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Copyright © 2008 Galileo Foundation 1

RISK OF SENSORY-MOTOR PERFORMANCE FAILURES AFFECTING VEHICLECONTROL DURING SPACE MISSIONS: A REVIEW OF THE EVIDENCE

William H. Paloski1,2, Charles M. Oman3, Jacob J. Bloomberg1, Millard F. Reschke1, Scott J. Wood1, Deborah L. Harm1, Brian T. Peters1,Ajitkumar P. Mulavara1, James P. Locke1, and Leland S. Stone4

1 NASA Johnson Space Center, 2101 NASA Parkway, Houston, TX 77058 (USA)2 University of Houston, 3855 Holman St, Houston, TX 77204 (USA)3 Massachusetts Institute of Technology, 77 Massachusetts Ave.,

Cambridge, MA 02139 (USA)4 NASA Ames Research Center, Moffett Field, CA 94035(USA)

Paloski, W.H., C.M. Oman, J.J. Bloomberg, M.F. Reschke, S.J. Wood, D.L. Harm, B.T. Peters, A.P. Mulavara, J.P.Locke, and L.S. Stone. Risk of sensory-motor performance failures affecting vehicle control during space missions:a review of the evidence. J. Grav. Physiol. 15(2):1-29, 2008. – NASA’s Human Research Program (HRP) has identifieda number of potentially significant biomedical risks that might limit the agency’s plans for future space exploration,including missions back to the Moon and on to Mars. Among these risks is the: “Risk of Impaired Ability to MaintainControl of Vehicles and Other Complex Systems.” We examine the various dimensions of this risk by reviewing theresearch and operational evidence demonstrating sensory-motor performance decrements during space flight thatmight affect vehicle and complex system control, including decreased visual acuity, eye-hand coordination, spatialand geographic orientation perception, and cognitive function. Furthermore, we evaluate this evidence to identifythe current knowledge gaps that must be filled through further research and/or data mining efforts before the riskcan be fully mitigated. We conclude that the true operational risks associated with the impacts of adaptive sensory-motor changes on crew abilities to control vehicles and other complex systems will only be estimable after the gapshave been filled and we have been able to accurately assess integrated performance in off-nominal operational set-tings.

Key words: Vestibular, Visual, Spatial disorientation, Eye-hand coordination, Gravito-inertial force

INTRODUCTION

NASA’s Human Research Program (HRP) hasidentified a number of potentially significant bio-medical risks that might limit to the agency’s plansfor future space exploration, which include missionsback to the Moon and on to Mars. Among them is the:“Risk of Impaired Ability to Maintain Control of Vehiclesand Other Complex Systems,” which is described as fol-lows: “Space flight alters sensory-motor function, asdemonstrated by documented changes in balance, locomo-tion, gaze control, dynamic visual acuity, eye-hand coordi-nation, and perception. These alterations in sensory-motorfunction affect fundamental skills required for piloting andlanding airplanes and space vehicles, driving automobiles

and rovers, and operating remote manipulators and othercomplex systems. However, relationships between thephysiological changes and real-time operational perform-ance decrements have not yet been established, owing toboth the inaccessibility of operational performance data andthe presence of confounding, non-physiological factors inmost known instances of significant operational perform-ance decrement. While space flight induced alterations insensory-motor performance are of concern for upcominglunar missions, they are of greater concern for Mars mis-sions due to the prolonged microgravity exposure duringtransit, which will more profoundly affect landing task per-formance and subsequent operation of complex surface sys-tems.”

Control of vehicles and other complex systems isa high-level integrative function of the central nerv-ous system (CNS). It requires well-functioning sub-system performance, including good visual acuity,eye-hand coordination, spatial and geographic orien-tation perception, and cognitive function. Evidencefrom space flight research demonstrates that the func-tion of each of these subsystems is altered by remov-ing gravity, a fundamental orientation reference,

Address for correspondence:William H. Paloski, Ph.D. Department of Health and Human Performance3855 Holman St. Garrison Room 104Houston, TX, 77204-6015Email: [email protected]

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SENSORY-MOTOR PERFORMANCE RISKS DURING SPACE FLIGHT

which is sensed by vestibular, proprioceptive, andhaptic receptors and used by the CNS for spatial ori-entation, navigation, and coordination of movements.The available evidence also shows that the degree ofalteration of each subsystem depends on a number ofcrew- and mission-related factors.

There is only limited operational evidence thatthese alterations cause functional impacts on mission-critical vehicle (or complex system) control capabili-ties. Furthermore, while much of the operationalperformance data collected during space flight hasnot been available for independent analysis, thosethat have been reviewed are somewhat equivocalowing to uncontrolled (and/or unmeasured) envi-ronmental and/or engineering factors. Whether thiscan be improved by further analysis of previouslyinaccessible operational data or by development ofnew operational research protocols remains to beseen. The true operational risks will be estimable onlyafter we have filled the knowledge gaps and when wecan accurately assess integrated performance in off-nominal operational settings.

Thus, our current understanding of the Risk ofImpaired Ability to Maintain Control of Vehicles andOther Complex Systems is limited primarily to extrap-olation of scientific research findings, and, since thereare no robust ground-based analogs of the sensory-motor changes associated with space flight, observa-tion of their functional impacts is limited to studiesperformed in the space flight environment.Fortunately, many sensory-motor experiments havebeen performed during and/or after space flight mis-sions since 1959 (150). While not all of these experi-ments were directly relevant to the question ofvehicle/complex system control, most provideinsight into changes in aspects of sensory-motor con-trol that might bear on the physiological subsystemsunderlying this high-level integrated function.

I. EVIDENCE

A. Space Flight Evidence

To our knowledge, no relevant, randomized, con-trolled, human flight research investigations havebeen performed. Thus, this section begins with asummary of evidence obtained form observations ofcrew performance decrements during operational sit-uations. While largely circumstantial and clearlymulti-factorial (likely resulting from a combination ofphysiological, behavioral, environmental, and engi-neering factors), this evidence provides a basis forconcerns regarding the operational impacts of senso-ry-motor adaptation to space flight, as well as justifi-cation for continued investigation into the relative

roles of the various factors affecting crew perform-ance. Following the operational evidence section,summaries of evidence are provided in separate sec-tions for each of four physiological sub-issues relatedto the subject risk (oculomotor control, eye-handcoordination, spatial disorientation, and cognition).Within each section, the levels of evidence should beclear from context and/or references. Where neces-sary supporting studies from space flight analogenvironments (e.g., parabolic flight), space flight ana-log populations (e.g., vestibular deficient patients), orother critically relevant ground-based investigationsare included.

1. Evidence Obtained from Space Flight Operations

An accurate assessment of the risks posed by theimpacts of physiological and psychological adapta-tions to space flight on control of vehicles and othercomplex systems must account for the potentially off-setting influences of training/recency and engineer-ing aids to task performance. Thus, it behooves us toreview performance data obtained from space flightcrews engaged in true mission operations. Evidenceof operational performance decrements during spaceflight missions has been obtained from severalsources; however, to our knowledge no well-designed scientific studies have been performed oncritical operational task performance, so interpreta-tion is frequently confounded by small numbers ofobservations, inconsistent data collection techniques,and/or uncontrolled engineering and environmentalfactors. Much of the relevant, extant operational datahas been previously inaccessible to (or uninter-pretable by) life sciences researchers. Recent pro-grammatic changes have putatively improved accessto both data and experts to help with interpretation,though, so a major near-term goal is to mine theseoperational data to better assess what we alreadyknow about the risk.

Crew Verbal Reports A number of (unpublished)crew verbal reports were obtained early after flight bysome of the authors of this paper. While difficult tocombine, owing at least in part to the lack of stan-dardized questions and structured interview tech-niques, these reports are informative in that theyprovide insight into the individual crewmember per-ceptions. As an example, the following transcript(obtained by Dr. Reschke) captures impressions froma Shuttle commander obtained immediately (<4 hrs)after flight. The discussion focused on target acquisi-tion tasks the commander performed for Dr. Reschkeduring the flight and his difficulties with nausea, dis-orientation, posture, locomotion, etc. after the flight

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(italicized text indicates the crewmember’s responsesto the Dr. Reschke’s questions).

Did you try to limit your head movements? Ohyes, definitely. When you were trying to acquire thetargets only, ...did you notice any difficulty in spot-ting the targets? Oh yeah, oh yeah. Did it seem asthough the target was moving or was it you? I felt thatit was me. I just couldn’t get my head to stop when I want-ed it to. So it was a head control problem? Yeah, yeah inaddition to the discomfort problem it caused. So when youfirst got out of your seat today, can you describe whatthat felt like? Oh gosh, I felt so heavy, and, uh, if I evengot slightly off axis, you know leaned to the right or to theleft like this, I felt like everything was starting to tumble.When you came down the stairs did you feel unsta-ble? Oh yeah, I had somebody hold onto my arm. Did youfeel like your legs had muscle weakness, or … was itmainly in your head? It was mainly in my head.

Every crewmember interviewed by one of us onlanding day (>200 crewmembers to date) has report-ed some degree of disorientation/perceptual illusion,often accompanied by nausea (or other symptoms ofmotion sickness), and frequently accompanied bymalcoordination, particularly during locomotion. Ofparticular relevance to the ability to perform landingtasks, common tilt-translation illusions (see below)include an overestimation of tilt magnitude or mis-perception of the type of motion. Most also reportedhaving experienced similar symptoms early in flight;however, except in the most severely affected, thereseems to be no correlation between the severity of thesymptoms following ascent and those followingdescent. The severity and persistence of postflightsymptoms varies widely among crewmembers, butboth tend to decrease with increasing numbers ofspace flight missions. However, both severity andpersistence increase with mission duration.Symptoms generally subsided within hours to daysfollowing 1-2 week Shuttle missions but persisted fora week or more following 3-6 month Mir Station andISS missions. The degree to which these psychophys-ical effects might affect piloting skills is difficult tojudge, as recent, intensive training may have offsetany impact on Shuttle landings, especially undernominal engineering and environmental conditions,and long duration Mir and ISS crewmembers to datehave only piloted ballistic entry spacecraft, whichparachute in, allowing no human control inputs dur-ing the last 15 min before landing.

Shuttle Entry and Landing Spatial DisorientationDespite recent, intensive training for all Shuttle com-manders and pilots, some Shuttle landings were out-side of the desired performance specifications,perhaps, in part, because of spatial disorientation.

Shuttle entry and landing spatial disorientation (SD)differs from aviation SD (see below), at least in termsof prevalence. Most instrument rated aircraft pilotshave experienced SD, but episodes occur relativelyinfrequently in ordinary flying. In contrast, stimulicapable of producing SD are present during everyShuttle landing. At issue is whether the astronautcommander can successfully fly through the SD. Tilt-translation illusions (see below) do not occur in astro-nauts practicing approaches in the Shuttle TrainingAircraft (STA), so their first actual experiences withthese illusions occur during their first actual returnfrom space. Crews are forewarned about them, but sofar we do not know how to predict the direction andmagnitude of the effect, so a first-time flier cannotknow in advance which way to compensate. This isgenerally handled operationally by requiring com-manders to have previous space flight experience (aspilots). Fortunately, on the 120+ Shuttle flights todate, there have been no accidents specifically attrib-uted to SD. However, several lines of circumstantialevidence suggest that the margin for error may be lessthan generally recognized.

