1. Saccades, Pursuit, Eye-Head Coordination Introduction Materials

GAZE CONTROL IN MICROGRAVITY

1. Saccades, Pursuit, Eye-Head Coordination

C. Andre-Deshays, * I. Israel, * O. Charade, * A. Berthoz, * K. Popov, t and M. Lipshitst

*Laboratoire de Physiologie da La Perception et de L'Action CNRS, Paris, France; tlnstitute for Problems of Information Transmission, Academy of Sciences, Moscow, Russia : I. I o Abstract - During the long-duration spaceflight tie attention has been given to the pursuit and Aragatz on board the Mir station, an experiment saccadic systems, apart one study of Uri and exploring the different oculomotor subsystems in colleagues (9) who have reported an increase volved in gaze control during orientation to a fixed of latency and decrease of peak velocity of vi target or when tracking a moving target was exe sually guided saccades on 6 male cosmonauts cuted by two cosmonauts. Gaze orientation: with in a 7 -day flight. head fixed, the "main sequence" relationships of Some modifications of saccades or com primary horizontal saccades were modified, peak velocity was higber and saccade duration was bined eye and head movements during orient sborter in fligbt than on eartb, latency was de ing could be expected in the absence of gravity creased and saccade accuracy was better in flight. given that, for instance, tonic deviation of eye With head free, gaze orientation toward the target position in the head has been observed during was achieved by coordinated eye and bead move changes of the gravitational vector in para ments, their timing was maintained in the borizon bolic flight (10). In addition, a bias in the ra tal plane; when gaze was stabilized on the target, tio between eye and head movements could there was a trend of a larger eye than head contri also be expected during orienting in order to bution not seen in prefligbt tests. Pursuit: Horizon minimize head movements, which may be a tal pursuit at 0.25 and 0.5 Hz frequency remained source of space-sickness. More generally, the smooth with a 0.98 gain and minor phase lag, on absence of the gravitational reference may im earth and in flight. In the vertical plane, the eye did not track the target with a pure smooth pursuit eye pair the programming and control of saccade movement, but the saccadic system contributed to or pursuit movements. gaze control. Upwarrl tracking was mainly achieved In the present paper, we shall report results with £ successior. of saccaoe~, wherea~ downward of experiments concerning hOiizontal and ver trackin~ W2S due t( wmoine( smooth pursuit ~mc tical visuc:l!~' guided saccade~ a!lc. smClott pur ca.di-u~ ~accacie~. :-i1!~ ::s~'mmei;:' was main(aineri sui: i1: h:.:raJQr su~jecI~. \,i\'ith th~ h~aC:. eilhe:- durin~ fiigh ~ ir, h~a(;' fb~ec ~nl h~ai ::-et S;iillltjon~l' :~~e ....J. . .-:. Or. earn"," heari p~aL veW::i:: v.:!~ (I!,,;;m.a U:.:V.'li'"(o" !r :ne ~~)!Tl;)anj :)!~ pa;-~:'

Introduction Materials and Methods In recent years a number of studies have been Experimental Procedure devoted to the investigation of the effect of gravity on the vestibulo-ocular reflex (1-5) and The visual stimuli were generated by 2 lin optokinetic nystagmus (1,6-8). However, lit- ear arrays of 813 LEDs alignerl on the two

331 332 C. Andre-Deshays et al arms of a cross whose center was at eye level. Head velocity was recorded by 2 angular The two arms were in the horizontal and ver rate sensors (ARS C141, measure range: tical directions relative to the space cabin wall. ±3000/s) fixed on the mask for yaw and pitch The LEDs were microprocessor driven in fixed rotations. sequences. All analog signals were filtered with the ac The first part of the experiment was per quisition system, "Super-Pocket," and sam formed with head fixed. The subject was fixed pled every 7 ms with a resolution of 12 bits. :,y means of torso and chin restraints, and belt The channels were mUltiplexed on 2 pulse fastened :0 :l table. "Nhen stuaying orie!1t:ng ccde-moduiation (PCvi; :~a!1ne!s and re eye :T! Gv.:rnents. ; ~. e:;\V i se :..:=::: ":is Y; lace:::e::.ts corded :m :l :rrpe ;',:corde, -:-::' ,-\.C :-::~ 30E). ' '' ~ ~ ~ :; r n.t 00n.r-:r: " ' '5~ "lr ~: ~ o -;'! .... r -~/ " I ! r\ iV J :. r : ..,,, '~' / ~ " ' uo;.:crs !3 comrol ' ·e:lit.~y tuJems.

