Dora Angelaki and William H. Paloski, Co-Chairs
Platform Presentations – Salons A, B, C, January 18
File# Title Authors
308 Neurophysiology D. Angelaki and W. H. Paloski
180 Synaptic Ribbon Plasticity in Utricular and Saccular
Maculae: New Clues to Functions?
M. D. Ross and J. Varelas
181 Orthostatic Intolerance and Autonomic Cardiovascular
Changes After Parabolic Flight
T. T. Schlegel, T. E. Brown, S. J. Wood,
E. W. Benavides, R. L. Bondar, F. Stein,
P. Moradshahi, D. L. Harm, J. V. Meck, P.
182 Vestibular Control of Sympathetic Activity H. Kaufmann, I. Biaggioni, A.
Voustianiouk, A. Diedrich, F. Costa, M.
Gizzi, S. Moore, T. Raphan, B. Cohen
183 The Role of Gravitoinertial Force Background, Spatial
Orientation and Contact Cues in Perturbations of
Reaching Movements by Coriolis Forces
P. DiZio and J. R. Lackner
184 Self-Motion System Frequency Response: Implications
D. E. Parker, H. H. L. Duh, J. O. Phillips,
T. A. Furness
185 STS-90 Neurolab Experiments on the Role of Visual Cues
in Microgravity Spatial Orientation
C. M. Oman, I. P. Howard, T. Smith, A.
C. Beall, A. Natapoff, J. E. Zacher, H. L.
186 Visual Orientation in Unfamiliar Gravito-Inertial
C. M. Oman, I. P. Howard, W. L.
Shebilske, J. S. Taube
187 Visually-Induced Adaptation of the Translational
M. Wei, H.-H. Zhou, D. E. Angelaki
188 Otolith and Vertical Canal Contributions to Dynamic
G. D. Kaufman, F. O. Black, C. C.
Gianna, W. H. Paloski, S. J. Wood
189 Characterization of Sensory Integration and Control
Strategies That Regulate Human Postural Control in
R. J. Peterka
190 Spatial Reorientation and Sensory-Motor Balance Control
in Altered Gravity
W. H. Paloski, S. J. Wood, G. D.
Kaufman, F. O. Black, M. F. Reschke
191 Perception of Tilt (Somatogravic Illusion) in Response to
Sustained Linear Acceleration During Space Flight
B. Cohen, G. Clement, S. T. Moore, T.
192 Context-Specific Adaptation of Gravity-Dependent
Vestibular Reflex Responses (NSBRI Neurovestibular
M.Shelhamer, J. Goldberg, L. B. Minor,
W. H. Paloski, L. R. Young, D. S. Zee
193 Locomotion After Long-Duration Spaceflight: Adaptive
Modulation of a Full-Body Head and Gaze Stabilization
J. J. Bloomberg, A. P. Mulavara, C.
miller, P. V. McDonald, C. S. Layne, J.
Houser, H. Cohen, I. B. Kozlovskaya
194 Recovery Trajectories to Perturbations During
C. Wall and L. Oddsson
195 Maintaining Neuromuscular Contraction Using
Somatosensory Input During Long Duration Spaceflight
C. S. Layne, A. P. Mulavara, P. V.
McDonald, C. J. Pruett, J. J. Bloomberg
196 Effect of Microgravity on Afferent Innervation C. D. Fermin, R. F. Garry, Y-P. Chen, D.
197 The Effect of Spaceflight on the Ultrastructure of Adult
Rat Cerebellar Cortex
G. R. Holstein and G. P. Martinelli
198P Developing Future Countermeasures for the Detrimental
Effects of Space Flight: Role of Otolith Systems and
Resolution of Tilt/Translation
F. O. Black, S. J. Wood, C. C. Gianna,
W. H. Paloski
199P Use of the Neurologic Function Rating Scale Following
Space Shuttle Flights
J. B. Clark and J. U. Meir
200P Varied Practice and Response Generalization as the
Basis for Sensorimotor Countermeasures
H. S. Cohen, J. J. Bloomberg, C. Roller,
201P Somatosensory Suppression of Re-Entry Disturbances P. DiZio and J. R. Lackner
202P Neurovestibular Aspects of Artificial Gravity H. Hecht and L. R. Young
203P Responses of Eye Movement Related Vestibular Neurons
to Linear Acceleration
W. M. King, W. Zhou, B. Tang
204P Influence of Sensory Integration on the Neural
Processing of Gravito-Inertial Cues
205P Inflight Centrifugation as a Countermeasure for
Deconditioning of Otolith-Based Reflexes
S. T. Moore, G. Clement, A. Diedrich, I.
Biaggioni, H. Kaufmann, T. Raphan, B.
206P The Influence of Visual Rotational Cues on Human
Orientation and Eye Movements
L. Zupan, D. M. Merfeld, K. King
Dora E. Angelaki, Ph.D.
William H. Paloski, Ph.D.
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
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 multi-
system (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.
The neurophysiology group met first on Wednesday evening in a two hour session moderated by Chuck Oman, Jon
Clark, Tom Marshburn, and Jason Richards. The focus of this session was a discussion of the experiences of US
astronauts participating in the Phase 1 (Mir Station) long-duration flight program. A draft manuscript on the subject
authored by the moderators was distributed to all participants, and some novel video footage from the Mir station as
well as the ISS was presented. The main platform session, which is summarized in the next section, lasted throughout
most of the day on Thursday. The session was very busy, with little time for questions following each presentation,
and insufficient scheduled break time. Nevertheless, the session was well attended and achieved its primary goal of
presenting the scope and depth of the entire NASA-NSBRI neurophysiology research program to all of its
SUMMARY OF PRESENTATIONS
Ross, MD and J Varelas. Synaptic Ribbon Plasticity in Utricular and Saccular Maculae: New Clues to Functions?
Ross and Varelas presented cellular evidence of vestibular plasticity during space flight. They reported that utricular
and saccular maculae differ completely in their responses to weightlessness. Their results confirmed previous
findings of increased numbers of synapses in Type II hair cells of the utricular maculae, with Type I cells showing
lesser increases. In the saccular maculae, however, they found that synapses in Type II cells remain relatively stable
throughout flight and postflight, while Type I cells fluctuate.
From Washington University School of Medicine, Department of Anatomy and Neurobiology, St. Louis, MO (D.
Angelaki) and NASA Johnson Space Center, Life Sciences Laboratories, Houston, TX (W. Paloski).
Holstein, GR and GP Martinelli. The Effect of Spaceflight on the Ultrastructure of Adult Rat Cerebellar Cortex.
Holstein and Martinelli also presented cellular evidence of vestibular plasticity during space flight. They reported
that changes observed in the ultrastructure of Purkinje cells from the adult rat cerebellar cortex harvested 24 hrs after
shuttle launch suggest that space flight induces excitotoxic responses in Purkinje cells.
King, WM, W Zhou, and B Tang. Responses of Eye Movement Related Vestibular Neurons to Linear Acceleration
King et al. reported that specific classes of neurons were identified in the brainstem of awake behaving monkeys that
selectively process and transform otolith sensory inflow into an occulomotor command for gaze stabilization during
translation. These central vestibular neurons, characterized by their discharge pattern and anatomical connections,
transmit otolith signals that are modulated by gaze. They point out that unlike semicircular canal reflexes, eye
movements produced by otolith-ocular reflexes depend on gaze direction and are inherently disjunctive.
Fermin, CD, RF Garry, YP Chen, and D Zimmer. Effect of Microgravity on Afferent Innervation.
Fermin et al. reported that some members of S100 Calcium Binding Proteins (CBP) family are expressed in
vestibular afferents of chicken at 1g, and that the mRNA of certain mammalian CBP S100 isoforms share
distribution characteristics with chicken isoforms. They further reported that the expression pattern changes
following mechanical injury of vestibular afferents and suggested that gene expression and protein distribution of
S100 CBP may be affected by altered gravity.
Otolith Ambiguity Studies
Zupan, L, DM Merfeld, and K King. The Influence of Visual Rotational Cues on Human Orientation and Eye
Zupan et al. investigated how the central nervous system separates the otolithic measurement of gravito-inertial force
into estimates of gravity and linear acceleration. They measured eye movements and subjective roll in human
subjects during and after roll optokinetic stimulation about the subject's naso-occipital axis. They reported that, in
addition to a torsional optokinetic after-nystagmus observed for all orientations, a horizontal after-nystagmus was
observed to the right following clockwise stimulation and to the left following counterclockwise stimulation. They
suggest that these observations are in agreement with the GIF resolution hypothesis that suggests that subjective tilt
illusion will induce a non-zero estimate of interaural linear acceleration, and therefore a horizontal translational VOR
even in the absence of "true" linear acceleration.
Wei, M, HH Zhou, and DE Angelaki. Visually-Induced Adaptation of the Translational Vestibulo-Ocular Reflex.
Wei et al. reported on an experiment addressing the issue of visually-induced learning in the resolution of gravito-
inertial forces. Preliminary results during cross-axis adaptation of the translational vestibulo-ocular reflex in primates
suggest that learning effects in the resolution of gravito-inertial forces are limited and probably more complex than
Merfeld, D. Influence of Sensory Integration on the Neural Processing of Gravito-Inertial Cues (poster).
Merfeld reported on plans for a future flight project (currently in definition phase) to investigate how certain neural
processes of sensory integration adapt when astronauts experience weightlessness. The specific processes to be
studied are those underlying the use of rotational cues to interpret ambiguous gravito-inertial cues via internal
Schlegel, TT, TE Brown, SJ Wood, EW Benavides, RL Bondar, F Stein, P Moradshahi, DL Harm, JM Fritsch-Yelle,
and PA Low. Orthostatic Intolerance and Autonomic Cardiovascular Changes after Parabolic Flight.
Schlegel et al. reported that syndromes of orthostatic intolerance resembling those occurring after space flight were
induced by a brief (2 hr.) parabolic flight. The mechanisms differed between vomiters and non-vomiters, and
vomiting was associated with increases in R-R interval variability and carotid-cardiac baroreflex responsiveness,
suggesting that the emetic reflex transiently increases resting fluctuations in efferent vagal-cardiac nerve traffic.
Moore, ST, G Clément, A Diedrich, I Biaggioni, H Kaufman, T Raphan, and B Cohen. Inflight Centrifugation as a
Countermeasure for Deconditioning of Otolith-Based Reflexes (poster).
Moore et al. reported on plans for a future flight study to confirm results from the Neurolab mission suggesting that
in-flight centripetal accelerations may protect subjects from postflight orthostatic intolerance.