Shuttle landings, to date, have all been successful,but landing performance has been more variable thandesired. The timing and shape of the commander’scontrol input during the flare depends critically oncorrect perception of speed, altitude, attitude, andsink rate. The flare maneuver, in turn, determines thereadily measurable landing performance metrics,such as touchdown sink rate, speed, and distance. Ofall the landings between STS-1 and STS-108, theShuttle crossed the runway threshold abnormally low20 times. Seven landings touched down abnormallylong or short, and 13 had high touchdown sink rates,with three exceeding the 5 ft/sec structural limit.Moore et al. (118) recently reported that touchdownspeeds during the first 100 Shuttle landings variedwidely, with 20% outside of acceptable limits and sixequaling or exceeding the maximum speed of 217knots/hr (main landing gear tires are rated at 225knots/hr maximum speed). They also note that thefastest landing on record (224 knots/hr) was linked tothe commander’s momentary spatial disorientation(32), as was the second fastest (220 knots/hr).Normally, commanders perform better than thiswhen flying the STA and the flight simulators. A dif-ferent analysis of Shuttle landing compared pilotingperformances in terms of sink rate at touchdown. Fig.1 shows preflight performances flying the STA andsubsequent postflight performances in the Shuttle bycommanders of all missions from STS-43 to STS-108.The average STA and STS touchdown sink rates weresimilar, and almost all STA touchdown sink rates fellin the desirable range; however, the STS touchdown

sink rate distribution exhibits greater variability, withmore than 10% exceeding the desired sink rate attouchdown.

Of particular note was the landing of the eight-day STS-3 mission in 1982. The commander, who wasflying visually, took over manual control of the vehi-cle 30 seconds before landing at White Sands, NM.The vehicle was decelerating at 0.25 g. Starting atflare, when the commander attempted to lower thenose of the Shuttle, the vehicle exhibited a pilotinduced oscillation (PIO) of three full cycles withincreasing amplitude that continued through touch-down. Post-flight analysis showed no engineeringanomaly in the flight control system. The command-er was a highly experienced test pilot, very familiarwith conventional PIO and with the 0.25g decelera-tion of landing. However, it is possible that he under-perceived his pitch attitude because of tilt-translationambiguities and caused the PIO by making largercontrol stick movements than necessary to compen-sate for the misperception. This could have been fur-ther exacerbated by inappropriate manual controlinputs to the stick caused by miscalibration of eye-hand coordination. In a recent interview, however,the commander denied having any issue with PIO, ormisinterpreting pitch attitude. His recollection wasthat the nose came down earlier than expected as theShuttle began to slow down. He said the stick was notresponsive when he first attempted to pitch the nose

back up, but then it seemed to over-respond andpitched up more than he expected. Because he wasthen concerned about a potential problem with thestick, he brought the nose down and left it down. Thecommander’s recollection appears to be consistentwith the landing video, but not with data from thecontrol stick that showed five large amplitude rever-sals in the pitch plane command after main geartouchdown. While difficult to reconstruct so longafter the event, this may be noteworthy as an unrec-ognized case of spatial disorientation in a highlyexperienced pilot.

Increasing pilot awareness of the PIO problem,modifying software to reduce control authority auto-matically when oscillatory control outputs are detect-ed, adding a heads-up display (HUD) pitch attituderead-out, and restricting landings to low cross-windand good visibility conditions have so far preventedPIO recurrence. However, it is clear that control phaseand gain margins during the landing maneuver areroutinely near limits of stability, and that pilots mak-ing their first Shuttle landing must overcome disori-enting perceptions not encountered during preflighttraining in the STA.

Flight surgeons now examine every returningShuttle crewmember for evidence of neurologicaldysfunction within several hours of landing.Crewmembers are scored for subjective symptoms,coordination, and functional motor performance.McCluskey et al. (102) analyzed data from nine mis-sions, and noted trends, such as a correlation betweentouchdown sink rate and postflight difficulty per-forming a sit-to-stand maneuver without using thearms. Scores indicating neuro-vestibular dysfunctiongenerally correlated with poorer flying performances,including a lower approach and landing shorter,faster, and harder.

These observations suggest that further analysisof Shuttle landing performance is required. Wherepossible, objective landing performance data shouldbe compared directly with objective sensory-motorphysiological data to determine what associationsexist between landing performance and physiologicaladaptation.

Apollo Lunar Landing Spatial Disorientation TheApollo Lunar Module (LM) had a digital autopilotthat on later missions was capable of fully automaticlandings. While the Apollo crews used the autopilotthrough most of the descent, all elected to fly thelanding phase manually, using angular rate and lin-ear velocity control sticks to adjust the vehicle trajec-tory while visually selecting the landing point.Landing sites and times were chosen so that the sunangle provided good visibility, but the crews had



Figure 1. Cumulative distribution functions allowing compar-ison between landing performances (vertical velocity at touch-down) before flight in the Shuttle Training Aircraft (STA) andthose at the end of mission in the Space Shuttle (STS).

Vertical Velocity at TouchdownSTS Landing versus STA

Cum

Dis

t Fx

1

0.9

0.8

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0-7 -6 -5 -4 -3 -2 -1 0

STS 43 - 108––– STS––– STA*

* Note: STA data from same CDRs within 1 month of launch

> -5 fpsacceptablee

> -3.5 fpsdesired


problems recognizing landmarks and estimating dis-tances because of ambiguities in the size of terrainfeatures. The vehicles had no electronic map or land-ing profile displays. The commander flew visually,designating the landing spot using a window reticle,while the second astronaut verbally annunciatedvehicle states and status. Unfortunately, the landingarea was generally not visible to the crew until theLM pitched to nearly upright at an altitude of about7000 feet and distance of about 5 miles from touch-down with only 1-2 minutes of fuel remaining.Spatial disorientation was a concern during landingbecause visibility was reduced by the window design(views downward and to the right were blocked) andby lunar dust blowback that impaired surface andattitude visibility. For example, the Apollo 11 and 12crews reported difficulty in nulling horizontal ratesduring landing because of blowing dust, and theApollo 12 and 15 crews reported virtually no outsidevisibility in the final moments of landing. Visibilitywas improved in later missions by new hoveringmaneuvering procedures that reduced blowing dust.

Horizontal linear accelerations could not beavoided during the gradual descent to the landingzone or during hover maneuvers just before touch-down. Since lunar gravity is only 1/6 that on Earth,lunar landers had to pitch or roll through angles sixtimes larger than on Earth to achieve a given hori-zontal acceleration using the engine thrust vector. Thedirectional changes in gravito-inertial force these tiltscreated would have been larger than those on Earth,arguably making tilt-translation ambiguity illusionsmore likely. The Apollo crews trained for their mis-sions in a 1/6 g Lunar Landing Training Vehicle,which did not simulate the vestibular effects of 1/6 g.Prior to their missions the only 1/6 g vestibular stim-ulation they received was during limited parabolicflight training. With the world watching, the Apollocrews did not acknowledge any spatial disorientationevents during landing. They did later admit feeling alittle “wobbly” when they emerged to walk onto thelunar surface, but reported that coordinationimproved steadily during first few hours of lunarambulation.

Apollo Landing Geographic Disorientation TheApollo LM utilized inertial navigation, updated byoccasional star sights, radar orbital data from Earth,and radar altimetry during descent. Nonetheless,there was uncertainty in the accuracy of their com-puted position as they descended into the landingzone. Since crews could not look straight down, thefinal approach trajectory to the landing area had touse low angles (16-25˚) so crew could see ahead.Mission planners only knew the landing zone terrain

to 10 m resolution, so the crews had to confirm visu-ally the LM trajectory and then sight the computer’santicipated touchdown point using a front windowreticle. Given the fractal nature of lunar craters, iden-tification of surface features was challenging.Humans interpret surface shape from shading basedon a “light comes from above” assumption. This cancreate a “Moon crater” illusion (146) in which distantconcave features, such as lunar craters, can be per-ceived as convex objects, such as hills, when viewedlooking “down sun.” The crews had to choose a suit-ably flat landing area, as judged by surface albedoand the absence of shadows indicating small cratersor fissures. Landings were planned with sun eleva-tions of 5-23˚, so shadows were of moderate length,and with the crew facing down sun at a slight angle,so that shadows would be visible. The human eye canresolve 1.5 ft detail at a distance of about 4000 ft. Asmore surface details became visible, the commandertypically redesignated the landing point (often sever-al times), and eventually took over and flew manual-ly, usually to a point somewhat beyond the finalcomputer redesignated spot. He judged horizontalvelocity looking out the window or using a cockpitDoppler radar display, and he used the LM shadowas a gauge, while listening to callouts of altitude, alti-tude rate, horizontal velocities, and fuel status. Sincesurface slope is impossible to judge visually lookingstraight down, the commander chose the final land-ing spot looking horizontally, and then flew over itand began final descent. At 50-100 feet, dust oftenobscured the outside view, and the vertical descent totouchdown sometimes had to be made relying pri-marily on instruments. The descent engine was cutoff just before touchdown, to avoid explosion or dam-age should it contact the surface. The landing geardesign assumed a maximum surface elevation differ-ence of two feet within the landing gear footprint,and a maximum 12˚ terrain slope (157). Finding a flatlanding spot was highly desirable, since vehicle tiltson the surface complicated surface operations andsubsequent takeoff.

All six Apollo landings were ultimately success-ful. However, the Apollo 15 crew experienced geo-graphic disorientation. When they pitched over, theycould not identify the craters they were expecting,and the commander had to choose a landing spot inan unplanned area. Maintaining full awareness of theterrain immediately beneath the lander was usuallyimpossible during the final phase of landing, and inone case the LM engine was damaged on touchdown(82, 113). The Apollo 12 commander encounteredheavy dust blowback and said, “I couldn’t tell whatwas underneath me. I knew it was a generally good areaand I was just going to have to bite the bullet and land,

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because I couldn’t tell whether there was a crater downthere or not.” He later added, “It turned out there weremore craters there than we realized, either because we did-n’t look before the dust started or because the dust obscuredthem.” The following mission, Apollo 14, landed safe-ly, but on a seven-degree slope. Apollo 15 experi-enced severe dust blowback that contributed tomaking the hardest landing of the program (6.8ft/sec), with the vehicle straddling the rim of a 5 ftdeep crater, buckling the bell of the descent engine,and causing an 8˚vehicle tilt. Apollo 16 and 17 experi-enced less dust obscuration and landed closer tolevel.

It seems likely that similar problems will beencountered when crews once again begin landingvehicles on the lunar surface. Improved navigationaids could help to avoid geographic disorientation,and increased reliance on auto-land capabilities couldhelp maintain the landing performance within equip-ment specifications. However, improved trainingtechniques, including realistic simulation of visual-vestibular inputs, will likely be required should com-manders choose to use manual landing modes. Thechallenge of manual landing is likely to be muchgreater for Mars landings, owing primarily to theincreased transit time in microgravity. A combinationof more profound adaptation to microgravity anddecreased training recency will likely increase sub-stantially the risks associated with manual landing onMars. [Note that using continuous artificial gravity,created by rotating all or part of the vehicle duringtransit, might well mitigate this risk (as well as manyof the other biomedical risks), but the impact of pro-longed exposure to a rotating environment on pilot-ing a spacecraft would need to be investigated beforecommitting to such a solution.]