_~ ~ or : ,~ J ~ er: ~:.i ; ~;: . '-r:1~5. J.:lL.. .. ~ ., -!. : :~ : ':' "~l(":( :": "" ..::,sr:lcnaU[S .. Jne ::1e .2 CQ~monau[s l p .)r Jewn ::.lqe~ ~umps, ~ver:i :: ;e~Jnds. sek~rec: 'cr ,;1e ::11ssion) /<.lnic:pmeC: 'In .E:ar;:h -:-:'us each sec;uence ...:cmained 3 steps, anc in ~his experiment with ne whoie iJrotccol. was repeated 3 times. For the study of pursuit The cosmonauts performed j ~raining sessions eye movements, the target was moving sinu (each 1 h long) in the Center for Cosmonauts soidally in 2 sequences, horizontally: 4 cycles training; The Star City, in order to learn the at 0.25 Hz, ± 15° and 4 cycles at 0.125 Hz, experimental procedures. The 2 cosmonauts ±30° with a peak velocity of 24°/s, then ver appointed to the mission both had experience tically: 4 cycles at 0.5 Hz, ± 7 .5° and 4 cycles in high performance jet aircraft and prior at 0.25 Hz, ± 15°, with a peak velocity of space flight experience. The preflight data 24°/s. The same sequences of fixed and mov were collected on the 2 cosmonauts on days ing targets were then presented again in the F-60, F-30, and F-2 before launch; the inflight head free condition with the subject instructed tests were carried out on mission days FD5, to use both eye and head to acquire the tar FD18, and FD22 for subject 1 and on FD20 get. In the space station, the cosmonauts stood for subject 2; the postflight tests were obtained upright facing the cross, 80 cm away. On at R + 2, R + 7, R + 30 for subject 1 (after earth, the subjects were in the same position, 26 days in space) and R + 7 for subject 2 (af or seated during the postflight sessions. Sub ter 6 months in orbit). jects wore a mask, which projected horizon tal beams of light on each side of the head to give landmarks on the horizontal arm of the Data Collection and Analysis cross for correct head repositioning at the be ginning of each session. Eye movements were recorded by conven Horizontal and vertical components of eye tional electro-oculography (EOG) methods. movements, head velocity, target patterns, EOG electrodes were applied at the very be- and a voice channel were recorded on line by impedance stabilization. We did not observe tern ("Super-Pocket''). To read out data on the any significant drift during the recording ses ground, the 2 PCM channels were sent to a de sions in illuminated conditions. The calibra modulator, and the serial output was used to tion procedures were obtained from 3 stepwise generate computer magnetic tapes for off-line fixation task sessions (5° step from 0° to ±15° analysis with a HP 1000 computer. horizontally and vertically, each fixation last From the calibrated eye position records, ing 2 s) performed before orienting to fixed the computer calculated angular horizontal targets and before the pursuit task. Each re and vertical eye velocities after smoothing (low cording session had I-min duration and started pass digital filter with a cutoff frequency of by zeroing the offset. This offset compensa 100Hz, - 3dB), introducing no phase shift for tion was limited to ±50 mY. The gain of the the peak value. Head position was calculated EOG preamp was 4000 with a low-pass filter by integrating velocity traces. bandwidth of 0 to 700 Hz. For the analysis of the orienting task, the Gaze Control in Microgravity 1 333 primary saccade was detected by marks placed Results manually at the onset and end of the eye move ments on visual inspection of position and 1) Orientation to Fixed Targets velocity traces, and a specially designed com puter program calculated latency, accuracy, Head Fixed Condition and dynamic (saccade duration and saccade peak velocity) parameters of primary saccades in correlation with target parameters. The Horizoma/ saccades same analysis was done for head movement by manual marking each event. Using velocity Latencies. In attentive subjects, the sudden thresholds (eye position when eye velocity was displacement of a target from one position to e ow s or more an-SO mS and head po- anothel evokes a saccade after-a laten1:y--ot------f sition when head velocity was below 5°/s for about 180 to 220 ms (dispersion given under 50 ms), this program computed the fixation the form of two standard deviations ranged point reached by eye and head. from 50 to 100 ms) (from pooled data by For the analysis of pursuit, we used the Becker [11]). In control Earth conditions, we original eye position traces without removing found an average latency of 191 ± 42 ms for saccades to calculate the overall saccadic-pur the 5 control subjects (3 trials for each sub suit position gain and phase, adjusting the best ject), 201 ± 48 ms for subject 1 (3 tests pooled fitting sinusoid on the eye position trace and together and 3 trials per test) and 226 ± 50 ms comparing it to the target sinusoid. We recon for subject 2 (3 tests pooled together and 3 tri structed gaze position by adding eye and head als per test). In Figure 1, the latency mean val channels after calibration. ues and standard deviation are shown for As there were only 2 cosmonauts, for sta subjects 1 and 2, preflight, inflight, and post tistical analysis we used separate t tests for flight. In microgravity, for both cosmonauts, each cosmonaut allowing individual compar there was a trend for decrease in latency after ison between preflight, inflight, and postflight target onset. Latency was 172 ± 45 ms at FD5, data. 180 ± 61 ms at FDI8, and 175 ± 62ms atFD22

