Modifications of gain asymmetry and beating field of vertical optokinetic nystagmus in microgravity

Neuro~t~ence Letter~, 63 (1986) 271 274

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Elsewer Soentlfic Pubhshers Ireland Lid NSL 03756 M O D I F I C A T I O N S OF GAIN A S Y M M E T R Y AND BEATING FIELD OF V E R T I C A L O P T O K I N E T I C N Y S T A G M U S IN M I C R O G R A V I T Y

G CLEMENT, T VIEVILLE, F LESTIENNE and A BERTHOZ Laboratotre de Phy~lologte Neurosensorwlle du C N R S , 15, rue tie l'Et ole de Mbdeeme, F-75270 Parl~ Cede x 06 ( France )

(Recelvcd October 10th, 1985, Revised version received November 7th, 1985, Accepted November 8Ih, 1985)

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Optoklnetlc nystagmus (OKN) was measured in human subjects before, during and after exposure to mlcrogravlty induced by either parabohc flight or space flight The downward (slow phase up) OKN gain was greater than upward gain m normal grawty On first exposure to mlcrogravlty th~s asymmetry was reversed In addition, the beating field of OKN tended to shift downward, and the vertical optokmetlc after nystagmus (OKAN) time constant was increased This reversed asymmetry disappeared after 3 days of space flight On return to 1 g gravity, there was a general drift of the eye m the upward &rectlon during either spontaneous eye movements or OKN This suggests that the sacculus normally influencesmean vertical cye pos~t~onand the perception of the subjective horizontal direction, both of which are gravity dependent It is currently t h o u g h t that the o t o h t h s of the vestibular organs exert an influence on VlSUO-motor f u n c t i o n a n d particularly on optokinetlc n y s t a g m u s ( O K N ) , Evidence for this fact stems from lesion experiments in the m o n k e y which show that m a c u l a r lesion induces an e n h a n c e m e n t of O K N slow phase in both directions [4, 5, 8], a n d that uvula a n d n o d u l u s lesion (structures k n o w n to relay otohthlc influence) modifies optoklnetic after nystagrnus ( O K A N ) [10]_ In addition, although the gain of the otolith-ocular reflex in the h o r i z o n t a l plane is very small, a strong effect of d y n a m i c otohthlc s t i m u l a t i o n by linear acceleration has been d e m o n s t r a t e d on the slow phase o f O K N [l] Lastly, it is k n o w n that there is a n a s y m m e t r y of upward and d o w n w a r d O K N which has been a t t r i b u t e d to a potential action of gravity [6] However, all these o b s e r v a t i o n s are hmited because of the difficulty of applying a simple linear acceleration on earth where the gravitational field is present a n d introduces a p e r m a n e n t bias M l c r o g r a v l t y induced by parabolic or space flight is an elegant way to suppress the gravity vector selectively We have used this c o n d i t i o n to study the influence of gravity o n O K N . M o n o c u l a r h o r i z o n t a l a n d vertical optokinetlc s t i m u l a t i o n was p r o d u c e d by a portable b a t t e r y - o p e r a t e d s t i m u l a t o r made of a simple belt on which was presented a checkerboard p a t t e r n (each square s u b t e n d i n g 5 ' of visual angle) driven by a D C battery-operated m o t o r This belt was placed inside a small box (10 cm x 9 cm × 8 cm) fixed to a pair of goggles_ The p a t t e r n was viewed t h r o u g h d o u b l e Fresnel lens Pat-

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tern velocity was 20' and 53 /s measured at the center of the screen It was illuminated with red light m order to minimize changes in the electrooculogram (EOG) when going to darkness for the measurements of O K A N Eye movements were measured by D C E O G with no detectable couphng between horizontal and vertical electrodes Care was taken to avoid any artefact due to DC drift of the EOG- any conclusions concerning D C bins such as shown In Fig I have been drawn only from records on which controls showed that there was no artefactual drift. Calibration was made before and after each test Experiments were performed on one subject during parabohc flight, yielding 25 s of mlcrogravlty, and on two subjects (P. Baudry and S A1 Saud) during a 7-day space flight aboard the US Shuttle Discovery Each test cons~sted of 40 s of pattern motion In light followed by 20 s of darkness. Tests were performed 30, 5 and 4 days before launch (F--30, F - 5 , F - 4 ) , every day during flight ( F D I to FD7), and within 1 h after landing ( R + 0 ) , and finally 3 and 60 days postflight (R + 3, R + 60) O K N gain was calculated as the ratto of mean eye velocity and pattern velocity between 20 and 40 s after sUmulus onset D a t a analysts shows that the O K N gain does not change sigmficantly for a pattern velocity of 20°/s. However, at 53'/s the horizontal gain was decreased on the first exposure to mtcrograwty. It recovered a normal value after a few days (Fig 1C). The 'beating field' (area of the oculomotor range in which eye movements are made) remained unchanged during the flight by comparison with pre- and postflight measurements The most striking result, how-

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Fig 1 a optokmetic nystagmus in response to a vertical pattern motion directed upward with a velocity of 53 '/s Records show the horizontal (H) and vertical (V) components of eye movements obtamed 30 days before flight ( F - 30), on the first and fifth day of flight (FDI and FD5) and within I h after landing (R-~ 0) B and C gain of optokmetic nystagrnus m the vertical (B) and horizontal (C) dlrecUon for a pattern velocity of 53 '/s Unfilled symbols are data m response to upward (or rightward) moving pattern, filled symbols to downward (or leftward) moving pattern Stars represent results obtained during parabohc fltght