Rendezvous and Docking A top priority in the U.S.space program is assuring crew and vehicle safety.This priority gained significant focus in June 1997 fol-lowing the collision of the Progress 234 resupply shipwith the Mir space station during a manual dockingpractice session. There were two separate attempts todock the Progress with the Mir that day. In the firstattempt, docking was aborted after the radar used forrange calculations apparently interfered with a cam-era view of the Progress. In the second, near fatalattempt, mission managers decided to turn the radaroff and leave the camera on. For this arrangement towork the Mir commander asked his two crewmates tolook for the Progress approach through a porthole,and once sighted, to provide range information withhandheld range instruments. Trouble began whenneither the camera view nor the visual spotters couldlocate the Progress as it closed on the station. When

spotters moved between modules to obtain a betterview, they lost their frame of reference, and wereuncertain which direction to look. Once spotted, theProgress’ speed was above an acceptable rate, and itwas very close to the Mir. Braking rockets on theProgress, fired by the Mir commander, failed to slowthe velocity of the approaching spacecraft. No rangeinformation or other position data were available toassist the commander. To complicate matters, one ofthe other crewmembers may have bumped into thecommander as he attempted to make last secondinputs to the approaching Progress via joystick. Theresulting collision tore a portion of the solar panel onthe Mir, punched a hole in the Spektr module, andcaused a decompression of the station.

Loss of situational awareness, spatial disorienta-tion, and sensory-motor problems, including difficul-ties with vision, head-hand-eye coordination, and aninability to judge distance and velocity with limitedfeedback likely contributed to this outcome. Targetacquisition studies have shown dramatic changes inthe speed at which target visualization can beachieved, delaying response time by as much as a1000 msec. Eye-hand response could take as long asanother full second. A delay of two seconds is a life-time when a spacecraft is closing, and not respondingto joystick commands intended to decrease forwardvelocity. Members of the Russian Institute ofBiomedical Problems (IBMP) believe that the collisionbetween Mir and Progress was caused by poor situa-tional awareness, spatial disorientation, and sensory-motor problems (I.B. Kozlovskaya, personalcommunication). After the fact, Ellis (48) performed arigorous, quantitative analysis of the available visualand non-visual information and suggested a numberof potential sensory-motor and cognitive/psy-chophysical contributions to the crash. To avoidhuman factors contributions to future crashes suchrigorous analyses should be performed well beforeattempting any three-dimensional visual-motor con-trol task.

Teleoperator Tasks The ISS teleoperation system hasbeen heavily used in ISS construction, and it will con-tinue to be used to support EVA operations, as well asin grappling/docking of rendezvousing cargo vehi-cles. Training and operating the Shuttle and ISS tele-robotic manipulator systems as well as teleroboticallycontrolled surface rovers presents significant sensory-motor challenges (40, 91, 106). These systems are usu-ally controlled using separate rotational andtranslational hand controllers, requiring bimanualcoordination skills and the ability to plan trajectoriesand control the arm in some combination of end-effector or world reference frames. The abilities to




visualize and anticipate the three-dimensional posi-tion, motion, clearance, and mechanical singularitiesof the arm and moving base are critical. Thus, opera-tors must have the cognitive abilities to integratevisual spatial information from several different ref-erence frames. Often the video cameras are not ideal-ly placed, and in some situations (e.g. ISS operations)the views may actually be inverted with respect toone another, so cognitive mental rotation and per-spective taking skills are also important (91, 106).Teleoperation is sufficiently difficult that several hun-dred hours of training are required to qualify, and alloperations are monitored by a second qualified oper-ator, backed up by a team of trainers and engineers onthe ground. Recency is important, so ISS astronautsperform on-orbit refresher training. Despite all thetraining and precautions, however, there have beenfour-five significant ISS teleoperation incidents (e.g.,collisions with a payload bay door, significant viola-tions, or close calls) over the course of the first 16 ISSincrements (185). Procedures are updated after eachincident, but there are generic common factors relat-ing to spatial visualization skills, misperception ofcamera views, timeline pressures, and fatigue.

Driving Performance Driving a vehicle is one ofthe most complex sensory-motor/cognitive tasksattempted by most humans, and driving performanceis known to be impaired in vestibular patients (38).Page & Gresty (131) reported that vestibular patientsexperience difficulty in driving cars, primarily onopen, featureless roads or when cresting hills, andMacDougal & Moore (97) reported that the verticalvestibulo-ocular reflex contributes significantly tomaintaining dynamic visual acuity while driving.Adaptive changes in sensory-motor function duringspace flight can compromise a crewmember’s abilityto optimize multi-sensory integration, leading to per-ceptual illusions that further compromise the abilityto drive under challenging conditions. During theJune 2006 Apollo Medical Operations Summit inHouston, TX, Apollo crewmembers reported thatrover operations posed the greatest risk for injuryamong lunar surface EVA activities. During roveroperations, crewmembers often misperceived theangles of sloped terrain, and the bouncing fromcraters at times caused a feeling of nearly overturningwhile traveling cross-slope, causing the crewmem-bers to reduce their rover speed as a result (Apollo 15report). This is not surprising given the evidence oftilt-translation disturbances following G-transitions,as incorrect perceptions of vehicle accelerations, tiltedterrain, and uneven (bumpy) surfaces may causeinappropriate responsive actions. While automaticcontrol systems can compensate for some deficiencies

in performance, lessons learned from the Apollo mis-sions (113) suggest that manual takeover is requiredas a minimum safe guard, and therefore countermea-sures must concentrate on mitigating risks associatedwith crewmembers in the control loop for rover oper-ations.

Implications for CEV Design There are specific spa-tial disorientation issues to address with the crewexploration vehicle (CEV) currently being designedfor lunar missions. As a capsule, CEV will differ fromthe Shuttle in opportunities to induce disorientation.In the CEV, crews will stow their seats after ascent, sothere will be no up/down cues except for the cockpitpanels and the windows. CEV, like Shuttle, will prob-ably be manually docked when crewed, while thelogistics (cargo) version may have auto-docking. Thecrew’s ability to remain visually oriented with ISSduring proximity operations is a concern (S.Robinson, CEV Cockpit Team, personal communica-tion). The developers must undertake analyses toensure that the integrated visual out-the-window,camera imagery, display information, and sensor datawill be sufficient to perform the envisioned three-dimensional docking tasks reliably.

2. EVIDENCE OBTAINED FROM SPACE FLIGHTSCIENTIFIC INVESTIGATIONS

Studies Demonstrating Decrements in VisualPerformance

High visual acuity is critical to performing pilot-ing tasks, and it is very important to controlling othervehicles (e.g., rovers and automobiles) and complexsystems (e.g., robotic arms and other remote manipu-lators). Rapidly locating and reading instrument dis-plays, identifying suitable landing locations, free ofcraters, rocks, etc., and tracking the motion of targetsand/or objects being manipulated are among thetasks requiring good vision enabled by optimized eyemovement control. A large body of evidence demon-strates that the G-transitions associated with spaceflight disrupt oculomotor performance. Highlightsare summarized in the following subsections.

Static Visual Acuity Space flight studies of staticvisual acuity, contrast sensitivity, phoria (relativedirections of the eyes during binocular fixation), eyedominance, flicker fusion frequency, and stereopsis(ability to perceive depth) have been performed todetermine whether space flight causes inherentchanges in ocular function that affect visual perform-ance (reviewed in Clément (37)). Except for contrastsensitivity, in-flight studies have revealed minimal

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changes in visual function (55, 168). However, in sub-jective clinical reports from 122 Shuttle crewmembersbetween 1995 and 1998, 15% indicated decrements innear vision acuity during flight (Longitudinal Studyof Astronaut Health). This decreased acuity likelyresults from fluid shifts or gravity-related changes inocular geometry (37), and it is generally overcome byusing magnifying spectacles and/or large font sizeson documents and displays.

Smooth Pursuit Eye Movements To see an objectclearly, the visual axis of the eye must be aligned toproject the object of interest onto the fovea, a smallregion, centrally located on the retina, containinghigh concentrations of rods and cones. To accomplishthis during voluntary visual tracking of moving tar-gets (e.g., a bird flying by) without head movements,the CNS oculomotor control system produces smoothpursuit eye movements. Reschke et al. (149, 154)reported that space flight disrupts smooth pursuiteye movements (Fig. 2). Testing 39 crewmembersfrom 20 separate Shuttle flights using a simple pointstimulus sinusoidal tracking task (0.33 Hz in eitherhorizontal or vertical planes), they found that, rela-tive to preflight values, eye movement amplitudeswere reduced and the number of corrective saccadeswas increased just after flight. The functional impactis that visual acuity would be degraded by this inabil-ity of the oculomotor control system to keep target ofinterest focused on the fovea (Fig. 3). In other studies,André-Deshays et al. (1) found no in-flight changes inhorizontal or vertical smooth pursuit tracking per-formance two Mir Station cosmonauts, but, Kornilovaet al. (87) found changes similar to those reported byReschke et al. (149) during other Mir station flights.Early in-flight they found that the eye movementamplitude responses to vertical pulsed movements of

a point stimulus decreased (undershot the target) andnumbers of corrective saccades increased relative topreflight values. They also reported performancedeterioration in pursuit tracking of a point stimulusmoving vertically or diagonally, with these effectsbeing most pronounced early in-flight (flight day 3),late in flight (flight days 50, 116, and 164), and earlyafter flight. Thus, it appears that during and earlyafter space flight the amplitude of smooth pursuit eyemovements is reduced, the saccadic system must beutilized extensively to maintain accurate target track-ing, and vision is degraded by an inability to main-tain the target focused on the fovea.

Vestibulo-Ocular Reflex (VOR) Function Duringhead and/or body movements, the gaze stabilizationsystem maintains high visual acuity by coordinatingmovement of the eyes and head so as to stabilize theimage of interest on the fovea. The vestibulo-ocularreflex (VOR), a servo system that uses head motionsignals sensed by the semicircular canals and otolithorgans to generate vision-stabilizing compensatoryeye movements, is critical to this function. Blurredvision, oscillopsia (illusory movement of the visualworld), and/or reduced dynamic visual acuity occurwhen this gaze compensation mechanism is disrupt-ed. Vestibulo-ocular reflex function is plastic, mean-ing it can adapt to different environmental stimuli(16). For example, the VOR gain (amount of eye rota-tion caused by a unit of head rotation) adapts whenindividuals begin wearing new prescription eyeglass-es. A number of relevant flight experiments havedemonstrated that various VOR response propertiesare modified during and after space flight, and thatthe degree of adaptation varies among subjects andexperimental conditions (reviewed Reschke et al.(154)). Some of these are summarized in the following

Figure 2. Smooth pursuit eye movements in the vertical planebefore and after space flight (154). The smooth sinusoidal linerepresents the target motion, while the other line representsthe eye movements. Note the presence of saccades after flightbut not before flight. Figure 3. Cumulative time foveation is off target during the

smooth pursuit-tracking task depicted in Figure 2.

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paragraphs.Several investigations were conducted to deter-

mine the effects of weightlessness on the VORresponses to horizontal angular (yaw) head motions.Early studies relied mainly on voluntary (active) headoscillations to stimulate the VOR at frequencies rang-ing from 0.25 to 1 Hz (13, 170, 173, 176, 180), but pas-sive rotational stimulation was sometimes employedbefore and after flight (13). These early studies detect-ed no significant in-flight or postflight changes inyaw VOR gain, or, when changes were observed (60),the direction of the changes varied among subjects.Later experiments associated with the D-1, SLS-1, andSLS-2 Spacelab missions utilized passive body move-ments provided by step changes in the angular veloc-ity of rotating chairs to stimulate the VOR. Duringparabolic flight, the persistence of the yaw VORresponse after the chair motion stopped wasdecreased in eight astronauts tested just before spaceflight (124, 130) and in normal subjects (44). However,after 4-10 days in orbital flight, the yaw VOR persist-ence was no different from preflight values in five ofthe eight astronauts tested, although active headpitch movements (“dumping”) did not interfere withthe VOR persistence, as it consistently did on Earth.Early after flight (1-2 days), the persistence wasdecreased relative to preflight in nine of 12 astronautstested, but it eventually returned to preflight valuesin all (124, 126, 130). These findings suggest that tran-sitions to and from weightlessness temporarilyreduce the contribution of brainstem mechanismsthat normally extend the low frequency bandwidth ofthe human angular VOR response.