Kaufmann, HC, I Biaggioni, B Cohen, A Diedrich, M Gizzi, R Clark, F Costa, and D Saadia. Vestibular Influences
on Autonomic Cardiovascular Control.
Kaufman et al. reported that forward acceleration in the naso-occipital axis (as sensed by the otoliths) increases
sympathetic efferent activity in the peroneal nerve.
Spatial Orientation Studies
Cohen, B, G Clément, ST Moore, and T Raphan. Perception of Tilt (Somatogravic Illusion) in Response to Sustained
Linear Acceleration During Space Flight.
Cohen et al. reported results from the Neurolab mission suggesting that the somatogravic illusion induced by
centrifugation is maintained in space. They found that the illusion of tilt increased as flight continued and depended
on the magnitude of linear acceleration, suggesting that astronauts continue to assign the gravito-inertial acceleration
as the spatial upright after adaptation to altered gravity.
Parker, DE, HBL Duh, JO Phillips, and TA Furness. Self-Motion System Frequency Response: Implications for
Parker et al. examined the frequency response of the visual self-motion system and found a motion frequency where
the summed response of the visual and inertial self-motion systems was maximized. Their data support the
hypothesis that conflicting visual and inertial motion cues at this "cross-over" frequency would be more likely to
elicit sickness than conflicting cues at a higher frequency.
Oman, CM, IP Howard, T Smith, AC Beall, A Natapoff, JE Zacher, and HL Jenkin. STS-90 Neurolab Experiments
on the Role of Visual Cues in Microgravity Spatial Orientation
Oman et al. reported using a Virtual Environment to record the subjective vertical in 4 astronauts during flight. They
found that astronauts became more dependent on dynamic visual cues, and some also on static visual cues. He also
reported that the subjective vertical is labile and can influence figure recognition and shading interpretation.
Oman, CM, IP Howard, WL Shebilske, and JS Taube. Visual Orientation in Unfamiliar Gravito-Inertial
Oman et al. also described results of a collaborative NSBRI research project on human visual orientation cues in
humans and animals. They reported that performance of humans in 3D spatial memory experiments correlates with
ability to mentally rotate 2D and 3D objects, and improves with training. They also reported that parabolic flight
studies of rat head direction cells show that cells continue to respond in 0-G, and occasionally show changes in
preferred direction that correspond to visual reorientation illusion onset in humans.
DiZio, P and JR Lackner. The Role of Gravitoinertial Force Background, Spatial Orientation and Contact Cues in
Perturbations of Reaching Movements by Coriolis Forces.
DiZio and Lackner reported that rapid adaptation to rotating artificial gravity environments is possible. They also
reported that the motor effects of the rate of adaptation to Coriolis force perturbations are equivalent in 2g, 1g, and
0g force backgrounds, but disorientation and motion sickness elicited by head movements during body rotation are
less severe in low force backgrounds. Finally they reported that non-supportive contact with the environment during
voluntary movement is a critical orientation cue driving adaptation.
DiZio, P and JR Lackner. Somatosensory Suppression of Re-Entry Disturbances (poster).
DiZio and Lackner also reported on plans for a future flight study to assess the role of non-supportive contact with
the environment (haptic inputs) during voluntary movement in spatial orientation and adaptation to altered gravito-
Context-Specific Adaptation Studies
Shelhamer, M, J Goldberg, LB Minor, WH Paloski, LR Young, and DS Zee. Context-Specific Adaptation of Gravity-
Dependent Vestibular Reflex Responses (NSBRI Neurovestibular Project 1).
Shelhamer et al. reported that during parabolic flight the magnitude of gravito-inertial force can be used as a context
cue for switching between adapted saccade states. They found evidence for retention of this adaptation after 8
months. They also reported that the gain of the translational LVOR can be made context-specific, using head tilt as a
context cue and that saccadic eye movements can be adapted in a context-specific manner, using a number of
different context cues. For interaural translations, they found head roll to be a more effective context cue than head
pitch. Finally, they reported that sensorimotor adaptation to head movements during short-radius centrifugation (23
rpm, 1 g at the feet) can be induced and retained for at least a week.
Cohen, HS, JJ Bloomberg, C Roller, and AP Mulavara. Varied Practice and Response Generalization as the Basis
for Sensorimotor Countermeasures (poster).
Cohen et al. presented preliminary data demonstrating that variable context adaptation may result in more rapid
adaptive responses to novel environments through response generalization. They also described a future ISS study
being planned to develop sensorimotor training regimens that promote adaptive generalization of locomotor function
as a means of facilitating the adaptive transition between gravitational environments.
Paloski, WH, SJ Wood, GD Kaufman, FO Black, and MF Reschke. Spatial Reorientation and Sensory-Motor
Balance Control in Altered Gravity.
Paloski et al. described a future flight study that will examine the fragility of the postural readaptation response by
challenging crewmembers during postflight recovery with unusual z-axis acceleration created using a short radius
Posture and Locomotion Studies
Peterka, RJ. Characterization of Sensory Integration and Control Strategies that Regulate Human Postural Control
in Changing Conditions.
Peterka reported that the human balance control system relies predominantly on proprioceptive cues during quiet
stance, but becomes increasingly reliant on graviceptor (vestibular) cues when balance is perturbed. He also showed
that loss of vestibular function profoundly alters and limits a subject’s ability to utilize his/her remaining visual and
proprioceptive cues, suggesting that reinterpretation of vestibular cues following space flight might be expected to
produce similar deficits.
Bloomberg, JJ, AP Mulavara, C Miller, PV McDonald, CS Layne, J Houser, H Cohen, and IB Kozlovskaya.
Locomotion After Long-Duration Space Flight: Adaptive Modulation of a Full-Body Head and Gaze Stabilization
Bloomberg et al. reported that after space flight, astronauts show reductions in dynamic visual acuity during
locomotion. These data, along with supporting ground-based studies, reveal the existence of a full-body, gaze
stabilization system that exploits the multiple degrees of freedom available during locomotion to help maintain clear
vision during body movement.
Layne, CS, AP Mulavara, PV McDonald, CJ Pruett, and JJ Bloomberg. Maintaining Neuromuscular Contraction
Using Somatosensory Input During Long Duration Spaceflight.
Layne et al. reported that application of pressure to the feet of free-floating astronauts enhanced the stereotypical
lower limb neuromuscular activation associated with rapid arm movements. This suggests that the plantar sensory
inputs can be used to enhance motor unit activation and may therefore be used as a countermeasure to inflight muscle
Wall, C and L Oddsson. Recovery Trajectories to Perturbations During Locomotion.
Wall and Oddsson described a novel method to study perturbations of gait during steady locomotion by giving small
(5–10 cm) disturbances to one foot during the support phase while recording the response with optical trackers.
Preliminary results demonstrated a vestibular dependence by showing that normal subjects recover from the
perturbations in 3–4 steps, while a pilot Labyrinthine Deficient subject required a much longer recovery time.
Artificial Gravity Precursor Studies
Kaufman, GD, FO Black, CC Gianna, WH Paloski, and SJ Wood. Otolith and Vertical Canal Contributions to
Dynamic Postural Control.
Kaufman et al. reported that 90-minute hypergravity (1.4g) stimulus (roll plane centripetal acceleration) induces
postural and subjective vertical changes in normal and some vestibular deficient subjects.
Black, FO, SJ Wood, CC Gianna, and WH Paloski. Developing Future Countermeasures for the Detrimental Effects
of Space Flight: Role of Otolith Systems & Resolution of Tilt/Translation (poster).
Black et al. described a new study that will establish the extent to which otolith-mediated tilt and translation
responses can be adapted at different stimulus frequencies, and then examine whether subjects can 'dual adapt' to
altered sensory environments using the orientation of gravity to provide context.
Hecht, H and LR Young. Neurovestibular Aspects of Artifical Gravity (poster).
Hecht and Young described a new multicenter study investigating whether head and body movements during high
rate artificial gravity are tolerable and how such artificial gravity can be implemented most efficiently. The study will
also investigate methods to minimize the undesirable side-effects of neurovestibular adaptation associated with
intermittent artificial gravity.
Clark, JB and JU Meir. Use of Neurologic Function Rating Scale Following Space Shuttle Flights (poster).
Clark and Meir reported that a Neurological Function Rating Scale has been designed for clinical assessment of
neurological dysfunction associated with space flight. Over 100 crewmembers have now been rated on landing day,
and the most severe deficits observed were in gait station and occulomotor disturbances.
IMPLICATIONS FOR FUTURE RESEARCH
The critical path research plan defines the following five risks (in order of importance) for neuro-vestibular
1. Disorientation and inability to perform landing, egress, or other physical tasks, especially during/after g-level
2. Impaired neuromuscular coordination and/or strength.
3. Impaired cognitive and/or physical performance due to motion sickness symptoms or treatments, especially
during/after g-level changes
4. Vestibular contribution to cardioregulatory dysfunction.
5. Possible chronic impairment of orientation or balance function due to microgravity or radiation.
The current NASA-NSBRI research program addresses each of these risks to some degree, and of the 24 critical
questions posed beneath these risks, the current program addresses 21. Thus, the current program appears to have
The neuroanatomical results from the peripheral vestibular and cerebellar regions presented at the workshop are
extremely important, providing limited anatomical evidence for the long-noted behavioral adaptive responses.
Further work should be supported both in tracking the anatomical changes that occur as a function of space flight and
in correlating the observed anatomical changes to concomitant behavioral changes.
The vestibulo-autonomic studies presented at the workshop just scratch the surface of the field. Nevertheless, they
demonstrate that the vestibular system may exert important influences on both the cardioregulatory system and the
motor control system. Further work should be supported in both areas, preferably by cross-disciplinary teams.
The context-specific adaptation studies and related artificial gravity precursor studies are providing important
background evidence, in humans, supporting the development of intermittent, rotational artificial gravity as a multi-
system countermeasure. NASA-NSBRI should begin funding multi-disciplinary groups to develop and test specific
artificial gravity protocols in ground-based studies, and, concomitantly, should begin developing the hardware and
infrastructure required for flight testing of an artificial gravity countermeasure.
SYNAPTIC RIBBON PLASTICITY IN UTRICULAR AND SACCULAR MACULAE:
NEW CLUES TO FUNCTIONS?