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ever, IS the reversal of asymmetry and the change in beating field observed in the vertical direction A series of samples of the records ts shown on Fig_ 1A. Before flight ( F - 30), when the pattern starts moving upward, slow phases go up, but quick phases bring the beating field downward On F D I , the slow phases are clearly slower, and the eye tends to drift downward On FD5, the gain and the beating field are nearly normal, although the downward drift is present Within 1 h after landing ( R + 0 ) a strong (3 5 /s) drift of the beating field in the upward direction occurs, together with a significant increase in gain Calibration was made by asking the subject to lixate the extremxtles of squares on the lmmobde pattern within the optoklnetic stimulator The subJect who had always made a perfectly stable calibration also had a tendency to drift upward during calibration This upward drive was still present 3 days after flight This suggests a strong perceptual effect similar to the one repeated by Melvlll Jones and Berthoz [7] after adaptation of the vestibulo-ocular reflex and by Gauthler and Robinson [3] after reversing prism adaptation O K N gain measurements (F~g I B) show that before flight the O K N slow phase up had a greater gain for th,s subject This asymmetry is reversed on FD1, as well as during the 25 s of parabolic flight This immediate gain reversal suggests that the asymmetry is due to the action of gravity The reversal disappears after 3 days On return, immediately after landing, there is a small but sigmficant increase m gains, but the asymmetry is back to the initial ,,alue (Fig IB) Thesc results represent the first systematic study of OKN made in m~crograwty Although only one subJect gave stable results, the second subject gave results which are similar We do not exclude the posslblhty that the changes observed here are only wihd for the particular subject, but if they are confirmed in future flights, they lead to several ~mportant conclusions Firstly, the reversal of vertical O K N asymmetry both in parabohc and space flight indicates a clear effect of gravity on this asymmetry Unpublished results by Droulez who studied the effect of head tilt (on earth) on O K N slow phase lead to the same conclusion They confirm the results of Matsuo and Cohen [5] on the monkey Secondly, the fact that there is adaptation after about 3 days, ~s reminiscent of the time necesssary for astronauts to overcome the symptoms of space sickness (although P Baudry did not get sick) and is therefore suggestive of a standard adaptation time for visual-vestibular interaction It also is the time taken for recovery of VOR gain which was decreased In both pitch and yaw rotation axes [9] and for the adaptation of postural asymmetries [2]. Lastly, the large upward drift observed on return IS an indication that central adaptation to remowll of gravity has taken place All these results would be compatible with a general downward drive exerted by the otohths (probably ma,nly the sacculus) on the first exposure to mlcrogravlty and an upward drive on the first day of return The initial downward drive could be explained by hypothesizing that, during free fall, the antigravity tonic Influence exerted by the sacculus, which tends to hft upward both the limbs and the eyeball, in order to compensate for the downward pull by gravity, would be suppressed Conversely, on return, the brain would have adapted and the return to 1 g gravity would be perceived as an upward linear acceleration inducing an upward drive opposing the downward inertial force vector (which is in opposite direction to acceleration)

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This research was supported by grants from Centre National d'Etudes Spattales, Paris Engineering of the experimental equipment was designed by F X. $6n6 and M Ehrette, with the collaboration of P. Simon. We gratefully thank Dr. M. R Reschke, S Wood, J. Hayes for their support, E. Mtchel for his help m accommodatmg the expertment, and above all P Baudry and S. AI-Saud. I Bmzza, A , L6ger, A,, Droulez, J , Berthoz, A and Schmld, R , Influence of otollthlc stimulation by horizontal hnear acceleration on optokmet~c nystagmus and visual motion perception, Exp Brain Res, 39 (1980) 165 176 2 Clement, G , Vl6vllle. T, Lestienne, F and Berthoz, A , Adaptatlve modlficaUons of postural control mechanisms in m~crograwty, m preparation 3 Gauthler, G M and Robinson, D A , Adaptation of the human vesttbulo-ocular reflex to magmfymg lenses, Brain Res, 92 (1975) 331 335 4 Igarashl, M , Takahashl, M . Kubo, T , Levy, J K and Homlck, J.L, Effect of macular ablaUon on vertical optokinetlc nystagmus in the sqmrrel monkey, Oto-Rhlno-Laryngol, 40 (1978) 312-318 5 Matsuo, V and Cohen, B, VertLcal optokmeuc nystagmus and vestibular nystagmus m the monkey Up-down asymmetry and effects of gravity, Exp Brain Res, 53 (1984) 197-216 6 Matsuo, V, Cohen, B, Raphan, T, DeJong, V and Henn, V, Asymmetric velocity storage for upward and downward nystagmus, Brain Res, 176 (1979) 159 164 7 Melvlll Jones, G and Berthoz, A , Mental control of the adaptive process. In A Berthoz and G Melvdl Jones (Eds), Adaptive Mechanisms in Gaze Control Facts and Theories (Reviews of Oculomotor Research, Vol 1), Elsevier, Amsterdam, 1985, pp 203-208 8 TakahashJ, M , Igarashl, M and Homlck, J L , Effect of otohth end organ ablation on horizontal optokmetlc nystagmus in the squirrel monkey, Oto-Rhmo-Laryngol, 39 (1977) 74-81 9 Vi6vdle, T , Cl6ment, G , Lestlenne, F and Berthoz, A., Adaptive modification of the optokmetlc and vestlbulo-ocular reflexes m mlcrograwty In D Zee and T Keller, Adaptive Processes in Visual and Oculomotor Systems, Pergamon, m press 10 Waespe, W , Cohen, B and Raphan, T , Dynamic modification of the vestlbulo-ocular reflex by the nodulus and uvula, Exp Brain Res, m press