Unlike yaw plane head movements, pitch androll plane head movements in normal gravity changethe orientation of the head relative to the gravity vec-tor, thereby modulating gravitational stimulation ofthe otolith organs. One might expect, therefore, thatthe pitch and roll plane VOR would be more affectedby space flight than the yaw plane VOR. The pitchVOR response to voluntary head oscillations has beenmeasured during and after space flight at frequenciescomparable to those described above for yaw. WhileWatt et al. (180) reported no changes in pitch VORduring or after flight, others have reported changes.For example, Berthoz et al. (15) found that the VORgain in subjects exposed to 1 Hz pitch head oscilla-tions was significantly increased 14 hrs after landingwhen compared with late in-flight (flight day 5 and 7)and sub sequent postflight measurements. They alsoreported an in creased phase lag (delay between headmotion and elicited eye motion) during the in-flighttests. However, the change in gain and phase rela -tionship was not significant due to a high dispersionof the data. In a separate study, Viéville et al. (176)reported a decrease in vertical VOR gain for 0.25 Hzvoluntary pitch oscillations in a subject tested on STS-51G. In another series of experiments examining cos-monauts returning from space flight, Clarke et al. (34,35) reported decreased vertical VOR gains for headoscillations ranging from 0.12 Hz to 2.0 Hz, and areversal of the normal asymmetry of vertical VORgain, with greater gains during downward headmovements than during upward movements. Theyalso reported changes in torsional VOR during vol-untary head movements in the roll plane during and

Figure 4. Head (H), eye (E), and gaze (G) movements during target acquisition beyond the effective oculomotor range before (leftpanel) and after (right panel) flight.

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after space flight. These findings further demonstratethat VOR is disrupted early after insertion into orbitand again following the return to Earth. Fortunately,central adaptive processes re-establish VOR responseproperties over time in the new environment, result-ing in recovery of accurate stabilization of vision dur-ing head and/or body movements in the newenvironment. However, critical mission activitiesrequiring accurate gaze stabilization during headmovements (e.g., piloting/landing a spacecraft) willlikely be performed less skillfully during or soon afterG-transitions.

Eye-Head Coordination and Target Acquisition Gazeis the direction of the visual axis in three-dimension-al space. It is defined as the sum of eye position withrespect to the head and head position with respect tospace. Acquisition of new visual targets of interest isgenerally accomplished using coordinated eye-headmovements consisting of a saccadic eye movementthat shifts gaze onto the target combined with a VORresponse that maintains the target on the fovea as thehead moves to its final position. Space flight modifieseye-head coordination during target acquisition (88,171) and ocular saccadic performance (1, 149, 154,175). Reschke et al. (149) also showed that perform-ance of target acquisition tasks requiring coordinatedeye-head movements is degraded during and afterspace flight, particularly for targets placed outsidethe central field-of-view in the vertical plane, requir-ing pitch head movements for target acquisition (Fig.4). Grigoryan et al. (61) showed that changes in theseparameters after flight contributed to a near doublingof the latency required to fixate peripheral targets.Also, Sirota et al. (166) showed that during adaptationto space, non-human primates trained to perform avisual target acquisition task requiring accurate per-ception of peripheral targets showed delays in theonset of the gaze response and made significantlymore errors in identifying the visual characteristics ofthe peripheral targets.

Dynamic Visual Acuity Oculomotor (gaze) controlorchestrated by the CNS is critical to dynamic visualacuity, the ability to see an object clearly when theobject, the observer, or both are moving. Deficientgaze control experienced following G-transitionscause oscillopsia, or blurred vision, and decrementsin dynamic visual acuity, with stationary objectsappearing to bounce up and down or move back andforth during head movements. Decreased dynamicvisual acuity caused by space flight can lead to mis-perception of sensory information and poses a uniqueset of problems for crewmembers, especially duringentry, approach, and landing on planetary surfaces.

Visual disturbances could adversely affect entry andlanding task performance, such as reading instru-ments, locating switches on a control panel, or evacu-ating a vehicle in suboptimal visual conditions (e.g.,smoke in the cabin). Postflight oscillopsia anddecreased dynamic visual acuity could decreasecrewmember safety when returning to normal duties(e.g., driving a rover, scuba diving, or piloting an air-craft) or activities of daily living (e.g., driving, contactsports, climbing ladders, etc.) after flight.

Under certain conditions, even persons withhealthy vestibular function can experience compro-mised visual performance. Human factors (i.e.ergonomics) investigations looking at the effects ofwhole-body vibration have documented changes invisual performance over a wide range of stimulusconditions (26, 59, 105, 119). An important factor fordetermining the visual performance in these investi-gations is the transmissibility of the vibration to thehead. Factors such as the subject’s posture and mus-cle tone, as well as their coupling to contact surfacesor added masses, can have an effect on visual per-formance. The coupling between astronauts and theirspacecraft during critical phases of the mission (e.g.,entry, landing) could therefore affect their ability tosee clearly. McDonald et al. (103) discussed the impli-cations to gaze control of adaptive changes in muscu-loskeletal impedance and posture after space flight.Musculo-skeletal impedance is also affected by G-loading, which in turn affects vibration sensitivity; G-and vibration loading often occur together duringlaunch and entry/landing. Visual performance maywell be degraded while standing during piloting, asproposed for the currently planned lunar missionsand previously employed during the Apollo pro-gram. In a series of experiments on returningcrewmembers, Bloomberg and colleagues have docu-mented decrements in dynamic visual acuity (DVA)while walking immediately after space flight. First, ina ground-based study, they demonstrated that DVA(assessed by having subjects read numbers of differ-ent font size while walking on a treadmill) was effec-tive at identifying differences in visual performancebetween labyrinthine deficient patients (patients withvestibular system abnormalities) and a group of nor-mative control subjects (72). The same paradigm wasthen used to demonstrate decreased DVA perform-ance in astronaut subjects following return from long-duration space flight (17). More recently, asecond-generation test (using Landolt C charactersinstead of numbers) was used to document decre-ments in DVA performance as a function of time afterflight in 14 crewmembers returning from long-dura-tion space missions (139). Acuity assessments weremade both while standing still and while walking at


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6.4 km/h on a motorized treadmill to produce bodyself-motion. The difference between the walking andstanding acuity measures provided a metric of thechange in the subject’s ability to maintain gaze fixa-tion on the visual target while walking. Postflight(one day after landing) changes in gaze control pro-duced decreases in dynamic visual acuity duringwalking. For some subjects the decrement wasgreater than the mean acuity decrement seen in apopulation of vestibular impaired patients collectedusing a similar protocol. The population meanshowed a consistent improvement in DVA perform-ance during the two-week postflight recovery period.These data probably underestimate the DVA decre-ments experienced by crews during and immediatelyafter landing.

Changes in dynamic visual acuity also contributeto functional changes (on the ground) in patients withvestibular disorders (71). For various reasons, physi-cians often caution patients with vestibular disordersagainst driving (38). One such patient, referred to arehabilitation program, specifically identified aninability to stabilize visually the car’s instrumentpanel as a reason for self-limiting driving (H. Cohen,personal communication). Clark & Rupert (33) reporton a case study involving a student naval aviatorwith a similar complaint. Turbulence caused the avi-ator to become unable to see the instrument panelclearly. Testing revealed that the student had defec-tive vestibulo-ocular reflex (VOR) function. As aresult, his eye movements were not able to compen-sate adequately for the motions of his body in turbu-lent conditions.

No decrements in visual acuity should be expect-ed under conditions where a non-moving person isvisually fixating a stationary target (see Static VisualAcuity above). However, vestibular impairment canrestrict a person’s ability to make the appropriate eyemovements that are necessary to compensate formovements of the head. Inappropriate or inadequateocular compensation results in an inability to stabilizethe visual image on the retina. It has been shown thatfor values above 2°/sec, increases in retinal slip veloc-ity are accompanied by decreasing visual acuity (43).This relationship between ocular compensation andacuity has led to attempts to use measures of dynam-ic visual acuity (DVA) as a diagnostic tool for identi-fying vestibular dysfunction (92, 163, 164, 174). Inthese studies, subjects’ visual acuity was assessedduring periods of self-motion. Regardless of whetherthe self-motion was generated by voluntary headrotations or passive whole-body rotations, the resultsindicated that DVA was capable of differentiatingbetween the control subjects and the patients knownto have vestibular deficits.

Studies Demonstrating Decrements in Eye-HandCoordination Performance

Eye-hand coordination skills are also criticallyimportant to performing piloting tasks and control-ling other vehicles and complex systems. Reaching toswitches on instrument panels, smoothly guiding thetrajectory of a flight- or ground-based vehicle, andcarefully positioning the end-effector of a robotic armare some of the tasks requiring high levels of eye-hand coordination. While not studied as intensivelyas oculomotor performance, a number of studies ofeye-hand coordination have been performed duringspace flight missions. The following subsections sum-marize some of the key evidence supporting eye-hand control performance decrements associatedwith space flight.

Control of Aimed Arm Movements When astronautsfirst encounter an altered gravity environment, armmovements are often inappropriate and inaccurate(52, 81, 120). During the Neurolab Space Shuttle mis-sion (STS-90), Bock and co-investigators (20) per-formed an experiment in which subjects pointed,without seeing their hands, to targets located at fixeddistances but varying directions from a commonstarting point. Using a video-based technique tomeasure finger position they found that the meanresponse amplitude was not significantly changedduring flight, but that movement variability, reactiontime, and duration were all significantly increased.After landing, they found a significant increase inmean response amplitude during the first postflightsession, but no change in variability or timing com-pared with preflight values. In separate experiments,Watt (180, 181) reported reduced accuracy duringspace flight when subjects pointed to memorized tar-gets. This effect was much greater when the handcould not be seen before each pointing trial. Whensubjects pointed at memorized locations with eyesclosed, the variability of their responses was substan-tially higher during space flight than during controlsessions on Earth. In other studies (14, 136), the inves-tigators found that when crewmembers on the Mirstation pointed to targets with eyes open, variabilityand mean response amplitude remained normal, butthe movement duration increased by 10 to 20% overthe course of the mission (flight day 2-162).

Reaching and Grasping Thornton & Rummel (172)showed that basic tasks such as reaching and grasp-ing were significantly impaired during the Skylabmissions. Later, Bock et al. (19, 21-24) investigatedpointing, grasping, and isometric responses during



brief episodes of changed gravity, produced by para-bolic flights or centrifugation. These experiments pro-vided converging evidence suggesting that duringeither reduced or increased gravity, the mean ampli-tude of responses is larger than in normal gravity,while response variability and duration remainsunchanged. During the Neurolab Space Shuttle mis-sion, Bock et al. (20) found that the accuracy duringflight of grasping luminous discs between theirthumb and index fingers was unchanged from pre-flight values, but task performance was slower.