*Muriel D. Ross and **Joseph Varelas, *The University of New Mexico Health Sciences Center, Albuquerque,
N.M. ** Lockheed-Martin and NASA Ames Center for Bioinformatics, Moffett Field, CA
Research into the effects of weightlessness on rat vestibular maculae has consistently shown that ribbon synapses in
hair cells of the utricular maculae exhibit statistically significant changes in number, kind, and distribution when rats
are exposed to space flight (Ross, 1993, 1994, 2000). Synaptic plasticity was most evident when all type II hair cells
of these maculae were considered and was confined to type II cells in just the complete hair cells. Analysis of the
co-variance of the multiple variables (number, rod or sphere, pairs and groups) by the MANOVA feature of
software demonstrated further that day and weightlessness both had statistically significant effects
on type II hair cells (Ross, 2000). These results were obtained from the posterior portion of the utricular macula and
did not include the striola. For Neurolab, the striola and parastriolar area internal to the striola (pars interna) were
studied. The Neurolab striolar data in general support the findings in hair cells of the utricular maculae, but effects in
the saccular maculae differed. In saccular maculae, ribbon synapses in type I cells fluctuated while synapses in type
II hair cells remained relatively stable throughout the flight and up to postflight day 2. Only differences between
flight days 2 and 14 in ribbon synapses of type I hair cells were statistically significant. It cannot be argued that the
lack of significant differences in type II hair cells was due to inner ears utilized since utricular and saccular samples
were matched for the same rats in two cases.
The results in the saccular maculae raise the interesting question whether the anatomical findings signify very
different functions for the two maculae, even though both are subject to stimulation by gravitoinertial forces. This
report provides the data for the utricular and saccular maculae of the Neurolab experiment and compares the
findings with those previously obtained on SLS-1 and SLS-2. It also discusses the findings in light of previous
physiological data that indicated different functions for the two maculae (Fernandez et al., 1976a,b).
CURRENT STATUS OF RESEARCH
The Fisher strain of rats was used for this experiment. Rats were euthanized by decapitation on the ground on day
two of flight (Basal), in flight on flight days 2 (FD2) and 14 (FD14), and postflight on days 2 (PF2) and 14 (PF14).
Labyrinths were quickly removed from dissected temporal bones, fixed by immersion, and prepared for electron
microscopy as described previously (Ross, 2000). Unfortunately, only one of the four FD2 utricular maculae made
available to us proved useful for electron microscopic study. Study of the utricular maculae was limited, therefore,
to one Basal, one FD2 and one FD 14 sample. Attention then turned to the saccular macula. Study of the saccular
maculae is incomplete at this time. Two maculae from Basal, FD2, FD14 and PF2 will be analyzed. This Abstract is
based on two samples from FD2 and FD14 and one from a Basal and another from a PF2 rat which have been
studied thus far in 50 serial sections cut at 150 nm. The striolar area is identified in the rat by the presence of
myelination to the calyx in some afferents. In the case of a FD2 utricular and a FD2 saccular sample, an additional
set of 50 sections that crossed from the striola into pars interna was studied, to learn whether differences in synaptic
counts and other properties would be evident. Analysis of statistical significance was accomplished using the
ANOVA features of SuperANOVATM
software. All procedures used in this experiment were reviewed by the
Animal Use Committee established at NASA Ames Research Center and are in compliance with the Guide for the
Use of Laboratory Animals and the Animal Welfare Act.
Utricular macula: Mean values for number of ribbon synapses in type I cells of the utricular striolar area were as
follows: Basal; 2.034; FD2, 3.512; and FD 14, 2.400. The increment in synaptic mean value in ribbon synapses from
the Basal to FD2 was significant (p< 0.0044) as were differences in values for sphere-like ribbons (p< 0.0002). FD2
mean values for total synapses (p< 0.0408) and spheres (p< 0.0379) differed from FD14 values. For the parastriolar
area, pars interna, the mean value of synaptic ribbons was 3.543, differing significantly from the basal (p< 0.0013)
as did also sphere-like ribbons (p< 0.0014). Set two of FD2 also differed significantly from FD14 in total synapses
(p< 0.0209). and groups (p< 0.0447).
For type II hair cells, the Basal mean value for ribbon synapses at the striola was 4.744. For FD2, the mean value
was 9.000 and for FD14 it was 6.884. The differences between synaptic means between the Basal and FD2 were
significant for total synapses (p< 0.0001), spheres (p< 0.0034), rods (p< 0.0016) and pairs (p< 0.0003). FD14
differed from the Basal in total synapses (p< 0.0306), spheres (p< 0.0093), and pairs (p< 0.0074). For set two FD2,
the mean value of total synapses was 7.929. This value differed from the Basal (p< 0.0023) as did sphere-like
ribbons (p< 0.0008) and pairs (p< 0.0012). The two series from FD2 were essentially similar.
Saccular macula: In type I cells of the saccular macula, mean values were: Basal, 3.545; FD2, 2.646; FD14, 3.788;
PF2, 3.250. FD2 differed significantly from FD14 in total synapses (p< 0.0277) and in spheres (p< 0.0074). In type
II cells, the mean values of synaptic number were as follows: Basal: 6.939; FD2, 6.317; FD14, 6.382, PF2, 6.480.
None of these or other mean values (pairs, etc.) differed significantly.
Findings in the striolar area of the utricle were essentially similar to those obtained from the posterior part of the
macula on SLS-1 and SLS-2. That is, synapses increased in the hair cells, but changes were greater overall in the
case of type II cells. Nevertheless, the results in the striolar area of both the utricle and the saccule differ from those
obtained previously; i.e., in type II hair cells, synapses had doubled to 11.4±7.2 on day 13 of a 14 day flight (Ross,
2000). This is not surprising since the striola differs morphologically from other portions of the macula in
organization of hair cells, afferents and processes. In the saccular samples of this experiment, in contrast to the
utricular, ribbon synapses in type I cells had declined by FD2 but fluctuated on FD14 and PF2. In type II hair cells, a
slight decline in synaptic mean occurred by FD2 and was maintained through PF2. None of the changes in type II
cells was statistically significant. The fact that in two cases saccular and utricular maculae came from the same inner
ears precludes a difference in findings due to sampling. The conclusion thus far is that saccular and utricular
maculae differ in responses to weightlessness, with utricular type II hair cells showing the greater plasticity in
weightlessness. This result may be related to functional differences described by Fernandez and Goldberg (1976a,b).
Their experimental findings indicated that utricular afferents were most responsive to static tilt in the X direction
(left-right) while saccular afferents were primarily sensitive to Z direction (vertical or dorsoventral) tilt. Saccular
maculae had a lower sensitivity to static tilt. Present and previous findings (Ross, 2000) additionally show that
weightlessness has differing effects on striolar and posterior portions of the utricular macula. This is likely due to
varying morphological features of receptive fields. The resultant of gravitoinertial vectors acting on type I and type
II hair cells of a receptive field, plus parallel processing by many afferents, determines the message delivered to
central sites. Type II cells may be particularly sensitive to static stimuli and gravity while type I cells may be more
sensitive to phasic stimuli and translational accelerations (Ross, 2000). According to this hypothesis, the maculae
use two kinds of receptors as comparators to determine the afferent’s signal, with morphological variations from
location to location (including macular geometry and otoconial loading) contributing to the outcome.
Work is to be completed on postflight (PF2) and Basal samples. All data will be subjected to analysis of variance.
Fernandez C and JM Goldberg (1976a) Physiology of peripheral neurons innervating otolith organs of the squirrel
monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39:970-984.
Fernandez C and JM Goldberg (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel
monkey. II. Directional selectivity and force-response relations. J Neurophysiol 39:985-995.
Ross MD (1993) Morphological changes in rat vestibular system following weightlessness. J Vestib Res 3:241-251.
Ross, MD (1994) A spaceflight study of synaptic plasticity in adult rat vestibular maculas. Acta Otolaryngol
(Stockh) Suppl 516:1-14.
Ross MD (2000) changes in ribbon synapses and rough endoplasmic reticulum of rat utricular macular hair cells in
weightlessness and 1-g environments. Acta Otolaryngol (Stockh.) 120:490-499.
Orthostatic Intolerance and Autonomic Cardiovascular Changes after Parabolic
Todd T. Schlegel1
, Troy E. Brown2
, Scott J. Wood3
, Edgar W. Benavides2
, Roberta L. Bondar4
, Flo Stein5
, Deborah L. Harm1
, Janice V. Meck1
and Phillip A. Low6
Life Sciences Research Laboratories, National Aeronautics and Space Administration, Johnson Space Center,
Houston, Texas; 2
Wyle Laboratories, Houston, Texas; 3
Baylor College of Medicine, Houston, Texas; 4
Polytechnic University, Toronto, Ontario, Canada; 5
Maple Lake Non-Invasive Laboratory, Farmington, New Mexico;
Autonomic Reflex Laboratory, Mayo Foundation, Rochester, Minnesota. E-mail: firstname.lastname@example.org
INTRODUCTION: It is not clear that orthostatic intolerance (OI) in returning astronauts is strictly
contingent upon prolonged exposure to microgravity. To gain insight into acute conditions that may
exacerbate postspace-flight OI, we investigated the effects of brief parabolic flights—and of parabolic
flight-induced vomiting—on orthostatic tolerance and autonomic cardiovascular function. CURRENT
STATUS OF RESEARCH: Methods: R-R interval and arterial pressure power spectra, carotid-cardiac
baroreflex and Valsalva responses, and tolerance to 30 min of 80-degree head-up tilt (HUT) were measured
in 16 healthy subjects both before and after brief (2 hr) parabolic flights in the seated position. Results:
After parabolic flight: 1) the incidence of OI increased fourfold, with 8 of 16 subjects unable to tolerate 30-
min of HUT, compared to 2 of 16 subjects before flight; 2) 6 of 16 subjects vomited; 3) new intolerance to
HUT was associated with exaggerated falls in total peripheral resistance (P<0.05), whereas vomiting was
associated with increased supine R-R interval variability and carotid-cardiac baroreflex responsiveness
(P<0.05); and 4) the mode of new OI differed in subjects who did and did not vomit, with newly-intolerant
Vomiters experiencing comparitively isolated upright hypocapnia and cerebral vasoconstriction and newly-
intolerant non-Vomiters developing signs and symptoms reminiscent of the clinical postural tachycardia
syndrome. Conclusions: Results suggest first, that syndromes of OI resembling those occurring after space
flight can occur after a brief (2 hr) parabolic flight; and second, that recent vomiting can influence not only
responses to HUT, but also the results of supine tests of autonomic cardiovascular function commonly
measured in returning astronauts. FUTURE PLANS: An investigation of autonomic cardiovascular
responses to rapid HUT (in both pitch and roll) in labyrinthine-deficient vs. age- and gender-matched
healthy individuals. INDEX TERMS: Postural tachycardia syndrome, vomiting, microgravity,
hypergravity, vestibular, autonomic, baroreflex.