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o ;r"200j L () ~ - J 1 150 1 c. Subj , ~ 1 6 Subj 2 100~ ., Control ~-ri--~i--~i--'i---'ir--ri---ri---'i---'i--'i~) -60 -30 -2 +5 +18 +20 +22 R+2 R+7 R+30 DAY PRE FLIGHT DA Y IN FLIGHT DA Y POST FLIGHT

Figure 1. Latency (ms) for horizontal sacca des plotted as a function of time, before, during, and after the flight, In head fixed condition. Average latency averaged across 5 control subjects is shown ±1 SO, with a black square. Empty circles are for subject 1 and empty triangles for subject 2. Note that fIi~ht duration for subject 2 Is longer (6 months) than for subject 1 (26 days). iI 1 I. 334 C. Andre ~ 'J",h ays et a/ for subject 1 (statistically significant difference were generally overshot; more distant ones at P < 0.01 for each of the 3 inflight tests, were undershot (10% error amplitude for a relative to preflight or postflight tests) and target distance of 30° or more). We calculated 190 ± 51 ms at FD20 for subject 2 (difference the primary saccade accuracy by using the per at P = 0.06 level, between preflight and in centage of error amplitude: (AT - A E) X flight). After return to Earth, the values were 100/AT, where AT is the target jump ampli close to the preflight values in subject 1: 194 ± tude and AE is the amplitude of the primary 59 ms a[ R + 2,210 ± 49 ms at R + 7 (n = 36), saccade, We did not calculate the frequency ;:tnd :C5 ± 50 r:JS J.[ R + 30. :n subjec~ 2 after of -JcC'.lrrence of ,:;orrective sac.:ades. For :he

:e~:.1rn :0 ::::mh I R + :) .liter 6 months in mi- 5 control subjec:s, the~e was .tn average per ;';.:~..:;:: ':' ..:: .-:;:: 'C[ :)f ? "';)70 =7o/(J for :he fiigh[ ol[ l:17 = 39 :TIS ISlgnificanti:, .:::ir':·erer:.[ primary ;accaCe, in pretligh[ [es[s. for subject from )re:'ligh[ ';, aiues ar P = J,04, ! = 2 . .24), 1, :he :nea:l :::e~cent

o o +20%' IJ.J f I «« I «f- '-J '-o ' '- Q) Jl -o I ~ II I > o Subj 1 o A Subj 2 « I 0: • Control I, o:::::l o « -60 -30 -2 +5 +18 +20 +22 R+2 R+7 R+30 DA Y PRE FLIGHT DA Y IN FLIGHT DA Y POST FLIGHT

Figure 2. Accuracy of the primary eye saccade to horizontal target steps, in head fixed condition. Accuracy Is expressed as a percentage of error: IAT -AE) x 100 IfAT , where AT Is the target jump amplitude and AE Is the amplitude of the primary saccade. Mean values ±1 SE of mean are plotted as a function of time before, during, and after the flight. Black square is for the 5 control subjects, empty circles for subject 1, and empty triangles for subject 2. Negative values are for undershoot, positive ones for overshoot. j' Gaze Control in Microgravity 1 335

final eye position after saccade was accurately On R + 7, the slope was D = 2.S x A + 46.2, maintained on target, with corrective saccades very close to preflight value. For subject 1 when undershot. After return to Earth, there (Figure 4, panel a), the tendency was exactly was an undershoot of 13 .21tfo ± 11 % at R + 2, the same; the slope was lower inflight and, 10% ± 12% atR+7, and 6% ± 12% atR+ 30 even more, we could calculate that the slope for subject 1 and an undershoot of 5.3% ± 9% decreased progressively throughout the flight for subject 2. There was a significative differ 0.75 at FD5, 1.65 at FD1S, and 1.60 at FD22, ence between the values of the first inflight test relative to 2.32 preflight and 1.9 postflight). (FD5) of subject 1 relative to preflight (t = 5.3, However, these differences between the slopes P < 0.001) or postflight (t = 3.757, P < 0.001) were not statistically significant. values. There was a significant difference be For the relationships between eye peak ve tween in flight values and preflight (t = 5.1S, locit and saccade am . de the be fittin P < 0.001) and postflight values (t = 4.23, was obtained by using an exponential law . In P < 0.001) for subject 2. microgravity, the relationship between saccade peak velocity and saccade amplitude still fol Main sequence. We have plotted the relation lowed an exponential law (Figure 3, panel b ship between saccade duration and saccade for subject 2 and Figure 4, panel b for subject amplitude in Figure 3, panel a for subject 2. 1) with the well-documented saturation of From the raw data, we calculated the best re peak velocities above 20° saccade amplitude lation between D (duration) and A (amplitude) (for a review, see reference 11). However, we by fitting different types of regression. The observed an upward shift of the curves, which best values were obtained by using a linear re corresponded to an increased peak velocity rel gression: D = b x A + a. During the flight, ative to saccade amplitude for both cosmo the relation was always linear, but the slope nauts. In subject 1, the upward shift of the for subject 2 was lower inflight (D = 2.0S x curve was progressively larger throughout the A +45.6) than preflight (D=2.62 xA +4S.2). flight duration. In both subjects, there was a