Manual Tracking Changes in the ability ofcrewmembers to move their arms along prescribedtrajectories have also been studied in space. Forexample, Gurfinkel et al. (66) found no differences inorientation or overall shape when crew memberswith eyes closed drew imagined ellipses oriented par-allel or perpendicular to their long body axes. Inanother study, Lipshits et al. (94) examined the abilityof crewmembers to maintain a cursor in a stationaryposition in the presence of external disturbances.They found no performance decrements when thedisturbances were easily predictable. However, in fol-low-on experiment using more complex distur-bances, Manzey et al. (99, 100) found that trackingerrors were increased early in flight, but graduallynormalized within 2-3 weeks of exposure to the spaceenvironment. Later, Sangals et al. (162) reported aseries of step-tracking experiments conducted before,during, and after a three-week space flight mission toassess the effects of prolonged microgravity on a non-postural motor-control task. Task performance accu-racy was affected only marginally during and afterflight. However, kinematic analyses revealed a con-siderable change in the underlying movementdynamics: too-small force and, thus, too-low velocityin the first part of the movement was mainly com-pensated by lengthening the deceleration phase of theprimary movement, so that accuracy was regained atits end. They interpreted these observations as indi-cating an underestimation of mass during flight. Noreversals of the in-flight changes (negative afteref-fects) were found after flight. Instead, there was ageneral slowing down, which could have been due topostflight physical exhaustion. Bock et al. (20) report-ed data from another experiment during theNeurolab Space Shuttle mission, where subjectstracked with their unseen finger a target movingalong a circle at 0.5, 0.75, or 1.25 cycles/s. Subjects’response paths were found to be elliptical rather thancircular. They found that the variability of finger posi-tions about the best-fitting ellipse was significantlyhigher than preflight during the first in-flight session,and that responses lagged significantly behind the

target during the highest target speed condition.Performance normalized later during flight, butdeficits, albeit less pronounced, reappeared duringthe first two postflight test sessions. It should benoted that response slowing and increased variabilitywere limited to the first in-flight session for the track-ing paradigm, but were most pronounced duringlater in-flight sessions for the pointing paradigm.

Force Discrimination and Control During a MIR sta-tion mission the ability of a cosmonaut to reproduceseveral positions of a handle from memory was test-ed. The accuracy with which the handle was set to agiven position was reduced; however, the temporalparameters of the movement and the number of dis-cernable handle positions did not change (94, 154).

Fine Motor Control Campbell et al. (31) evaluatedthe feasibility of survival surgery performed on ratsduring the Neurolab Shuttle mission. Craniotomy, legdissection, thoracotomy, laminectomy, and laparoto-my were performed as a part of physiological investi-gations. Surgical techniques successfullydemonstrated in rats during space flight include gen-eral anesthesia, wound closure and healing, hemosta-sis, control of surgical fluids, operator restraint, andcontrol of surgical instruments. Although the crewnoted no decrement in manual dexterity, the opera-tive time was longer compared with the ground expe-rience due to the need to maintain restraint of surgicalsupplies and instruments. In another study, Rafiq etal. (145) measured the effect of microgravity on finemotor skills by investigating basic surgical task per-formance during parabolic flight. They found thatforces applied to the laparoscopic tool handles duringknot tying were increased force while knot qualitywas decreased during flight compared with groundcontrol sessions. Also, Panait et al. (135) studied theperformance of basic laparoscopic skills (clip applica-tion, grasping, cutting, and suturing) during parabol-ic microgravity flights. When compared with onegravity performance, they found that there was a sig-nificant increase in tissue injury and task erosion anda decreased trend in the number of tasks successfullycompleted.

Dual Tasking and Manual Performance Manzey et al.(99, 100) investigated motor skills in space underdual-task conditions. They found interferencebetween a compensatory tracking task and a concur-rent memory search task to be greater in space thanon Earth. The elevated interference was greatest earlyin flight, but gradually normalized, reaching the pre-flight baseline only after about nine months in orbit.In one of these studies, Manzey et al. (100) also found


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that task interference was independent of the difficul-ty of the memory search task, suggesting that the crit-ical resources affected were probably not thoserelated to memory, but rather those pertinent tomotor programming (both tasks required an immedi-ate motor response).

Laboratory tasks might underestimate the actualdeficits since they differ from a real-life scenario in anumber of ways. For example, the slowing of aimedarm movements was 10-30% in experimental tasks,but was up to 67% during routine activities on Skylabas analyzed using time and motion studies (90).Degradation of performance may be exacerbated inpart due to postural instability, which may not play arole when a pilot controls a landing while strappedinto a seat, but may have a greater impact if landingis performed while standing like during the Apollolunar landings.

Studies Demonstrating Decrements in SpatialOrientation Perception

Spatial disorientation has been one of the mostfrequently studied aspects of sensory-motor adapta-tion to and from space flight. Returning crewmem-bers report that the most overt physiologicalphenomena associated with space flight are inversionillusions at main engine cut off, occasional in-flightdisorientation, early-mission motion sickness, andhead-movement-contingent disorientation duringentry and landing. These neuro-vestibular phenome-na occur during and after G-level transitions, which,unfortunately, also correspond to mission phaseswhere physical and cognitive performance are partic-ularly critical for crew safety and mission success.Accurate perception of self-in-space motion and self-motion relative to other objects are critical to piloting,driving, and remote manipulator operations. A sum-mary of the main findings follows.

Manual Control of Vehicle Translation and Tilt Instudies performed immediately after two Spacelabmissions, returning astronauts were seated on a rail-mounted sled, and asked to use a joystick to null arandom linear disturbance movement along theirinteraural (6) and/or longitudinal (110) body axes.Four of the seven subjects tested showed improvedpostflight performance on the nulling task. Also,Merfeld (109) tested the early postflight performanceof astronauts trying to maintain a flight simulator inan upright orientation in the presence of pseudoran-dom motion disturbances about a tilt axis locatedbelow their seat. On landing day, both subjectsshowed impaired ability to control their tilt in thedark, but displayed normal responses when visual

motion cues were provided. Results confirm thatreturning crews have difficulty estimating their tiltorientation with respect to the gravitational verticalon landing day. The absence of change with visualcues shows that neuromuscular and fatigue factorswere not major contributors to the effect. It is impor-tant to note that the subjects in these experiments allknew whether tilt or translation motions were possi-ble. Subsequent experiments (137, 183) showed thatwhen subjects must resolve tilt-translation ambigui-ties, and are naïve to the possible motion, large mis-perceptions of tilt could result (see Tilt-Translationand Tilt-Gain Illusions below).

Spatial Disorientation During Space Flight The liter-ature on spatial disorientation events during spaceflight has been well-reviewed by Oman (122, 123).Numerous detailed firsthand accounts by astronautsand cosmonauts have also appeared (30, 39, 83, 93, 95,127). Almost all crewmembers describe a transientsomatogravic tumbling illusion or momentary inver-sion illusion upon reaching orbit, when main enginecutoff causes a rapid deceleration to constant orbitalvelocity. About 10% subsequently experience a senseof gravitational inversion that persists regardless ofrelative body orientation in the cabin, even with eyesclosed. Persistent inversion illusions are thought toresult from the combined somatosensory effects ofheadward fluid shift, and saccular otolith unweight-ing (115, 128).

Far more universal is the “visual reorientationillusion” (VRI), first described by astronauts on theSkylab and Spacelab-1 missions (39, 128). When crewfloat about in the cabin, they often experience a spon-taneous change in the subjective identity of sur-rounding surfaces, such that the “surface beneath myfeet seems somehow like a floor.” Oman et al. (39, 122,123, 128, 129) noted that astronauts must orient withrespect to a vehicle frame of reference defined bylocal visual vertical cues. However, architectural sym-metries of the cabin interior typically define multiple“visual vertical” directions, usually separated by 90˚.The Earth can provide yet another visual referenceframe when viewed through cockpit windows orwhile spacewalking. There is a natural tendency toperceive the subjective vertical as being aligned withthe head-foot axis, generally referred to as the“idiotropic” effect (116). Which visual reference framethe observer adopts thus depends strongly on relativebody orientation and visual attention. VRI occurwhen the perceived visual vertical reference frame isnot aligned with the actual, so that, for example, theoverhead surface is perceived as a deck. Recent datafrom animal experiments in parabolic and orbitalflight (123, 169) suggest that the VRI surface identity



illusion physiologically corresponds to a realignmentof the two-dimensional plane that limbic neurons useto code direction and location (see Physiological Basisfor Spatial Disorientation below). When VRI occur,crews lose their sense of direction with respect to theentire vehicle, and reach or look in the wrong direc-tion for remembered objects. Susceptibility to VRIcontinues through the first weeks in space, and occa-sional illusions have been reported after manymonths on orbit. Strong sensations of height vertigohave been described during spacewalks. These mightreflect sudden changes in the limbic horizontal frameof reference from the spacecraft to the surface of theEarth.

VRI can also occur on Earth, but reorientationsusually occur only in yaw perception about the grav-itational axis (e.g., when we emerge from a subwayand discover we are facing in an unexpected direc-tion). VRI about Earth-horizontal axes have been cre-ated using tumbling rooms and virtual realitytechniques. For example, Howard and colleagues (70,76, 77, 80) have shown that the direction and strengthof visual vertical cues depend on field of view, the rel-ative orientation of familiar gravitationally “polar-ized” objects, and the orientation and symmetry ofsurfaces in the visual background. Single planar sur-faces or the longer surface in a rectangular room inte-rior were most frequently identified as “down.”Oman (123) has noted that prior visual experienceand knowledge of the specific environment are alsoimportant factors. Even when VRI do not occur, thevisual verticals of adjacent or docked spacecraft mod-ules are often incongruently aligned. Astronauts typ-ically orient to the reference frame of the localmodule, and significant cognitive effort is required tosort out these multiple vehicle frames of reference.Using virtual reality simulations, Oman and col-leagues (4, 5, 123) have recently shown that subjectsremember the interiors of each module in a canonical,visually upright orientation. When performing tasksthat require subjects to interrelate different referenceframes, additional time is required and workloadimposed. The fastest responses occur when moduleverticals are congruently aligned. Significantlygreater time is required to perform simulated emer-gency egress navigation tasks when module visualvertical reference frames are incongruently aligned(125).

Physiological Basis for Spatial Disorientation Thephysiological basis of spatial orientation perceptionbecame better understood with the discovery in ratand primate limbic systems of place cells that codethe direction the animal is facing, independent ofhead movement. Also discovered were grid and place

cells that code various attributes of location relative tovisual landmarks (184), analogous to a map of thelocal environment. All three classes of cells respond ina navigation coordinate frame normally defined bythe plane of locomotion, even in 0 G and hypergravi-ty (86, 169). How larger (geo) scale environmentalknowledge is coded is not yet understood, but clini-cal evidence from patients with poor geospatial abili-ties suggests that these same limbic structures at leastparticipate.

Tilt-Translation and Tilt-Gain Illusions Arguably thegreatest space flight-related challenge to the humaninternal navigation system results from the ambigui-ties between tilt and translation stimuli. AlbertEinstein was the first to postulate “the completephysical equivalence of a gravitational field and acorresponding acceleration of the reference system”(47). According to his equivalence principle, linearaccelerations resulting from translational motions arephysically indistinguishable from linear accelerationsresulting from tilts with respect to gravity because theforces are identical in nature. The ability of the centralnervous system to resolve tilt-translation ambiguitiesis critical to providing the spatial orientation aware-ness essential for controlling activities in everydaylife.