VESTIBULAR CONTROL OF SYMPATHETIC ACTIVITY
Horacio Kaufmann*, Italo Biaggioni †, Andrei Voustianiouk*, André Diedrich†, Fernando Costa†, Martin Gizzi‡,
Stephen Moore *,Theodore Raphan,* & Bernard Cohen* * Department of Neurology, Mount Sinai School of
Medicine, New York, New York 10029, USA † Department of Medicine, Vanderbilt University, Nashville,
Tennessee 37232, USA ‡ New Jersey Neuroscience Institute, JFK Medical Center, Edison, New Jersey 08818, USA
The otolith organs sense head position with regard to gravity and initiate compensatory ocular and postural
reflexes that maintain upright posture. In the cat, these receptors also regulate sympathetic efferent vasoconstrictor
activity, which contributes to blood pressure maintenance during orthostatic stress. To test whether vestibulo-
sympathetic reflexes are present in humans, we stimulated otolith receptors along different head axes with off-
vertical axis rotation (OVAR) and recorded eye movements, pupillary diameter, beat-to-beat blood pressure, heart
rate, respiratory rate and sympathetic efferent activity in the peroneal nerve with a miniaturized microneurography
device. During OVAR, pupillary diameter, blood pressure, respiratory rate and sympathetic efferent activity to
skeletal muscle (MSNA) were entrained at the frequency of rotation,. MSNA increased in the nose-up position and
decreased when nose-down while the pupil constricted during nose up and dilated during nose down. MSNA was
closely correlated with blood pressure when nose-down, while arterial pressure was increasing, with a latency of
1.38 s, indicating that, in this position, it was driven by baroreflex afferents. MSNA was not correlated with blood
pressure but was tightly correlated with the gravito-inertial acceleration vector during the nose-up position, when
blood pressure was decreasing, at a latency of 0.6 s and was not affected during transient voluntary apnea. Hence, in
addition to the baroreflex, a gravitoinertial-sympathetic reflex most likely originating in otolithic vestibular neurons,
is present in humans and may contribute to blood pressure maintenance during forward linear acceleration, such as
experienced upon standing. Impairment of vestibular-sympathetic reflexes may contribute to orthostatic intolerance
in returning astronauts.
THE ROLE OF GRAVITOINERTIAL FORCE BACKGROUND, SPATIAL
ORIENTATION AND CONTACT CUES IN PERTURBATIONS OF REACHING
MOVEMENTS BY CORIOLIS FORCES
P. DiZio and J.R. Lackner . Ashton Graybiel Spatial Orientation Laboratory, Brandeis
University MS033, Waltham, MA 02545
The objective of the proposed research is to provide a technical base for evaluating the feasibility
of a rotating "artificial gravity" environment for long-duration space missions. Our focus is on
sensory-motor control and spatial orientation, and our goal is to understand how Coriolis forces
that are generated by body movements in a rotating environment disrupt movement coordination
and how to alleviate or prevent these disruptions. Previous studies showed that Coriolis forces
generated by arm reaching movements in a slow rotation room (SRR) disrupt the paths and
endpoints of the reaches but complete adaptation at 10 rpm is possible within 20 movements
even without visual feedback (Lackner & DiZio, 1994). The studies summarized here examined
1) whether studies conducted in the SRR in 1g accurately predict Coriolis perturbations and
adaptation in different force backgrounds, 2) whether neuromotor compensation for Coriolis
forces in the SRR involves neuromotor mechanisms that subserve reaching in a normal terrestrial
environment, and 3) the role of fingertip contact cues in calibration of reaching movement
CURRENT STATUS OF RESEARCH
Coriolis Perturbations and Adaptation in Non-terrestrial Force Backgrounds
Blindfolded subjects seated over the axis of a rotating chair attempted to reach forward from a
midline start button to a location 35 cm straight ahead also on their midline. Movements began
and ended on a waist-high, smooth desktop, and the fingertip was tracked with a motion analysis
system. Five subjects were each tested in the 0 g and 1.8 g phases of parabolic flight as well as
in 1 g, on separate days. Cued to move in the desired force level of successive parabolas, they
were able to complete 20 movements while stationary, 40 movements during 10 rpm
counterclockwise rotation, and 20 post-rotation, in one 40 parabola mission. Per-rotation reaches
were delayed until 2 minutes after rotation onset in order to allow semicircular canal activity to
equilibrate. The movements generated transient rightward Coriolis forces on the reaching arm,
which deviated reaching endpoints and movement paths to the right, relative to pre-rotation
baseline. Comparable errors occurred in 1 g, 0 g and 1.8 g. Complete adaptation of endpoint
and of path curvature were achieved during rotation, but adaptation was most rapid in 1 g.
Symmetric aftereffects were present when rotation stopped in all force backgrounds, and re-
adaptation occurred most quickly in 1 g.
Coriolis Effects During Active Turning and Reaching
Coriolis forces generated during passive, constant velocity rotation in either the SRR or a
rotating chair perturb reaching endpoint and trajectory until adaptation occurs. In these
conditions, there is no physiological signal indicating that the body is rotating. In a natural
environment, self-generated Coriolis forces are created whenever a reaching movement is made
and the torso is simultaneously turning. Subjects actively plan and control voluntary torso
rotation and receive sensory-motor feedback during their rotation. We measured the magnitude
of the Coriolis interaction torques and the accuracy of reaching movements directed toward
target locations that required synergistic, voluntary turning of the torso and extension of the arm.
These movements generated Coriolis torques about twice as large as in our previous 10 rpm SRR
experiments. However, reaching movement paths and endpoints were not deviated, compared to
performance in trials involving target locations requiring extension of the arm with no torso
The Role of Fingertip Contact Cues in Calibration of Reaching Movement Endpoint.
An unexpected result in previous studies was that fingertip contact with a surface at the terminus
of target-directed reaches is essential for adaptive elimination of endpoint errors caused by
transient Coriolis force perturbations in a rotating room (Lackner & DiZio, 1994). Therefore,
we measured how fingertip landing forces relate to reaching endpoint on a horizontal surface
when no perturbations are present. Four subjects stood in front of a 40 by 60 cm force plate
(Kistler Model 9268) resting on a desktop at waist height, in a normal stationary environment. A
laser dot was projected in various locations (7 or 22 cm distance, and 11 lateral locations at 5 cm
intervals), and subjects were instructed to reach and touch the target position using comfortable
arm and torso motions at a natural speed and to hold the finger in the touchdown position for 2
sec. The resultant forces 30-50 ms after initial contact peaked at ∼6 N and settled at ∼4 N by 200
ms. Horizontal shear forces decayed rapidly in this interval and then hovered around zero, the
vertical component remained constant over time. There were significant variations in peak
horizontal impact force as a function of target distance and lateral position. The direction of
horizontal impact force was highly correlated with target direction relative to the shoulder.
These three studies show that: 1) Studies performed in a rotating artificial gravity environment in
a 1 g force background predict accurately motor disruptions due to Coriolis force perturbations in
0 g and 1.8 g. Rapid adaptation to 10 rpm rotation is possible in 0g, 1 g and 1.8 g. 2) Motor
compensations for and adaptation to Coriolis perturbations is part of our natural neuromotor
repertoire. Central nervous system registration of self-rotation is an important context cue in
control of Coriolis interaction torques. 3) Terminal fingertip contact forces provide a spatial map
of reaching movement endpoint that contribute to calibration of limb position and sensorimotor
SELF-MOTION SYSTEM FREQUENCY RESPONSE: IMPLICATIONS FOR
D. E. Parker1,2
, H.B. L. Duh2
, J. O Phillips1
and T. A. Furness2
Department of Otolaryngology – HNS and 2
Human Interface Technology Laboratory, University of Washington,
Seattle, WA 98195-7923
Using a postural stability measure, we determined the frequency response of the visual self-motion system.
Based on the results, we proposed a visual-vestibular cross-over frequency range and hypothesized that conflicting
visual and inertial self-motion cues at the frequency of maximum cross-over would be more likely to evoke
simulator sickness (SS) / cybersickness than conflicting cues at a higher frequency. This hypothesis was supported
experimentally. Implications for alleviation of SS are discussed.
CURRENT STATUS OF RESEARCH
Three experiments are described. Experiments 1 and 2 determined postural disturbance evoked by visual
scene oscillation at different frequencies. Experiment 3 recorded SS at 2 frequencies of visual-vestibular conflict.
Methods – Experiments 1 and 2
Experiment 1. 11 subjects stood on a balance platform while viewing a scene that oscillated in roll. The
Chattecx balance platform automatically calculated dispersion around the center-of-balance. The visual scene, a
waterfall on the island of Maui, was presented on a VR4 head-mounted display that has a nominal 48° x 36° field-
Frontal visual scene roll oscillation was presented at 5 frequencies: 0.8, 0.4, 0.2, 0.1, 0.05 Hz. Peak scene
velocity was constant across frequencies (70°/sec). Subjects in a sharpened Rhomberg stance attempted to stand
steady during 10-sec data collection periods. Baseline data were collected in darkness before and after the visual
stimulus trials. The following data were collected for each trial: subjective difficulty rating (1-10 scale) and
dispersion of the center-of-balance.
Experiment 2 replicated Experiment 1 with the following changes. The visual scene was a simple black and
white radial pattern, similar to a propeller. This image was back-projected by a video projector onto a 36 inch
coated plastic dome. 10 subjects stood on the balance platform leaning forward so that their heads in the dome. The
FOV was about 180° x 180°.
Results - Experiments 1 and 2
Because of large inter- and intra-subject variability, difficulty ratings and balance dispersion scores were
‘standardized’: each visual trial score was divided by the average baseline performance for that subject. The results
from Experiments 1 and 2 illustrated in Fig. 1 show that balance disturbance was inversely related to scene
oscillation frequency. Statistical analysis (ANOVA) indicated that the effects of frequency were highly significant.
Conclusions - Experiments 1 and 2
The visual self-motion system exhibits low-pass filter characteristics. At frequencies below 5 Hz, the
vestibular self-motion system operates as a high-pass filter. Combining the data from Experiments 1 and 2 with a
previously reported vestibular frequency response (Melvill Jones & Milsum, 1965), we suggest that maximum
overlap between the 2 self-motion systems occurs at about 0.04 Hz. Conflicting motion cues at this frequency should
Methods – Experiment 3
Experiment 3. Using a rotator, 10 subjects were oscillated around their yaw axis at low frequency (0.07 or
0.08 Hz) or high frequency (0.20 or 0.18 Hz). Simultaneously they viewed a scene comprised of black and white
vertical stripes and also oscillated around the their yaw axis at low frequency (0.03 or 0.05 Hz) or high frequency
(0.20 or 0.25 Hz). The images were presented on the VR4. Peak chair angular velocity was about 60º/sec.