DURA TIONI AMPLITUDE EYE PEAK VELOCITY I AMPLITUDE DCms) Ep Cde9/sec) D 500 Ep '. 130 ./ / . . 400 110

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Figure 3. Main sequence relations for horizontal saccades in head fixed conditions in subject 2. (a) Eye sac cade duration (D) Is plotted versus eye saccade amplitude (A). The linear regression has been obtained from raw data in each condition (as shown in the inserted plot). The 3 preflight tests are pooled together. (b) Eye peak velocity (Ep) is plotted versus eye saccade amplitude (A). An exponential law has been fitted upon nu merical raw data. The 3 preflight tests are also pooled together. 336 C. Andre-Deshays et al

DURA TIONI AMPLITUDE EYE PEAK VELOCITY I AMPLITUDE Ep Cdeg/sec) DCms) 500 3 130 IN 1 2 400 POST 110 PRE PRE POST 300 90 ~2; 70J /~ " 200 5C // 30 A A -+I, -----"T-----"T------rl (deg) I I (deg) o 10 20 30 20 30 (a) (b)

Figure 4. Main sequence relations for horizontal saccades in head fixed conditions in subject 1. (a) Eye sac cade duration (D) versus eye saccade amplitude (A). The 3 preflight tests are pooled; inflight 1 curve is for FD + 5; inflight 2, FD + 18; infllght 3, FD + 20; the 3 postflight tests are pooled. (b) Eye peak velocity (Ep) versus eye saccade amplitude (A).

return towards preflight values after the flight. saccade by an average value of about 40 to These data suggest a decrease of duration and 70 ms on Earth in control subjects and cosmo a greater peak velocity inflight compared with nauts. This timing remained unchanged in preflight or postflight, but without statistical flight for both subjects, with the eye leading significance. the head by 60 ms ± 26 ms for subject 1 and 74 ms ± 32 ms for subject 2, in the horizontal Vertical saccades plane. In Figure 5, panel a is shown a visually The analysis of vertical sequences was dis- guided orienting movement with head free, turbed by numerous blinks and EOG lid arte- obtained in flight in subject 1. After comple facts at the end of these rapid eye movements. tion of the gaze saccade, the eye position in The available data were too poor to give reli- head continued to change because of a com able quantitative results about accuracy and pensatory movement induced by the vestibulo main sequence relationships, but we can con- ocular reflex (VOR) (12). This gaze, eye, and ~ ______~mm~~~~~~~nR~~~~imffirn~~~~~~~~wa~~ . sruneinflightas on (172 ± 43 ms for subject 1, n = 3 tests, and 187 ± 49 ms for subject 2, n = 1) as compared At the conclusion of the head saccade, the with preflight values (204 ± 45 ms for subject contribution of the head in the total gaze dis 1 and 220 ± 50 ms for subject 2) and with post placement was about 45070 to 60010 in preflight flight values (201 ± 43 ms for subject 1 and conditions (Figure 5, panel b). In micrograv 197 ± 46 ms for subject 2). ity, for both subjects, the head contribution decreased to 30010. Eye eccentricity in the orbit was therefore about 70070 of target eccentric Head Free Condition ity (about 20° for 30° jumps). The differences in eye or head contribution to overall gaze dis When the head of the subject was free, gaze placement between in flight and ground data shifts were composed of an ocular saccade and did not reach statistical significance. For both a head movement. The head tended to lag the subjects, this tendency towards an increased Gaze Control in Microgravity 1 337 B GB. E~ .. H--L1.

ORIENT ATION

SUBJECT 1 100% ~ ~ !§§ ~ A 80% ~ ~ ~ 60% ~~ ~ T 0° h I I 40% - r- r- - 20% - ~ l"'- i---