Two hypothetical mechanisms that have beenproposed for resolving tilt-translation ambiguities arefrequency segregation and multi-sensory integration.The frequency segregation hypothesis suggests thatlow frequency linear accelerations are interpreted astilt and high frequency accelerations as translation(101). This hypothesis appears consistent in principalwith the response dynamics of the different primaryotolith afferents (50, 140), secondary processing ofotolith input in the vestibular nuclei (85, 187), andalso with natural behavior (142). The multi-sensoryintegration hypothesis, on the other hand, suggeststhat the brain must rely on information from othersensors, such as canals and vision, to correctly dis-criminate between tilt and translation (2, 63). Morespecifically, it suggests that the brain learns to antici-pate a sequence of sensory feedback patterns for anygiven movement. This hypothesis generally involvesthe use of “internal models,” or neural representa-tions of physical parameters, and combines efferentand afferent information to resolve sensory ambigui-ty (45, 58, 121, 189, 197).

Although multi-sensory integration and frequen-cy segregation are typically posed as competinghypotheses, they are not mutually exclusive. The seg-regation of otolith-ocular responses as a function offrequency has been clearly demonstrated (e.g., 132).Yet one implication of frequency segregation is that


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there must be a mid-frequency crossover regionwhere it is difficult to distinguish tilt from translation.Paige & Seidman (133) reported that the crossoverfrequency is approximately 0.5 Hz in primates, andWood (186) suggested that it occurs at about 0.3 Hz inhumans. Multi-sensory integration may play a criticalrole near the crossover frequency.

Among the factors that facilitate sensory-motoradaptation, active voluntary motion may be one ofthe most important (182). Performing visual taskswith the intent to override vestibular input may alsocatalyze adaptation (64). Most sensory conflict theo-ries related to sensory-motor adaptation have beenderived from the concept of ‘efference copy’ whichstates that there are predicted sensory feedbacks forany given motor action (148, 178). Head movementkinematics on Earth yield invariant unique patternsof canal and otolith signals irrespective of other sen-sors (65). During adaptation to altered gravito-inertialenvironments, though, new patterns of sensory feed-back must become associated with head movementsto reduce sensory conflict. The observation that someastronauts tend to restrict head-on-trunk movementson orbit, preferring to rotate more from the waist thanthe neck, reflects an adaptive change in motor strate-gy that might further contribute to motion sickness(179) and post-flight postural and gait dysfunction(18). This is also a common symptom of patients withvestibular hypofunction.

Following adaptation to weightlessness duringspace flight, the reappearance of gravito-inertial forceduring reentry produces strong head movement-con-tingent vertigo, oscillopsia (illusory motion of theentire visual scene), and reduced visual acuity.Crewmembers train themselves to limit head move-ments, but some make deliberate small movements inan effort to accelerate readaptation. The illusory sen-sations persist for at least several hours after flight.During the initial recovery, it is often reported that 1-G feels like three. Crewmembers typically exit theShuttle using a wide gait, and a few long durationcrews have been simply unable to stand or walkunaided for several hours or longer. Crews typicallysay that when they tilt their heads, they feel that the“gain” of their head tilt sensation is increased, as iftheir head had rotated farther than expected. Typicalpilot comment: “That really tumbled my gyros.” Thesensation is thus reminiscent of the conventionalhypergravic G-excess illusion. Other returning astro-nauts describe a transient sensation of horizontal orslightly upwards linear translation as a result of headtilt (69, 138, 153). One of the most common post-flightillusions is of perceived translation, either of self orsurround, during a tilting motion (68). In one of thefirst post-flight experiments to investigate this phe-

nomenon, Reschke and colleagues (138, 155) used aparallel swing to provide horizontal (interaural axis)translation and/or roll rotation about the head naso-occipital axis. All six astronauts participating in thisstudy reported an increase in perceived lateral trans-lation during passive roll rotation after flight.

On the basis of these observations, and similarones reported by Young et al. (194), the otolith tilt-translation reinterpretation hypothesis (OTTR) wasproposed (138, 194). The OTTR hypothesis is basedon the premise that interpreting otolith signals asindicating tilt is inappropriate during space flight.Therefore, during adaptation to weightlessness, thebrain reinterprets otolith signals as indicating transla-tion only. Other post-flight observations that havebeen used to support the OTTR hypothesis includedecreased postural stability (75, 134) and decreasedstatic ocular counterrolling (177, 195). Relevant todriving tasks on sloped terrains, it is interesting tonote that performance during roll-tilt closed-loopnulling tasks is decreased for several days post-flight(107), while performance during translation closed-loop nulling experiments appears to be improved (7).

An alternative hypothesis proposed by Guedry etal. (65) suggests that rather than a reinterpretation ofotolith signals, adaptation to space flight mightinvolve ‘shutting down’ the search for position (tilt)signals from the otolith system in order to avoidvestibular conflict. This is based on the observationthat on Earth the initial head position relative to grav-ity before a head turn foretells the unique combina-tion of canal and otolith signals that will occur duringthe turn. The absence of a meaningful initial positionsignal from the otoliths on orbit may therefore befunctionally disruptive, and eventually neglected.Guedry’s hypothesis (65) also explains the post-flighttilt-translation disruptions described above, as wellas the increased immunity to Coriolis stimuliobserved following the Skylab missions (57).

Differences between active and passive motionsmay help explain some of the apparently contradicto-ry observations regarding post-flight tilt-translationdisturbances. For example, Golding et al. (56)observed striking differences in motion sickness sen-sitivity between active and passive tilts. It is likelythat the new ‘expected’ patterns of sensory cuesadopted during head tilts on orbit will differentiallyinfluence responses during reentry depending onwhether the motion is self-generated.

Merfeld and colleagues (108, 111, 112) have pro-vided additional insight into the origin and relation-ships between the post-flight Tilt Gain and OTTRillusions. Merfeld (108) noted that the OTTR hypoth-esis assumes that the utricular otolith mediates all tiltsensation, and that if otolith cues were simply rein-



terpreted as linear acceleration, a sustained head tiltshould produce a sustained accelerationsensation–not what is usually observed. He hypothe-sized that both types of illusions could result from achange in the effect of semicircular canal cues on esti-mating transient rotations of the direction of “down”relative to the head. Unless the CNS estimate of angu-lar velocity is aligned with the estimated direction ofgravity, a conflict occurs. His hypothesis (111), knownas the Rotation Otolith Tilt-TranslationReinterpretation (ROTTR) hypothesis, suggests thatthe CNS resolves this conflict by rotating the directionof its internal estimate of gravity at a rate proportion-al to the vector cross product of the estimated angu-lar velocity and gravity vectors. These rate constantsdetermined the dynamics of the resulting illusion.

Tilt-translation illusions can occur during space-craft pitching or rolling maneuvers, even if the pilot’shead remains stationary relative to the cockpit, andcould lead to in incorrect manual control responses.For example, a Tilt Gain illusion might result in anunder-response to a Shuttle wing drop, a sensationthat a wind gust was pushing the nose up unexpect-edly, resulting in under-rotation during the criticallanding flare maneuver. An OTTR illusion might pro-duce an over-response to a wing-drop, and perhapsthe sensation that a gust had suddenly pushed theShuttle off runway centerline. One implication ofROTTR theory is that the tendency toward Tilt Gainor OTTR illusions may be a personal characteristic. Ifso this could account for the diversity in the anecdot-al descriptions by astronauts. Unfortunately, there areas yet no systematic longitudinal clinical data on thedirection and strength of post-landing head tilt illu-sions in the Shuttle Program.

Two separate human experiments conducted onorbit by Clément et al. (36) and Reschke et al (151)investigated the effects of sustained linear accelera-tions during eccentric rotation created by short-radius centrifuges. Interestingly, subjects reported nosense of translation in either experiment during theconstant velocity centrifugation. Reschke et al (151)exposed subjects to 0.2 Gz at the head during 60 s ofconstant velocity, which was insufficient to provide avertical reference (12), possibly because of the oppos-ing G-gradient along the trunk and legs and/or therelatively small resultant force level (114). Clément etal. (36) exposed subjects to greater force levels (0.5 Gyand 1.0 Gz) for up to 5 min. These forces did providea vertical reference on orbit, with subjects perceivingroll-tilt when the resultant force was directed alongthe interaural axis, and inversion when the resultantforce was directed towards the head (36). Ocularcounterrolling was also unchanged during this exper-iment (117).

Physiological Basis for Tilt-Translation and Tilt-GainIllusions Some evidence exists that provides insightinto the physiological basis of these illusions. Forexample, in a series of rodent experiments, Ross andcolleagues (158-161) showed increased numbers ofsynapses in type II hair cells of the utricular maculaeduring and just after space flight. The findings ofincreased synaptic plasticity are consistent with thehuman behavioral studies suggesting an increasedgain of the otolith organs. These findings were alsosupported by an experiment performed by Boyle et al.(28) aboard the Neurolab mission, in which the pri-mary utricular afferent information was shown to behighly potentiated (up-regulated) during the first fewhours after space flight in oyster toadfish (Opsanustau) subjected to linear translations in various planes.These data were similar to those reported by Reschkeet al. (152), who found an enormous potentiation ofthe monosynaptic Hoffman (H-) reflex response earlyafter flight in human subjects from the Spacelab-1mission subjected to linear translational accelerationstimuli. This H-reflex response, which is modulatedby descending signals from the vestibular otolithorgans and normally aids in preparing the anti-grav-ity muscles for stable landing following a jump (orfall), had completely disappeared in these same sub-jects by the sixth flight day of the mission. Furtherevidence was obtained by Holstein et al. (74), whofound in rodents flown aboard the Neurolab missionultrastructural signs of plasticity in the otolith recipi-ent zone of cerebellar cortex (nodulus), an areathought to be critical for motor control, coordination,timing of movements, and motor learning. Rats flownfor 5-18 days in the Russian Cosmos BiosatelliteProgram also showed morphological changes in neu-ral structure, including decreased lengths in den-drites directed from cells in the reticular formationtoward structures in the vestibular nuclei and mor-phological changes in cerebellar structures includingmossy fiber terminals in the granular layer of thenodular cortex (89). Pompeiano (141) also studiedrodents flown aboard the Neurolab mission. Hefound biochemical evidence of plasticity (expressionof the immediate early gene c-fos and presence of fos-related antigens) in multiple regions of the brain,including the vestibular nuclei, which play a role incontrolling posture and eye movements, the nucleusof the tractus solitaries (NTS), which is involved inregulation of cardiovascular and respiratory function,the area postrema, which plays a role in motion sick-ness, the amygdala, cortical and subcortical areasinvolved in body orientation and perception, and thelocus coeruleus, which is involved in regulation ofthe sleep-wake cycle.


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Studies Demonstrating Decrements in CognitiveFunction

Controlling vehicles and other complex systemscan place high demands on cognitive and psychomo-tor functions. Space flight might affect these functionsthrough direct microgravity effects (such as thosedescribed in the preceding sections) or through stresseffects associated with sleep loss, workload, or thephysical and emotional burdens of adapting to thenovel, hostile environment (84). Kanas & Manzey (84)provide a good overview of the relevant evidence. Asshould be clear from the evidence presented above,space flight induces many of the hallmarks of a(reversible) vestibular lesion. Cognitive deficits, suchas poor concentration, short-term memory loss, andinability to multi-task occur frequently in patientswith vestibular abnormalities (78, 79). Hanes &McCollum (67) have recently published a thoroughreview of the literature suggesting broader interac-tions between vestibular and cognitive function(including oculomotor, motor coordination, and spa-tial perception/memory effects similar to thosedescribed above) and demonstrating a physiologicalbasis through observations of neuronal projectionsfrom the vestibular nuclei to the cerebral cortex andhippocampus. These results suggest that cognitiveabilities may be most compromised during landing,particularly if an off-nominal event occurred that hadnot been recently well-rehearsed.