To generate conflicting motion signals, visual and inertial oscillation were presented at slightly different
frequencies. For example, rotator oscillation at 0.07 Hz was combined with visual scene oscillation at 0.05 Hz.
Consequently, the phase relationship between the self-motion cues from the visual and inertial signals changed
continuously. Each subject received a maximum of 20 trials alternating between low and high frequency. The initial
trial was always low frequency so that carry-over effects worked against our hypothesis. SSQ symptoms [Kennedy
et al. (1993) International Journal of Aviation Psychology, 3, pp 203-220] were recorded before the experiment
started as well as during after each trial. The experiment was terminated if stomach awareness persisted for longer
than 1 minute following a trial, if “moderate” nausea was reported, or at the subject’s request.
Results – Experiment 3
Useful data were obtained from 8 subjects. Fig. 2 illustrates data from a moderately susceptible subject who
completed the full set of trials. Note that SS symptoms gradually increased across trails Note also that low frequency
oscillation evoked more SS than high frequency oscillation. Mean Total Sickness (TS) scores were significantly (p
= 0.012) larger for low frequency chair / scene oscillation (195.5) than for high frequency oscillation (128.8). Mean
Nausea scores also were significantly (p = 0.014) larger for low frequency oscillation (22.0) than for high frequency
Conclusions - Experiment 3
Our hypothesis is that simulator sickness may be most readily evoked by visual-inertial conflicts in the
frequency range where both the visual and the inertial self-motion systems are active. As expected, subjects reported
more motion sickness for low frequency conflicting motion stimuli than for higher frequency stimuli.
We are currently developing interventions to alleviate SS / cybersickness that we are evaluating using the
procedures described in the studies presented here.
Motion sickness, simulator sickness, cybersickness, sensory conflict, frequency response
Supported by a Contract with Eastman Kodak and National Aeronautics and Space Administration Grants NAG5-
4074 and NCC 9-56. We thank M. F. Reschke for loaning us the rate table, D. L. Harm for loaning us the balance
platform and Ryan McCaskey Cameron Lee, and Hillary Cummings for their assistance.
Fig. 1. Visual-Vestibular Cross-Over. Solid line:
vestibular response. Dashed line: visual response --
combined normalized data from Experiments 1 and 2.
Maximum overlap appears be about 0.04 Hz.
Fig.2 . SSQ Scores for low frequency chair / scene
oscillation (dashed line) and high frequency out-of-
phase oscillation (solid line).
STS-90 NEUROLAB EXPERIMENTS ON THE ROLE OF VISUAL CUES IN
MICROGRAVITY SPATIAL ORIENTATION.
, IP Howard2
, T Smith1
, AC Beall1
, A Natapoff1
, JE Zacher2
, and HL Jenkin2
Man Vehicle Laboratory, MIT, Cambridge, MA ; 2
Human Peformance Lab, York University, Toronto.
Purpose. Since gravitational "down" cues are absent in weightlessness, astronauts rely on vision and
proprioception for spatial orientation. Many maintain a local "subjective vertical" (SV), as evidenced by
reports of inversion illusions and visual reorientation illusions (VRIs). Instability in the SV direction in
micro-gravity can trigger space motion sickness.
Methods. On Neurolab, a Virtual Environment Generator (WinNT Pentium II PC driving a color 68deg
x45deg FOV stereo HMD) was used to quantify the direction of the SV when viewing static and rotating
visual scenes, susceptibility to circular and linear vection, and effects of SV manipulation on figure
recognition and shading interpretation. Results. Both linear and circular vection illusion magnitude
increased on flight day 4 in 2 subjects, and by day 16 for a third, when tested free floating vs. preflight
erect and supine. Both linear and circular vection were reduced in flight when a harness was worn which
held the subjects firmly to the deck with a 88 lb. force. Static visual scene orientation strongly influenced
the SV of one subject in flight and early postflight, but the SV of the other three was congruent with their
body axis. VRI frequency and onset angle in supine testing preflight and in flight were similar for most
subjects. We hypothesized that even in micro-gravity, complex figure recognition and interpretation of
shape from shading would show effects of SV manipulation. Three subjects had response biases or
performed the task inconsistently, which may have masked the effect. However, one demonstrated both
effects consistently, showing that choice of SV can have important perceptual consequences.
Conclusions. Results indicate that most astronauts become more dependent on dynamic visual and
proprioceptive cues, and some also respond to static visual orientation cues. The direction of the SV is
labile, and can influence figure recognition and shading interpretation.
Supported by NASA Contract NAS9-19536 and Canadian Space Agency 9F007-5-8515.
Index Terms: Neurovestibular, Neurolab, Spatial Orientation, Vection, Virtual Reality, Vision, Space
Physiology, Space Sickness
VISUAL ORIENTATION IN UNFAMILIAR GRAVITO-INERTIAL
Charles M. Oman1
, Ian P. Howard2
, Wayne L. Shebilske3
and Jeffrey S. Taube4
Massachusetts Institute of Technology1
, York University2
, Wright State University3
, and Dartmouth College4
INTRODUCTION: The most overt change affecting an astronaut in space flight is the immediate response of the
neurovestibular system to changes in gravity level. NASA’s Critical Path Roadmap defines spatial disorientation and
reduced performance on cognitive and physical tasks as one of the primary biomedical risks of spaceflight. On
earth, gravity provides a convenient “down” cue. Large body rotations normally occur only in a horizontal plane.
In space, the gravitational down cue is absent. When astronauts roll or pitch upside down, they must recognize
where things are around them by a process of mental rotation which involves three dimensions, rather than just one.
While working in unfamiliar situations they occasionally misinterpret visual cues and experience striking “visual
reorientation illusions”, in which the walls, ceiling, and floors of the spacecraft exchange subjective identities. VRIs
cause disorientation, reaching errors, trigger attacks of space motion sickness. MIR crewmembers say that 3D
relationships between modules - particularly those with different visual verticals - are difficult to visualize. Crew
members learn routes, but their apparent lack of survey knowledge is a concern should fire, power loss, or
depressurization limit visibility.
CURRENT STATUS OF RESEARCH:
Human visual orientation. We used an 8 foot tumbling room at York to investigate how the perception of self
orientation with respect to the vertical is dominated by gravity, the visual frame of reference provided by the room’s
realistic interior, or by the relative orientation of the subject’s body. There is a natural tendency to perceive the feet
as “down”. It has long been known that moving visual scenes can produce compelling illusions of self motion, but
it was not understood that motionless visual scenes could produce large sensations of static tilt under some
circumstances. We showed that when gravitationally supine subjects view a furnished room interior that was
similarly tilted 90 degrees with respect to gravity, so that it appeared upright with respect to their body, a majority of
subjects felt gravitationally upright. We call this a “Levitation Illusion”. If subjects extended their limbs above
their supine body, their limbs felt weightless. The strength of the illusion has been systematically studied in a large
group of subjects with the room and the subject in all the different possible orientations, modulo 90 deg. In certain
other relative orientations, subjects experienced VRIs– for example they perceived the floor of the room as a ceiling.
Susceptibility to the levitation illusion consistently increased with age. Vestibular function is known to degrade
with age, and the association between the orientation of familiar visual objects and gravity (which we refer to as
“visual polarity”) is probably a learned phenomenon. In a related experiment, we constructed a “mirror bed” device,
which allowed us to quantify how “visual polarity”. A subject lying gravitationally supine in the bed views the
laboratory through a mirror mounted at 45 degrees over his head. When strongly polarized objects are in view, the
subject interprets the view as horizontal, and feels subjectively almost upright. When weakly polarized objects are
seen, the subject feels nearly supine. Intermediate tilt perceptions can be created by manipulating the polarity (type
and arrangement) of objects in the visual scene. Understanding how the relative orientation of gravity, body axis
and the visual scene interact is potentially important for astronaut training, and also in entertainment and clinical
applications. Strongly polarized objects and pictures may prove useful in reducing the incidence of disorienting
VRIs in space station modules. Placing strongly polarized pictures in staircases might help some elderly people be
less prone to falling.
Three dimensional spatial memory and learning. What limits human ability to orient and navigate in a 3D
weightless environment ? Can spatial abilities in such 3D environments be improved by preflight training ? Most
navigation and spatial memory research has addressed only the terrestrial situation. We designed several 3D spatial
tasks (Oman, et al, 1999, 2000; Shebilske et al, 2000; Richards, 2000; Richards et al, in preparation) analogous to
those confronting astronauts trying to learn the spatial relationships between the six entrance hatches in a space
station node module of a space station. Experiments were conducted in both real and virtual environments. After a
brief period training, many subjects were able to perform the spatial tasks in any relative orientation to the visual
environment. Gravitational body position (erect vs. supine) had little effect. Subjects chose to remember the
relationships amongst objects as they would appear with the room in a specific “baseline” orientation, and
memorized opposite pairs of objects. Formal training with these concepts helped. Performance also correlated with
conventional paper-and-pencil tests of figure rotation ability. Subjects trained in two different environments
successively learned faster in the second, suggesting they “learned how to learn”. Ability was retained one day, one
week, and even one month after initial training. Another experiment showed that learning with randomly chosen
rather than grouped (blocked) sets of room orientations enhanced ultimate performance. We are currently extending
the paradigm to measure spatial memory across two previously learned modules, one of which is unseen. We want
to know if coalignment of the baseline memorized module orientations is critical for performance. Our ultimate
objective is to develop a methodology/pedagogy for generic and mission specific ISS preflight visual orientation
training. Another application of our paradigms is in the design and evaluation of emergency escape route markings
and systems of visual landmarks within modules that help crewmembers keep track of the principal axes of the ISS.
