain the health and operational performance of astronauts during longer missions. Depending on the etiology of the vestibular syndrome revealed by these tests, countermeasures will be proposed based on vestibular rehabilitation therapies currently used in patients with vestibular disorders, such as habituation, gaze stabilization, and/or balance training exercises.

T R Macaulay↗

Neuro-Vestibular Examination During and Following Spaceflight (Vestibular Health)

BACKGROUND Adaptation to microgravity during spaceflight causes neurological disturbances that are either directly or indirectly mediated by the vestibular system. These disturbances can include space motion sickness, spatial disorientation, and cognitive impairment, as well as changes in head-eye coordination, vestibulo-ocular reflexes, and control of posture and locomotion. Otolith-mediated reflex gains appear to adapt rapidly during spaceflight and after landing. However, animal studies have shown that structural modifications of the vestibular sensory apparatus develop during long-duration spaceflight. To date, no studies have characterized the severity of vestibular syndromes experienced by astronauts as a function of the duration of spaceflight or whether the effects are caused by changes at the peripheral end organs, midbrain, cerebellum, or vestibular cortex. OBJECTIVES We are investigating temporal vestibular changes in crewmembers of short, 6-month, and one-year missions to identify trends in adaptation of vestibular health and performance in orbit and after landing. We are also differentiating between peripheral and central vestibular forms of vertigo and oculomotor disorders. METHODS Recordings of eye, head, and body movements, as well as subjective reports of perception of motion, are being used to determine the presence of abnormal eye movements, dysmetria, motion sickness symptoms, and illusions of motion during head or body movements. This includes characterization of temporal trends in central compensation for vestibular (otolith) asymmetry. In-flight examinations are being performed early in the mission (Flight Days 1 and 30) and once every 2-3 months thereafter. Postflight examinations are performed after return (R) from the mission on R+0, R+4, R+9, and R+30. The inflight and postflight motion sickness questionnaires are customized to support data sharing across related studies. Ground-based control testing has been performed on healthy volunteers(18 females, 14 males;38.6 ± 9.2 years) in the laboratory to estimate mean normative responses, and on patients with bilateral vestibulopathy (BVP) (17 females, 13 males; 60.6 ± 13.0 years) at the University of Caen. RESULTS As of September 2024, two crewmembers have completed all preflight, inflight, and postflight testing. Additional crewmembers are currently enrolled and data collection is currently ongoing. For ground testing, BVP patients performed similarly to previous postflight astronauts on R+0 in various walking performance tasks. Three additional body movement perception tasks have been tested. For the Triangle Completion Task, BVP patients had a larger mean angle of deviation and longer mean distance than healthy controls. For the Self-Rotation Task and Distance Perception Task, BVP patients had larger errors than healthy controls. These data suggest that vestibular deficiencies impact all aspects of body movement perception tested; whereas previous studies suggest that vestibular deficiencies are only associated with directional errors, not with overall trajectories/path lengths. These data will be compared to those of crewmembers during early postflight readaptation. RELEVANCE If the observed symptoms in crewmembers are more deleterious after the year-long missions than those documented after 6-month missions, then relevant countermeasures will be required to maintain the health and operational performance of astronauts during longer missions. Depending on the etiology of the vestibular syndrome revealed by these tests, countermeasures will be proposed based on vestibular rehabilitation therapies currently used in patients with vestibular disorders, such as habituation, gaze stabilization, and/or balance training exercises. ACKNOWLEDGEMENT This work is supported by NASA’s Human Research Program Human Health Countermeasures Element.

T R Macaulay↗