B. Ground-Based Evidence

Few robust ground-based models are availablefor simulating/observing the impacts of space flighton a crewmember’s ability to maintain control ofvehicles and complex systems. Where relevantground-based studies exist, they have been includedin the discussions presented above. However, under-standing ground-based aviation experiences withspatial disorientation may be useful to identifyingand mitigating space flight related issues with spatialdisorientation. Thus, this section reviews studies onthe effects of spatial disorientation on aircraft control.

Spatial Disorientation in Aviation SpatialDisorientation (SD) is traditionally defined as a “fail-ure to correctly perceive attitude, position, and motion ofthe aircraft” (11), as displayed on the aircraft’s primaryattitude and flight control displays (53). A history ofaviation SD research, a taxonomy of the classic SDillusions, an explanation of the underlying physiolo-gy, and data on incidence of SD related accidentshave been well-reviewed by Previc & Ercoline (143),

Gillingham et al. (53, 54), and Young (191). Classic SD(e.g., somatogravic illusions, leans, G-excess illusions,inversion illusions, or Coriolis illusions) can resultfrom unusual vestibular stimulation or from sparse ormisleading visual cues (false horizons, ambiguoussize, or surface slant cues). SD has been further cate-gorized (54) as Type I (unrecognized), Type II (recog-nized), or Type III (incapacitating). Type 1 SD is themost insidious because the pilot is unaware the air-craft is in a dangerous state.

Spatial disorientation remains an enduring prob-lem in aviation. Surveys consistently indicate that amajority of pilots have experienced significant SD,many more than once. Pilots spend hours training,hoping that when SD occurs they will recognize itand be able to fly through it using their instruments.Incidence of SD depends on the type of flying andweather conditions. The likelihood that SD will createan accident goes up when flying at low altitude, sincethere is less time to recognize and recover. In US gen-eral aviation, SD is a factor in 15% of fatal accidents,a rate of one every 100,000 flying hours (NTSB 2007).Hence there is one fatal SD related accident approxi-mately every week. In US scheduled airline flying,most of which is at high altitude and on autopilot, theSD rate is far lower, though, as discussed below, con-trolled flight into terrain during approach remains aproblem. For similar reasons, in military flying, SDrates are higher in fighter/attack aircraft and helicop-ter operations than in military transport flying. In theUS Air Force, the overall SD rate is 0.5 per 100,000 fly-ing hours. SD was a factor in 14% of all major acci-dents, and insufficient or misleading visual cuescontributed to 61% of these (73, 96). Many militaryaircraft HUD displays automatically declutter to bet-ter support recognition and recovery of extreme atti-tudes. In US Army helicopter operations, most ofwhich take place at low altitudes, the overall SD ratehas been about 3 per 100,000 hours. However, the raterises by a factor of five at night, and by 20 when nightvision goggles are used (29, 41, 46). Lack of reliablevisual references has been the most frequent cause ofhelicopter SD fatalities, typically due to rain, fog,blowing snow or dust during landing.

There is evidence from flight simulator experi-ments that instrument flying experience and recency(within 2 weeks) helps pilots “fly through” disorient-ing transients created using galvanic stimulation ofthe vestibular system (98). However, applying suchstimulation to pilots flying visual approaches cantrigger pilot induced oscillations (97).

Geographic Disorientation and Terrain Awareness Asecond class of accidents and incidents are caused by“Geographic Disorientation,” defined as the failure to



recognize and/or maintain the desired position rela-tive to the external ground and airspace environment(3). Common examples include becoming lost in theair or on the ground and then straying into prohibit-ed airspace, landing at wrong airport, or taking off,landing, or intruding into an inappropriate runway,causing collisions or overruns. Cockpit map displayshave reduced these accidents, but do not (yet) depictrunway/taxiway details.

Loss of “Terrain Awareness” is almost always afactor in Controlled Flight Into Terrain (CFIT) acci-dents, where the pilot unintentionally flies into ter-rain, usually during the approach-and-landing phase.Ground proximity warning systems (e.g. GPWS,MSAW), mandated since the 1970s in civil transportaircraft, have reduced the number of CFIT accidents,but they still account for a third of all fatal accidentsin this sector over the past decade (25). CFIT canresult from classic spatial disorientation, but morecommonly results from loss of terrain awareness dueto preoccupation with other tasks, or incorrectly set-ting and/or inappropriately trusting the autopilot.Electronic cockpit map displays highlighting nearbyterrain (e.g. TAWS) and “synthetic vision” back-grounds for attitude indicators, depicting a virtual“out the window” view are expected to reduce CFITincidence.

Because the classic definition of spatial disorien-tation does not include Terrain Awareness orGeographic Disorientation, CFIT and geographic dis-orientation accidents are typically only categorizedby investigators as due to “Loss of SituationalAwareness.” At the most general level, SituationAwareness (SA) is defined as perception of elementsdefining a mental model of the current situation,comprehension of their meaning, and projection oftheir future status (49). Obviously, there are manydimensions to SA, including all elements of spatialknowledge, as well as awareness of traffic, weather,autopilot mode, fuel, system, and weapon status, etc.The more general SA concept has proven useful inunderstanding many types of accidents, partlybecause it emphasizes the importance of “confirma-tion bias” in attention, perception, and decision-mak-ing. Classic spatial disorientation accidents shouldalso be properly co-coded as loss of situation aware-ness accidents (144), but traditionally are not.

Overall, one concludes that large transport air-craft operations are relatively safe – less than one spa-tial disorientation related accident every 106approaches. However, in other aviation segments,where more of the flight is conducted at low altitude,in bad weather, and/or using sensory aids, the fatalaccident rate rises by an order of magnitude or more.

II. COMPUTER-BASED SIMULATION INFOR-MATION

While there are few robust ground-based modelsavailable for experimental investigations of theimpacts of space flight on a crewmember’s ability tomaintain control of vehicles and complex systems,many computer-based models of the vestibular sys-tem and sensory-motor control have been developed.Since these may be useful in simulating and/or pre-dicting the impacts of physiological adaptations onoperational performance, particularly under off-nom-inal conditions, a brief review of the relevant aspectsof the field is provided in this section. Before they canbe used in design and verification, though, these (andother) models must be quantitatively validated andcertified using targeted empirical studies.

Models of Vestibular Function and SpatialOrientation Vestibular neuroscientists have developedquantitative mathematical models for semicircularcanal and otolith function, eye movements, and cen-tral nervous system (CNS) estimation of angular andlinear motion perception. For example, Fernandez &Goldberg (51) modeled the firing frequency fi of indi-vidual semicircular canal afferents using a lineartransfer function model of the form fi(s)/ω(s) = s2 Ki[(Kr s +1)/( τd s + 1)( τ cs +1)( τa + 1)], where ω is thecomponent of head angular velocity in the canalplane, Ki is mid frequency gain, Kr is high frequencygain , τd and τ c are the time constants of endolymphflow drag development and cupula-endolymphreturn (62, 129), and τa is a time constant describingneural adaptation (193).

Young (196) originally suggested that the CNSfunctions like an adaptive (Kalman) filter when com-bining sensory cues, and introduced additionaldynamics into vestibular responses due to these cen-tral processes. Adapting inertial guidance theory,Young and colleagues (188, 192, 194) noted that lawsof physics dictate that the body’s graviceptorsrespond to the net gravito-inertial specific force (f = g– a), the physical quantity tracked by a pendulum ormeasured by a linear accelerometer (where a = linearacceleration vector and g = gravitational accelerationvector). A variety of different orientations and accel-erations can cause the same graviceptor stimulus. TheCNS must therefore use other cues to distinguish thecomponents caused by gravity from those caused bylinear acceleration. The CNS may estimate linearacceleration by maintaining an internal estimate ofthe direction and magnitude of (ĝ) and subtracting offthe graviceptor cue vector (â = ĝ - f). The direction ofdown, ĝ is estimated at low frequencies based on theaverage direction of graviceptor cues, f, and also


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visual cues, if available. Visual inputs are angular andlinear velocity of the visual surround with respect tothe observer. At high frequencies, semicircular canalcues and body movement commands are used. If thedirection of ĝ is misestimated, dramatic mispercep-tions of orientation and linear acceleration can result.

Although “optimality” of the human observer (inthe Kalman sense) has since been discounted, thenotion remains widely accepted that the CNS func-tions as an “observer,” in the control engineeringsense (27), estimating head orientation based oninternal representations of the direction of gravityand sensory organ dynamics. Others have elaboratedCNS observer-based models for semicircular canal-otolith interaction. For example, Raphan et al. (147),Robinson (156), and Merfeld et al. (111) developedinfluential observer class models for CNS estimationof head angular velocity and tilt, now often referredto as “central velocity storage” theories. Merfeld’scontemporary models for canal-otolith cue interac-tion in “down” estimation (108, 112) successfully pre-dict canal-otolith cue interaction in a variety ofexperimental situations. They are now widely uti-lized in research and the diagnosis of clinical vestibu-lar disorders. These models have occasionally beenapplied to aircraft accident investigation, albeit in alimited way, since they do not (yet) incorporateeffects of visual cues, and data on aircraft accidents isfrequently lacking.

Models of Manual Control Performance ManualControl theory was originally developed in the 1960s,when feedback control engineers sought to analyzeand predict the performance of humans in controlloops, and describe both the human (the operator)and the controlled system (the plant) within the samemathematical framework. The premise was thathuman operator performance could be approximatedwell using a “describing function.” Both compensa-tory tasks (where the operator sees only an error sig-nal) and pursuit tasks (where both the goal and plantoutputs are available) have been modeled this way. Asimple and widely used principle is the “crossovermodel” (104), which posits that the operator willinstinctively adopt an appropriate control strategysuch that at the open loop transfer function of theoperator and plant taken together resembles that of asimple integral process and a time delay in the regionof the crossover frequency. The operator can perceivethe rate of change of plant output, and create antici-patory phase lead that counteracts phase lags due tothe plant. If the plant is a vehicle, vestibular motioncues allow the operator to improve performance bycreating additional phase lead. However, the opera-tor’s transfer function is constrained. Some effective

time delay is always present due to perceptual, cog-nitive, and muscle activation effects. Also, operatorscannot respond to the second or higher derivatives ofplant output. The crossover model structure andparameter values thus quantify the operator’s controlstrategy. The model also has important emergentproperties: It predicts manual control gain and band-width limits. It also explains why humans cannot suc-cessfully stabilize higher than second order integralplant dynamics, unless the operator is able to monitorintermediate system outputs, in effect transformingthe task into concurrent (multi-loop) lower ordertasks. This is why an operator cannot successfully sta-bilize a hovering lunar lander or a helicopter (approx-imately triple integral plants) over a landing spotwithout reference to a real or artificial horizon, andwhy motion cues can have a dramatic effect on con-trolling marginally stable plants (165, 190). Thecrossover model has been extended to multi-loopcontrol and validated across a wide variety of plantdynamics, and extensively applied in many domains,particularly in the area of vehicle handling qualitystandards (192).

In the late 1960s, newer estimation and optimalcontrol concepts, such as the Kalman observer andcontroller, were used to extend manual control theo-ry. The optimal control model (10) posited that thehuman observer’s control strategy utilized an inter-nal dynamic mental model for the plant, and itweighted feedback information based on priorknowledge of uncertainties. (Concurrent efforts byneuroscientists led to the present generation ofObserver Theory models for orientation and sensoryconflict in motion sickness described earlier.) Earlyapplications included helicopter hovering and atten-tion sharing. Results demonstrated the importance ofvestibular motion cueing (9, 42).