Neural coding of spatial orientation in an animal model. We conducted experiments in a Long-Evans rat model to
better understand how the human sense of place and direction may be coded in 3 dimensions. In rats and primates,
limbic “head direction” cells appear to code head direction in a gravitational horizontal plane, independent of the
animal’s location, and roll or pitch of the head up to 90 degrees. The maximum response (“preferred direction”) lies
in a fixed direction which varies from cell to cell. In 1-G, moving a prominent background visual landmark results
in a corresponding re-orientation of the preferred directions of all HD cells by the corresponding angle. Until now,
HD cells response has been studied only in a gravitationally horizontal plane. We trained rats to crawl up a wall,
across a ceiling and down the opposite wall, in an apparatus that allows us to verify the 3D response characteristics
of HD cells in 1-G, and infer whether the response sensitivity remains anchored by gravity or whether the response
coordinate frame of the cell re-orients to the animal’s locomotion plane. Cells in some animals show robust
direction specific firing in the same world-centered reference frame when the animal is walking upside down, and
response on the walls depends on the wall and whether the animal was going up or coming down, as expected. In
other animals, the cells lose their direction specific firing on the ceiling. and there is a significant increase in
background firing, suggesting that the animals may be disoriented. We have also studied HD cell responses in
parabolic flight in a test chamber that was visually symmetrical in an up-down direction. All cells HD cells studied
maintained their direction specific discharge when the animal was on the floor or the wall of the chamber. However,
when placed on the ceiling of the chamber, HD cell directional specificity was frequently lost. In some cases, the
preferred direction of HD cell response reversed across the visual axis of symmetry of the cage, as expected if the
cell’s response coordinate frame had reoriented to the ceiling. When humans roll inverted in parabolic flight and put
their feet on the ceiling of the aircraft, they experience a VRI in which the ceiling seems like a “floor”, and the left-
right axis is reversed. We believe this is the first demonstration of the limbic correlate of a human 0-G spatial
orientation illusion. Our experiments provide insights on the role played by gravireceptors in stabilizing the human
sense of place and direction not only in astronauts, but also in vestibular and Alzheimer’s disease patients.
Allison, R., Howard, I.P., and Zacher, J. (1999) The effect of field size, head motion and rotational velocity on roll
vection and illusory self-tilt in a tumbling room. Perception, 28, 299-306.
Calton JL, Tullman ML, Taube JS (2000) Head direction cell activity in the anterodorsal thalamus during upside-
down locomotion. Soc Neurosci Abstr, Vol 26, Part 1, p. 983
Howard, I and Hu G. (1999) Visually induced reorientation illusions. Submitted to Perception.
Howard, I.P. and Jenkin, H.L. and Hu, G. (2000) Visually induced reorientation illusions as a function of age.
Aviation, Space and Environmental Medicine, 71(9), A87-A91.
Oman C, Shebilske W, Richards J, Tubre T, Beall A, Natapoff A. (2000) Three dimensional spatial memory and
learning in real and virtual environments. J. Spatial Cog. and Comp. (submitted)
Richards, JT (2000) Three dimensional spatial learning in a virtual space station node. SM Thesis, Dept. of
Aeronautics and Astronautics, MIT, Cambridge, MA September, 2000.
Shebilske, WL., Goettl, BP., & Garland, D. (in press). Situation Awareness, Computer-Automation, and Training. In
M. R. Endsley & D. Garland (eds.), Situation awareness analysis measurement. Mahwah, NJ: Lawrence Erlbaum.
Shebilske, W. L., Tubre, T., Willis, T., Hanson, A., Oman, C., and Richards, J. (2000). Simulating Spatial Memory
Challenges Confronting Astronauts. Proceedings of the Annual Meeting of the Human Factors and Ergonomics
Society, July 30, 2000.
Stackman RW, Tullman ML, Taube JS (2000) Maintenance of rat head direction cell firing during locomotion in the
vertical plane. Journal of Neurophysiology 83: 393-405.
Taube JS, Stackman RW, Oman CM (1999) Rat head direction cell responses in 0-G. Soc Neurosci Abstr 25: 1383.
Supported by NASA Cooperative Agreement NCC9-58 with the National Space Biomedical Research Institute
Visually-induced Adaptation of the Translational Vestibulo-Ocular Reflex
MIN WEI, HUI-HUI ZHOU AND DORA E. ANGELAKI
Dept. of Neurobiology, Washington University School of Medicine, St. Louis, MO 63110
The adaptive plasticity of the translational vestibulo-ocular reflex has been
investigated in rhesus monkeys after two hour exposure to either vertical or torsional
optic flow stimulation accompanied by lateral translation stimuli (0.5 Hz). Because of the
inherent ambiguity in the otolith system for the detection of linear accelerations, we
hypothesized that cross-axis adaptation of the translational VOR during lateral motion
would be preferentially selective for a torsional optic flow stimulus that would mimic a
roll tilt movement. However, the present results do not support this hypothesis. Instead,
there was a selective and significant increase in the amplitude of the orthogonal eye
movement component after exposure to both vertical and torsional optic flow stimulation.
Moreover, there was no difference in the size of adaptive changes for opposite directions
of torsional flow stimuli, including those in phase and out of phase with linear
acceleration. These results suggest that, at least at 0.5 Hz, there seems to be no
preferential visually-induced adaptive capacity of the otolith system for tilt/translation re-
interpretation during motion. Similarly as with the rotational VOR, translational VOR
exhibits a general form of cross-axis adaptation that operates for different directions of
optic flow stimulation.
OTOLITH AND VERTICAL CANAL CONTRIBUTIONS TO DYNAMIC
Kaufman, G.D. 2
, F. O. Black1
, C. C. Gianna1
, W. H. Paloski2
and S. J. Wood1
Legacy Health System, Portland, OR; 2
Johnson Space Center, Houston, TX
Our experiments focus on issues related to the effect of artificial gravity on vestibulospinal adaptation. Adaptation to
microgravity requires a re-organization of central nervous system (CNS) processing of the three major sources of
spatial information on earth: visual, vestibular and somatosensory (proprioceptive). Adaptation to microgravity is
characterized by a combination of perceptual and physiological responses to changes in gravitational acceleration.
Experimental results to date support the hypothesis that the absence of a gravity vector leads to adaptive changes in
neural strategies used for resolving ambiguous linear accelerations detected by the otolith systems. In the absence of
gravitational vertical, normally ambiguous visual references on earth become critical for orientation on orbit. In
microgravity, contact surfaces determine initial and final orientation references. The scientific goal of this ground-
based research is to understand how canal and otolith-mediated responses to linear translation and roll tilt can be
adapted by altered sensory environments. One question for effective sensorimotor countermeasure development is
the extent to which otolith-mediated responses can be adapted such that stimulation normally inducing tilt responses
will instead induce translation responses (and vice versa). Our first set of ground based experiments have addressed
this problem by studying postural responses to altered gravito-inertial vectors.
The postural instability immediately after shuttle egress observed in all crewmembers studied to date appears less
severe with increasing flight experience. This observation suggests that experienced astronauts may be able to
maintain contextually dependent adaptive states. Our results also support the hypothesis that exposure to artificial
gravity induced by centrifugation could be employed as a sensorimotor countermeasure during long duration space
CURRENT STATUS OF RESEARCH
Our project has studied postural control adaptation to dynamic linear acceleration stimuli delivered using a short arm
variable radius human centrifuge. Efficacy of adaptation protocols was measured using otolith-mediated roll-tilt
perception and postural stability in normal and vestibular deficient subjects. In all experiments, response variability
of each subject was determined with reference to baseline measures of each response. The adaptation period, from
30 to 90 minutes, consisted of constant velocity centrifugation. Short-arm centrifuge devices were driven by direct
drive motors (300 ft-lb at NASA, 80 ft-lb at Legacy). Subjects were seated upright with the long body (z) axis
parallel to, but 80 cm offset from, the Earth vertical axis of rotation. A snug four-point safety harness, and vacuum-
forming cushions, restrained the subject as comfortably as possible. The subject's head was free to rotate in all three
planes, but a cushioned stop provided relief from neck strain caused by the centrifugal force. The subjects faced
forward tangentially with the left (LEO) or right (REO) ear directed radially away from the axis of rotation.
Unilateral vestibular deficient subjects were tested in both orientations while all others were tested in only one
orientation. At the NASA facility, a one meter diameter hemisphere dome in front of the subject, and shrouds
attached around the subject chair, minimized rotation-related wind and sound cues. At the Legacy facility, no dome
or shroud was used, and the LED targets were presented on a thin aluminum bar.
Following a 20 s ramp-up period at a constant angular acceleration of 10 deg/s2
, the centrifuge angular velocity
was maintained constant for 90 min (in some cases, the adaptation period was shortened at the subjects’ request) at
200 deg/s, resulting in a gravito-inertial force (GIF) vector of 1.4 g tilted 45 deg in roll with respect to the subject.
After the adaptation period, the centrifuge was decelerated at 10 deg/s2
to a complete stop.
Our results showed that: 1) a 1.4 g artificial gravity stimulus (roll plane centripetal acceleration) over a period of 90
min is sufficient to induce postural and subjective vertical changes in normal subject s; 2) these changes are
dependent on both the orientation and magnitude of the applied gravito-inertial force (GIF), and perhaps on cross-
coupling forces; and 3) the changes require intact vestibular (presumably otolith) input.
After establishing the extent to which otolith-mediated tilt and translation responses can be adapted at different
stimulus frequencies and GIF magnitudes, our next series of experiments will examine whether subjects can 'dual
adapt' to altered sensory environments using the orientation of gravity to provide context. We will investigate
context specific adaptation by varying visual and somatosensory references. Demonstration of ‘dual-adaptation’ to
altered sensory environments will provide insight into the feasibility of using intermittent exposures to artificial
gravity induced by centrifugation as an in-flight sensorimotor countermeasure.
otolith, posture, adaptation, centrifuge, countermeasure
CHARACTERIZATION OF SENSORY INTEGRATION AND CONTROL STRATEGIES
THAT REGULATE HUMAN POSTURAL CONTROL IN CHANGING CONDITIONS
R. J. Peterka
Neurological Sciences Institute, Oregon Health Sciences University, Portland, Oregon 97006
Most researchers agree that human postural control requires active regulation via feedback
mechanisms to maintain balance. It is of interest to understand (1) how different components in
the feedback system influence overall postural stability, (2) how the postural control system uses
visual, proprioceptive, and graviceptive sensory cues, and (3) how the system compensates for
external perturbations, altered sensory environments, and sensory deficits. A basic
understanding of the postural control system should contribute to determining why astronauts
have balance problems following space flight, and perhaps how compensation can be facilitated.
CURRENT STATUS OF RESEARCH
We performed experiments that perturbed quiet stance using support surface and/or visual
surround rotational motions that evoked anterior/posterior (AP) body sway in subjects with
normal sensory function and with bilateral vestibular loss. The rotational motion followed a
pseudorandom waveform (60.5 s period) whose velocity amplitude spectrum was approximately
constant up to about 2.5 Hz. Each trial presented six to eight cycles of the pseudorandom
waveform with a peak-to-peak stimulus amplitude ranging from 0.5° to 8°. The response was
considered to be AP center-of-mass (COM) body sway angle. A cross spectral analysis between
the stimulus and response provided transfer function gain, phase, and coherence data that
characterized the dynamic behavior of the postural control system, and indicated the linearity of
the stimulus-response relationship. By convention, a gain value of 1 and phase of 0° at a
particular stimulus frequency indicate that the subject’s COM sway angle was perfectly aligned
with the stimulus (in amplitude and timing) at that frequency. A gain of zero indicates that the
subject’s COM sway angle remained oriented to earth vertical. Transfer function curve fits,
based on a simple feedback control model, were made to the gain and phase data. These curve
fits provided estimates of model parameters including a stiffness factor (corrective torque
proportional to COM position), a damping factor (corrective torque proportional to COM
velocity), response time delay, and a sensory integration factor. The sensory integration factor
provided information about the relative contributions of visual, proprioceptive, and graviceptive
sensory information to stance control.