When performing maneuvers such as flaring anaircraft on landing, a highly skilled human operatoruses a “precognitive control strategy,” and generatesopen loop, preprogrammed commands based on amental model of the plant. The preprogrammed com-mand accomplishes most of the maneuver, but theoperator completes the task by switching back to con-ventional compensatory manual control for finalerror reduction. The Shuttle landing flare is an exam-ple of a task accomplished using precognitive control(8). Landing performance depends critically on prop-er timing of the preprogrammed manual flare com-mand, and correct estimation of the aircraft state atthat moment. Incorrect precognitive manual com-mands result in greater need for subsequent compen-satory error reduction. After the flare, the pilot exerts“tight” control over aircraft altitude and altitude ratein order to achieve a smooth touchdown, employing



relatively high control gain. Because the Shuttle flightcontrol system has inherent phase delays and ratelimits, excessively large pilot control gain can makethe combined pilot-vehicle system unstable, and trig-ger pilot induced oscillations (104). At the time it wasnot generally recognized that misperceptions of vehi-cle pitch attitude and rate could also potentially causeover control and pilot induced oscillations (PIO), butthey were detected during the Shuttle EnterpriseApproach and Landing Test flight test program,where disorientation was presumably not a factor.Since control system delays could not be eliminated,a stopgap solution was to detect large oscillatory con-trol stick commands using a suitable nonlinear filter,and adaptively reduce pilot control authority (167).Adaptively reducing control authority worked for“conventional” PIO. However, as described earlier,STS-3 subsequently experienced a PIO despite thePIO suppression filter. The only solution for disorien-tation induced PIO is to provide strong visual cues topitch and pitch rate via a HUD, and restricting land-ings to conditions of good visibility. If the Shuttlewere required to land in brownout/grayout condi-tions (e.g. as are Lunar Landers), PIO would be a con-tinuing concern.

III. RISK IN CONTEXT OF EXPLORATION MIS-SION OPERATIONAL SCENARIOS

Sensory-Motor Standard

A sensory-motor standard has been drafted(NASA Standard 3001) for exploration class missions:“Pre-flight sensory-motor function shall be within normalvalues for age and gender of the astronaut population. In-flight Fitness for Duty Standards depend on mission andhigh risk activities, and they shall be assessed using metricsthat are task specific. Sensory-motor performance limits foreach metric shall be operationally defined.Countermeasures shall maintain function within perform-ance limits. Post-flight rehabilitation shall be aimed atreturning to baseline sensory-motor function.” However,operational performance limits related to flight vehi-cle control (particularly for post-adaptation activities,such as rendezvous/docking and entry/landing),ground vehicle control (e.g., Lunar or Martian rovers),and remote manipulator/teleoperation activitieshave not yet been established.

Risks During Piloted Landings

Piloting a spacecraft through entry and landing isone of the most difficult tasks associated with spaceflight. The consequences of failing to complete thistask successfully could be catastrophic, resulting in

loss of life, vehicle, or other assets. While all pilotedlandings from space have been successful to date, theevidence presented above suggests that the landingperformance has been lower than desired for both theShuttle and the Lunar Lander. To the (currentlyunknown) extent physiological adaptations play arole in these performance decrements, we can antici-pate that the risk of failure will become much greaterduring Mars missions. There is strong evidence thatthe six-month outbound trip (without artificial gravi-ty) will cause a much more profound sensory-motoradaptation to zero-G than occurs during a 1-2 weekShuttle mission. This will likely cause a more pro-found physiological response to the G-transition dur-ing entry/landing; however, the impact of thereduced amplitude (3/8 g vs. 1 g) of the transition isunknown. Furthermore, piloting recency willdecrease from 1-2 weeks during the Shuttle programto approximately six months during a Mars mission,decreasing the probability that a pilot will be able tofly through any spatial disorientation that accompa-nies the G-transition. Even piloted landings on theMoon present some unique risks, owing to the effectsof the novel gravitational environment on spatial andgeographic orientation and the potential for lunardust obscuring vision during critical phases of land-ing.

Risks During Rover Operations

The risk of performance failure (i.e., loss of vehi-cle control) while driving an automobile is high forthose having vestibular deficiencies and for thosewhose cognitive and/or sensory-motor functions areimpaired by ethanol, fatigue, or certain medications.Crewmembers readapting to Earth-gravity followingreturn from space flight exhibit similar performancedecrements, and, as a result, are currently restrictedfrom driving automobiles for a short time (2-4 days)after Shuttle missions and a longer time (8-12 days)after ISS missions. The impact of sensory-motoradaptations on driving rovers on either Moon orMars is unknown. While the potential consequencesof performance failure while driving a rover are lessthan those of piloting a space craft through entry andlanding, the possibility of crew injury (or death) orloss of the rover exists, particularly in the vicinity ofsteep-sided craters. The duration of the initial adap-tation period to the Lunar or Martian gravity envi-ronment is also unknown, and, while likely to beproportional to the time spent in zero-G transit, can-not be determined until it can be measured on theplanetary surface. Thus, the amplitude and durationof increased risk during rover driving are currentlyunknown.


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Risks During Rendezvous/Docking and RemoteManipulator System Operations

Apart from the Spektr incident, performance dataon rendezvous/docking has so far eluded theauthors. However, evidence provided above suggeststhat the incidence of performance failure duringremote manipulator operations aboard the Shuttleand ISS has been fairly well characterized (at leastoperationally). There is no reason to suspect that per-formance of these zero-G operations will be any dif-ferent from our ISS experience during an outboundtransit to Mars. Thus, we would not expect the risk toincrease. However, the risk impacts of an additional18 months at Mars gravity followed by six months atzero-G during return transit are unknown, and maywell lead to an unacceptable range.

Risks While Operating Other Complex Systems

The risk of performance failure during operationof any complex system is multi-factorial. However,operation of any system requiring good visual acuity,eye-hand coordination, (balance/locomotor skills forsurface operations), spatial orientation, and/or cogni-tion could be impaired by physiological adaptationsto novel gravitational environments. The risk ofimpairment is generally greatest during and soonafter G-transitions, but the amplitude and duration ofthe increased risk would need to be evaluated on asystem-by-system basis.

Risks During Near-Term Missions

Despite programmatic guidance that this risk beconsidered low in priority for ISS and Lunar mis-sions, there is significant evidence suggesting that thecontrol of vehicles or complex systems is compro-mised after as little as a few days of exposure tospaceflight environments, and that severity increaseswith increasing exposure time (as might be expectedfor ISS stays and extended Lunar sorties). While theseissues may be more severe for Mars missions withoutartificial gravity, significant risks remain quite realeven for more standard ISS and Lunar operations. Asthe Columbia Accident Investigation Board (CAIB)report warned us repeatedly, a small number of suc-cesses without catastrophic failure (e.g., a little over100 Shuttle landings and 6 lunar landings) does notmean that risk, including human sensory-motoradaptation risks, can be ignored. The near missesreported above provide evidence in this regard. Thearchitecture being employed for NASA’s return to theMoon requires a much more challenging re-entry G-

force and vibration regime than was used duringApollo. Indeed, any human control effort, even undernominal Orion re-entry/descent/landing scenarios,will likely be much more difficult than for Shuttlelandings if this design remains. Furthermore, some ofthe off-nominal human interventions being contem-plated may push human performance of a decondi-tioned crewmember beyond its absolute limit (e.g.,human backup roll control authority during a 5Gx re-entry after three weeks in space). Finally, the properresolution of automation-human control authoritydecisions requires an objective and quantitativeunderstanding of sensory-motor compromises. Therisk of sub-optimal decisions in this regard hasimportant ramifications for overall missionsafety/reliability calculations. Thus, we recommendthat this risk be considered high priority for all spaceflight mission scenarios.

IV. KNOWLEDGE GAPS

The authors, representing the NASA sensory-motor discipline team, have identified the series ofknowledge gaps listed below. Each of them must befilled before this risk can be fully assessed and/ormitigated. The NASA Human Health andPerformance Program has identified the followingknowledge gaps as high priority for the sensory-motor discipline group:

1. There is little evidence correlating extant oper-ational performance data (e.g., extra-vehicular activi-ty performance, remote manipulator systemoperations performance, rendezvous and dockingperformance, Shuttle landing performance, etc.) withclinical and/or research observations of post-landingsensory-motor performance decrements.

2. There is little experimental evidence demon-strating the effects of disorientation and/or inter-individual differences (e.g., in spatial skills) onsupervisory control (e.g., space telerobotic operationsand vehicle docking).

3. There is little experimental evidence demon-strating that flight-related changes in sensory-motorperformance (reduced visual acuity, oscillopsia, headmovement contingent tilt-translation/tilt-gain illu-sions, misperception of vehicle attitude and accelera-tion, unrecognized (type I) spatial disorientation) willcause decrements in and/or limitations to pilotedlanding of vehicles upon arrival at Mars.

4. There are no validated tests to define standardsfor acceptable operational performance ranges basedon crewmembers’ demonstrated post-flight sensory-motor capabilities and disabilities. Nor are there anyvalidated tests to define the linkages between func-tional capabilities and physiological changes.



The Program has also identified the following,relevant knowledge gaps as lower priority for thesensory-motor discipline group, as they belong pri-marily to another discipline:

5. There is little experimental evidence demon-strating how flight-related changes in human super-visory/manual control (including vision, vestibularfunction, and spatial memory) should affectConstellation designs for lunar landings and roveroperations (including geographic orientation, main-taining spatial orientation while maneuvering, visu-ally verifying the suitability of the landing zone, andmaintaining altitude, attitude, and terrain awarenessduring vertical descent and touchdown).

6. There is no validated multi-factorial cognitiverisk assessment test to evaluate spatial skills and/ordefine acceptable ranges of cognitive and psychomo-tor performance.

7. Periodic in-flight medical examinations do notassess vestibular function.

V. CONCLUSION

A large body of sensory-motor and psychologicalresearch data obtained from space flight experimentsover the past half-century demonstrates significantdecrements in oculomotor control, eye-hand coordi-nation, spatial orientation, and cognition duringspace flight missions. While these changes are mostsevere during and after G-transitions, the most cru-cial time for many critical operational tasks (e.g.,landing and egress), only limited information is avail-able to assess the operational impacts of thesechanges. Some of the operational observations arecompelling, but are confounded by unknown envi-ronmental and engineering influences. Others appearto raise little concern, but the safety margins are diffi-cult to estimate. During exploration missions, we canexpect that most performance DURING G-transitionswill be degraded further by the influence of extendedtime in flight (Mars missions), but the potential influ-ence of extended time in hypogravity (Mars andLunar missions) is unknown.

The true operational risks associated with theimpacts of adaptive sensory-motor (and other)changes on crew abilities to control vehicles and othercomplex systems will only be estimable after the gaps(identified above) have been filled and we have beenable to accurately assess integrated performance inoff-nominal operational settings. While exclusivecrew selection procedures, intensive crew training,and highly reliable hardware/software systems havelikely minimized the operational impacts of thesesensory-motor changes to date, the impacts of newmission and vehicle designs may offset some benefits.

Forward work in this area must account for themulti-factorial nature of the problem. While sensory-motor and behavioral (cognitive) disciplines clearlyhave roles to play, muscle (strength and endurance)and cardiovascular (orthostatic tolerance) disciplinesalso must be involved, as should human factorsexperts, training experts, vehicle designers, missiondesigners, and crewmembers. Mechanisms for facili-tating cross-disciplinary investigations are onlybeginning to be established. Future success will clear-ly require more progress in these approaches.

ACKNOWLEDGEMENTS

The authors are indebted to Elisa Allen, JodyCerisano, Julie Esteves, George Ford, and LauraTaylor for their efforts locating and assembling theevidence.

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