Body sway responses generally followed the stimulus waveform indicating that subjects
tended to orient to the moving support surface and/or visual surround. For a given test condition,
there was a remarkably linear relationship between the stimulus and response indicated by
coherence function values which were large and changed little with changing stimulus
amplitudes. However, transfer function gains decreased with increasing stimulus amplitude
indicating that the overall behavior of the postural control system was a nonlinear function of
stimulus amplitude. These apparently conflicting results can be reconciled if one hypothesizes
that the relative contribution (sensory channel weighting) of visual, proprioceptive, and
vestibular sensory cues changed as a function of the stimulus amplitude.
For example, when support surface and/or visual stimuli were close to perceptual threshold
levels (0.5° peak-to-peak stimulus amplitude), our model-based analysis indicated that visual
cues contributed about 35%, proprioceptive cues about 50%, and graviceptors about 15% of the
sensory orientation information used by the postural control system. However, with the largest
amplitude stimuli (8°), the postural control system used about 5% visual, 15% proprioceptive,
and 80% graviceptive information. The increased utilization of graviceptive cues produced a
proportionally greater orientation toward earth vertical and less towards the visual or support
surface stimulus, consistent with the observed reduced gains.
In contrast to normals, subjects without vestibular function showed little or no ability to
reduce gain with increasing stimulus amplitude. As a result, body sway increased linearly with
increasing stimulus amplitude, resulting in falls at larger stimulus amplitudes. This is consistent
with a limited ability to alter the proportion of visual and proprioceptive cues used for postural
control. Additionally, the results indicated that the vestibular system was the primary source of
graviceptive information used for postural control over the frequency range tested.
When the stimulus was provided by support surface rotations, other system factors also
changed with increasing perturbations. Subjects increased their stiffness but did not change their
damping. Modeling work demonstrated that an increase in stiffness without an accompanying
increase in damping can lead to resonant behavior (~1 Hz) and eventually to instability.
However, experimental results showed that the increased stiffness was compensated by an
apparent decrease in response time delay from about 190 ms to 100 ms. Response time delay is
usually considered to be a fixed factor which adversely affects a feedback control system.
However, our results suggest the overall dynamic behavior of stance control is maintained, in
part, by actively regulating the response time delay.
The simple task of maintaining quiet stance was shown to involve a complex sensory
integration process where the relative contribution of different sensory systems changes as a
function of environmental and stimulus conditions. Additionally, subjects appear to regulate the
dynamic behavior of their postural control system by changing their stiffness and altering the
timing of corrective responses. Subjects without vestibular function have limited ability to alter
their use of available sensory cues when stimulus conditions change. This suggests that the
vestibular system plays an important role in regulating the sensory integration process. Perhaps
this sensory integration regulation is disrupted in returning astronauts who have altered their
interpretation of vestibular sensory cues to accommodate the free fall environment of space.
Our current model of the postural control system is descriptive in nature. It provides a means
of quantifying experimental results in terms of simple dynamic factors (stiffness, damping, time
delay, sensory channel weighting), and characterizing how these factors change as a function of
stimulus and environmental conditions. The next step is to develop a predictive model that
accurately reflects the true structure and function of the human postural control system.
Postural Control, Balance, Sensory Integration, Vestibular, Vision, Proprioception, Human.
SPATIAL REORIENTATION AND SENSORY-MOTOR BALANCE CONTROL IN
W. H. Paloski1
, S. J. Wood2
, G. D. Kaufman3
, F. O. Black2
, and M. F. Reschke1
Johnson Space Center, Houston, TX; 2
Legacy Health Systems, Portland, OR; 3
UT Medical Branch, Galveston, TX
This space flight investigation will examine changes in spatial processing of sensory-motor function following
adaptation to microgravity and will explore the feasibility of forcing changes between motor program sets optimized
for different gravito-inertial environments. Pre- and post-flight measurements will be made on ten astronaut subjects
(first-time fliers) selected from several short-duration Shuttle missions. Our first specific aim is to examine adaptive
changes in the spatial reference frame used for coding orientation and motion as a function of space flight. By
examining the effects of head tilt on balance control, one of the most significant post-flight manifestations of
sensory-motor adaptation to microgravity, we will test the hypothesis that there is a reorientation of central vestibular
processing from a gravitational frame of reference to a head-centric frame of reference as a function of adaptation to
microgravity. Our second specific aim is to examine the feasibility of altering the readaptation process following
space flight by providing discordant canal-otolith-somatosensory stimuli using short-radius pitch axis centrifugation.
Previous observations by our laboratory suggest that exposure to this stimulus during, or soon after, sensory-motor
readaptation to the terrestrial environment will trigger a switch in central vestibular processing from the external
(gravitational) reference frame used on earth to the internal (head-centered) frame of reference used in microgravity.
Demonstration of centrifuge-induced switching between sensory-motor program sets learned for different
gravitoinertial environments will provide insight into the feasibility of using intermittent exposures to artificial
gravity induced by centrifugation as an inflight sensory-motor countermeasure during long duration space flight
missions. Furthermore, confirmation of these earlier results will have important operational implications for
protecting crew safety by constraining postflight activities of returning astronauts.
CURRENT STATUS OF RESEARCH
The influence of head tilt on the control of postural equilibrium will be studied using a modified NeuroCom
computerized dynamic posturography system. We have previously employed this system’s sensory organization tests
(SOT) to demonstrate postflight reductions in the effectiveness of vestibular control of posture and increased
reliance on visual inputs for posture control. In the present experiments, we propose to use the six standard
NeuroCom SOT conditions, which combine two proprioceptive conditions (fixed-support, sway-referenced support)
with three visual conditions (eyes open, eyes closed, sway-referenced vision). We also propose to incorporate two
additional test conditions to examine the influence of head tilt on balance control with absent vision and inaccurate
(sway-referenced) proprioceptive inputs. The two new conditions will modify the standard SOT 5 by adding dynamic
voluntary head movements and static head tilts. The dynamic head movements will consist of 0.33 Hz sinusoidal
head oscillations in the roll or pitch planes. A modulated auditory tone will will aid the subject in maintaining a
constant frequency of oscillation while operator feedback will be provided to maintain the same magnitude
(approximately 30° in each direction). The static head tilts will consist of fixed 30° right or left head tilts. The static
tilts will be made in the roll plane to avoid changing the antero-posterior center-of-gravity locations and because
normal subjects are capable of performing this maneuver without altering postural stability. We expect that the
changes in head tilt conditions will not significantly affect postural stability in crewmembers preflight; however,
immediately after flight we expect that head tilts will further exacerbate postural instability by decoupling the head-
centered spatial reference frame from the gravity reference frame.
The pitch axis centrifugation stimuli will be provided by the JSC short-arm centrifuge. Pitch rotation will be
provided about an earth-vertical axis with subjects in a left-side down position. The subjects will be oriented with
their interaural axes positioned 50 cm from the axis of rotation (i.e., body center of mass approximately over the axis
of rotation), and thus will be exposed to eccentric rotation (i.e. short-radius centrifugation). The nominal centrifuge
rotation profile will be: 1. Accelerate at 25 deg/sec2
to constant velocity of 140 deg/sec; 2. Maintain constant
velocity rotation at 140 deg/sec for 120 sec (subject in dark); 3. Superimpose a 0.33 Hz, 40 deg/sec sinusoidal
velocity profile upon the 140 deg/sec constant velocity for 20 cycles (subject in dark); 4. Continue the constant plus
sinusoidal profile for 20 more cycles, with matched full field optokinetic stimulus; 5. Return to constant velocity
rotation for 60 sec (subject in dark); 5. Decelerate at 25 deg/sec2
to stop. After the stop the subjects will remain
stationary for two minutes and then the rotation profile will be repeated in the CCW direction. Binocular three
dimensional eye movements will be measured throughout using video-oculography techniques. Perceptual reports of
self-motion will be recorded during the pitch centrifugation. Immediately prior to and following the pitch
centrifugation trials, postural control will be assessed using the sensory organization tests described above.
Subjects will be exposed to the pitch axis centrifugation during two preflight test sessions and two postflight
recovery test sessions, as shown in the figure. The R+3 days time frame was selected for the postflight session based
on our previous posturography studies showing that balance control is nearly recovered in all short duration
crewmembers by this time frame. We do not expect this centrifugation exposure to significantly affect the dependent
measures during the preflight testing or the R+90 days session. However, according to our second hypothesis,
exposure to these discordant stimuli during postflight recovery (R+3) will trigger a return to spatial processing using
a head-centered frame of reference, and will therefore transiently disrupt sensorimotor control. This hypothesis will
be tested by comparing the postural measurements obtained after centrifugation with those obtained immediately
before centrifugation and with those obtained immediately following space flight. Note that crewmembers will tested
again on R+4 days (the day following the centrifuge exposure) and R+8 days to determine whether any disruption to
postflight recovery persists. To comply with the JSC Institutional Review Board recommendations, the subjects will
also be tested at R+90 days. This final test will ensure that participating crewmembers have no long term sensitivity
to the centrifuge stimuli or disruption of sensorimotor function.
R0 R1 R2 R3 R4 R5 R6 R7 R8
o oo oo
A B C
Preflight Inflight Postflight
Figure 1: The measurement timeline per mission consists of three preflight sessions, and postflight sessions on R+
(recovery days) 0, 2, 3, 4, 8 and 90. Each test session (indicated by open circles) will require tests of postural
equilibrium. The anticipated readaptation curve for the postural performance is depicted, showing a disruption in
recovery on R+3 following the pitch centrifugation exposure (solid bar).
A better understanding of the nature of sensory-motor recovery from short space flights will help us determine
the mechanisms of adaptation of balance control. The use of the postflight centrifugation stimulus will allow us to
better understand what sensory stimuli may retard or reverse the readaptation process, and therefore know which
activities may also contribute to decompensation during recovery from vestibular pathology. New understanding
gained in our research on mechanisms of vestibular system conditioning will be fundamental to further development
of artificial gravity countermeasures and potentially to new vestibular rehabilitation techniques.
During the initial phase of funding, experiment definition was completed and the experiment was approved for
implementation as a pre-/post-flight Detailed Supplemental Objective (DSO 635). An experiment crew briefing was
recently completed, resulting in the first flight crew member agreeing to participate during the STS-104 mission in
mid 2001. A preliminary ground-based study has been initiated to refine the posture protocol by examining the effect
of head movement frequency and plane of motion on balance control. In addition, the JSC Short-Arm Centrifuge
Facility is being reconfigured to accommodate the proposed eccentric pitch visual-vestibular interaction paradigm.
PERCEPTION OF TILT (SOMATOGRAVIC ILLUSION) IN RESPONSE TO
SUSTAINED LINEAR ACCELERATION DURING SPACE FLIGHT
Bernard Cohen, Gilles Clément, Steven T. Moore and Theodore Raphan
From the Departments of Neurology and Physiology, Mount Sinai School of Medicine, New York, NY
(BC, STM), the Centre de Recherche Cerveau et Cognition, CNRS/UPS,Toulouse, France (GC) and the
Department of Computer and Information Science, Brooklyn College, Brooklyn, NY, USA (TR, STM).
Four astronauts were exposed to interaural and head vertical (dorsoventral) linear accelerations of 0.5-g and
1-g during constant velocity rotation on a centrifuge, both on Earth and during the 1998 Neurolab (STS-90)
orbital space flight. Subjects were oriented either left-ear-out or right-ear-out (Gy centrifugation), or lay
supine along the centrifuge arm with their head off-axis (Gz centrifugation). Pre-flight centrifugation,
producing linear accelerations of 0.5-g and 1-g along the Gy (interaural) axis, induced illusions of roll-tilt
of 20° and 34° for gravito-inertial acceleration (GIA) vector tilts of 27° and 45°, respectively. Pre-flight
0.5-g and 1-g Gz (head dorsoventral) centrifugation generated perceptions of backward pitch of 5º and 15º,
respectively. In the absence of gravity during space flight, the same centrifugation generated a GIA that
was equivalent to the centripetal acceleration and was aligned with the Gy or Gz axes. Perception of tilt
was underestimated relative to this new GIA orientation during early, in-flight Gy centrifugation, but was
close to the GIA after 16 days in orbit. During the course of the mission, in-flight roll tilt perception during
Gy centrifugation increased from 45° to 83° at 1-g and from 42° to 48° at 0.5-g. Toward the end of the
flight, subjects reported that they felt as if they were lying-on-side'. Subjects felt 'upside-down' during in-
flight –Gz centrifugation from the first in-flight test session, which reflected the new GIA orientation along
the head dorsoventral axis. The different levels of in-flight tilt perception during 0.5-g and 1-g Gy
centrifugation suggests that other non-vestibular inputs, including an internal estimate of the body vertical
and somatic sensation, were utilized in generating tilt perception. Interpretation of data by a weighted sum
of body vertical and somatic vectors with an estimate of the GIA from the otoliths, suggests 1) that
perception weights the sense of the body vertical more heavily early in-flight, 2) that this weighting falls
during adaptation to microgravity, and 3) that the decreased reliance on the body vertical persists early
post-flight, generating an exaggerated sense of tilt. Graviceptors respond to linear acceleration and not to
head tilt in orbit, and it has been proposed that adaptation to weightlessness entails reinterpretation of
otolith activity, causing tilt to be perceived as translation. Since linear acceleration during in-flight
centrifugation was always perceived as tilt, not translation, the findings do not support this hypothesis.
Supported by NASA Contract NAS 9-19441
CONTEXT-SPECIFIC ADAPTATION OF GRAVITY-DEPENDENT VESTIBULAR REFLEX
RESPONSES (NSBRI NEUROVESTIBULAR PROJECT 1)
, J. Goldberg2
, L.B. Minor1
, W.H. Paloski3
, L.R. Young4
, and D.S. Zee1
Johns Hopkins University School of Medicine, Baltimore MD, 2
Baylor College of Medicine,
Houston TX, 3
NASA Johnson Space Center, Houston TX, 4
MIT, Cambridge MA
Impairment of gaze and head stabilization reflexes can lead to disorientation and reduced performance in
sensorimotor tasks such as piloting of spacecraft. Transitions between different gravitoinertial force (gif)
environments – as during different phases of space flight – provide an extreme test of the adaptive capabilities of
these mechanisms. We wish to determine to what extent the sensorimotor skills acquired in one gravity environment
will transfer to others, and to what extent gravity can serve as a context cue to assist in maintaining the appropriate
sensorimotor responses in different environments.
We use the general approach of adapting a response (such as the VOR) in a particular manner (e.g. gain increase)
in one context, adapting in a different manner (e.g. gain decrease) in another context, and then seeing if the context
cue itself can cause switching between the previously-learned adapted responses.
Various experiments investigate the behavioral properties, neurophysiological bases, and anatomical substrate of
context-specific learning, emphasizing otolith (gravity) signals as a context cue. The following is an outline of the
methods and major results for each experiment which is a part of this project.
CONTEXT-SPECIFIC ADAPTATION IN PARABOLIC FLIGHT (MS)
This experiment studies the ability of human subjects to switch between two adapted saccade gains based on
various context cues. Saccadic gain is adaptively increased (using a standard double-step paradigm) in one context,
and decreased in the other context, then tested to see if the context cue can cause switching between the two adapted
Results show that saccades can be adapted in a context-specific manner, using vertical eye position, horizontal eye
position, head tilt, and upright/supine orientation as cues. The effectiveness of a cue appears to depend on its
relevance to the response being adapted: horizontal eye position is a more effective cue for horizontal saccade
adaptation than is vertical eye position. Gravity magnitude (0g vs. 1.8g) during parabolic flight can also be used as a
context cue. Some adaptation appears to be retained after 8 months. Lunar and Martian g levels can recall
adaptations imposed during 0 g.
CONTEXT-SPECIFIC ADAPTATION OF THE HUMAN LVOR (MS, DSZ)
This experiment studies the ability of subjects to switch between two adapted LVOR gains based on the context
cue of head tilt (gravity orientation). Subjects are translated laterally at 0.7 Hz, 0.3 g. During adaptation, for 5 min a
visual display moves so as to ask for a gain of ×0 with the head rolled left or pitched up, then for 5 min a gain of ×2
is asked for with the head rolled right or pitched down. This is repeated for 1 hr. Sine and step translations before
and after adaptation determine if head orientation alone causes switching between the two adapted gains.
Results show that the orientation of gravity with respect to the head can serve as a context cue. For inter-aural
translations, head roll is a more effective context cue than is head pitch. This is analogous to the situation with
saccade adaptation: the closer the context cue is to the response being adapted, the more effective it is.
CONTEXT-SPECIFIC ADAPTATION OF RESPONSES TO CENTRIFUGATION (LRY)
This experiment studies context-specific adaptation in human subjects during repeated exposure to short-radius
centrifugation, so that they will have the appropriate oculomotor responses and subjective orientation in both the
rotating and non-rotating environments and be able to switch between them. Subjects make head movements while
rotated at 23 rpm (1g gradient from head to feet), while eye position, subjective orientation, and motion sickness are
Yaw head movements during rotation initially provoke disorientation and inappropriate vertical eye movements.
Repeated head movements in this situation reduce (adapt out) the noncompensatory eye movements. Adaptation to
the centrifugation does occur; three 10-min adaptation sessions produced adaptation that was retained (at reduced
level) a week later. Adaptation to head movements to one side did not generalize to head movements in other
directions. While motion sickness disappears after 10 adaptation sessions, vertical nystagmus and illusory tilt do not.
Context-specificity of the adaptation is apparent since subjects did not experience motion illusions when off the
centrifuge between test sessions.
PROPERTIES AND CONTEXT-SPECIFICITY OF VESTIBULOCOLLIC REFLEX (JG, WHP)
This experiment quantifies and models the contributions of canal and otolith feedback to head movements induced
by trunk rotations and translations in 3 dimensions. The head/neck system is inherently unstable in 1 g and requires
tonic neck activity, mediated via the vestibular system, for upright posture. Rotations (centered and eccentric) are
applied to human subjects while upright or supine, to assess the contributions of gravity and tangential acceleration.
Properties of the head-neck control system (VCR) in three dimensions can be adequately modeled by a relatively
-order linear system, plus a single dead-zone nonlinearity. Adaptation of this system to changes in head
inertia can be induced. This adaptation can be made dual-state, such that the appropriate neural control mechanisms
for head stabilization change modes immediately upon a change in head inertia.
CEREBELLAR CONTRIBUTION TO CONTEXT-SPECIFIC ADAPTATION (DSZ, LBM)
These experiments determine the role of the vestibulocerebellum in otolith-ocular reflexes and their adaptation,
and the relationship between the translational LVOR and pursuit.
In rhesus monkey, bilateral removal of the flocculus and paraflocculus produced almost complete loss of the
horizontal LVOR (even after the angular VOR had recovered). Likewise, human cerebellar patients have comparable
defects in pursuit and the LVOR, while the AVOR appears to be controlled independently. This suggests that the
vestibulocerebellum plays a critical role in the generation of the LVOR, and that there is a tight relationship between
the generation of the LVOR and smooth pursuit. A separate experiment showed systematic variations in the axis of
eye rotation at different vertical elevations, during pursuit, AVOR, and LVOR. Axis tilts for pursuit and LVOR were
almost identical, and different from that for the AVOR, again showing a close relationship between neural processing
for pursuit and the LVOR.
Context-specific adaptation of smooth pursuit eye movements has been demonstrated in both humans and rhesus
monkeys. Using vertical eye position as a context cue, the initial acceleration of the eyes, when presented with a
moving target, can be made to decrease with the eyes elevated, and to increase with the eyes depressed.
LVOR gain adaptation has been induced in squirrel monkeys, and was specific to the frequency used for
adaptation. Following adaptation of LVOR gain, there was no significant change in the torsional eye movements to
head tilt, suggesting that the responses to head tilt and head translation are not tightly coupled.
During extended space flight crew members may live in artificial gravity and make transitions to and from
weightlessness for planetary exploration and return to Earth. If they learn sensorimotor skills such as piloting in the
normal gravity of Earth, will they be able to perform them adequately in the weightless or the artificial gravity
environment? We have convincing evidence for context-specificity in various sensorimotor responses. Such context-
specific adaptation is a potential countermeasure to the performance decrements seen during these transitions. In
addition, experiments on the relationship between pursuit and LVOR have implications for countermeasures based
on adapting translation versus tilt responses mediated by the otoliths.
Sensorimotor adaptation, vestibular, oculomotor, saccade, VOR, LVOR, otolith, Coriolis, VCR, cerebellum,