Received: 23 August 1995 / Accepted: 6 March 1996
A bstract The possibility of synergistic interaction be tween the canal and otolith components of the horizontal vestibulo-ocular reflex (VOR) was evaluated in human subjects by subtracting the response to pure angular rota tion (AVOR) from the response to combined angular and translational motion (ALVOR) and comparing this differ ence with the VOR to isolated linear motion (LVOR). Assessments were made with target fixation at 60 cm and in darkness. Linear stimuli were acceleration steps attaining 0.25 g in less than 80 ms. To elicit responses to combined translational and angular head movements, the subjects were seated on a Barany chair with the head dis placed forwards 40 cm from the axis of rotation. The chair was accelerated at approximately 300 deg/s^ to 127 deg/s peak angular velocity, the tangential acceleration o f the head being comparable with that of isolated trans lation. Estimates of the contribution of smooth pursuit to responses in the light were made from comparisons of isolated pursuit of similar target trajectories. In the dark the slow phase eye movements evoked by combined ca nal-otolith stimuli were higher in magnitude by approxi mately a third than the sum of those produced by transla tion and rotation alone. In the light, the relative target displacement during isolated linear motion was similar to the difference in relative target displacements during eccentric and centred rotation. However, the gain of the translational component of compensatory eye movement during combined translational and angular motion was approximately unity, in contrast to the gain of the re sponse to isolated linear motion, which was approxi mately a half. Pursuit performance was always poorer
D. Anastasopoulos
Department of Neurology, University of loannina, loannina, Greece
D. Anastasopoulos • C. C. Gianna (E l) • A. M. Bronstein M. A. Gresty
MRC, Human Movement and Balance Unit, Institute of Neurology,
National Hospital for Neurology and Neurosurgery, Queen Square, London W CIN 3BG, UK
Fax: 0171 837 7281, e-mail: [email protected]
than target following during self-motion. The LVOR responses in the light were greater than the sum of the LVOR responses in the dark with pursuit eye movements. We conclude that, in response to transient motion, there is a synergistic enhancement o f the transla tional VOR with concurrent canal stimulation and that the enhancement of the LVOR in the light is not due solely to pursuit.
Key words Vestibulo-ocular reflex ■ Otoliths • Eye movements • Pursuit
Introduction
Visual stability during the high acceleration angular and translational transients which occur during natural head movements (Gresty 1973) is maintained by vigorous ‘vestibular ocular reflex’ (VOR) eye movements, which compensate for both translational and angular compo nents of motion (Gresty and Bronstein 1986; Snyder and King 1992; Viirre et al. 1986). The origin o f the angular VOR (AVOR) is canalicular and the reflex has w ell-es tablished dynamics. It is presumed that compensation for the translational component is of otolithic origin (Young 1972). However, it is not known whether these compen satory eye movements for the translational component of motion are separate otolith ocular reflexes summating with canal responses or originate from a synergistic en hancement of canalicular and otolithic signals (Gresty et al. 1987).
In order to assess these possibilities, the experiments reported here evaluate the interaction o f the LVOR with the AVOR. The translational VOR component in com bined angular and translational motion was estimated by subtracting the response to pure angular rotation (AVOR) from the response to combined angular and translational motion (ALVOR) obtained by rotation with the head off axis. In theory, this difference should be equal to the LVOR, that is to say the response obtained with a matched isolated linear acceleration profile (see “Meth ods”).
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The gain o f the isolated LVOR is lower in the dark (Baloh et al. 1988; Bronstein and Gresty 1988; Buizza et al. 1980; Lichtenberg et al. 1982; Niven et al. 1966) than when enhanced with vision in inverse proportion to tar get viewing distance (Paige 1989; Schwarz et al. 1989). Accordingly the study also compared responses obtained in darkness and with fixation targets for the three condi tions o f motion (AVOR, LVOR, ALVOR).
Compensatory eye movements in the light may have components of smooth pursuit and optokinesis combined with vestibular reflex eye movements. Accordingly we independently assessed pursuit (of a large target) to esti mate how much o f the responses in the light might be driven by visually guided following.
M aterials and methods
The experiment measured responses to linear motion, rotational motion and combined rotational-translational motion using motion transients to enhance the automaticity of responses.
Apparatus and stimuli
Horizontal LVOR
Subjects were seated upright, with head and torso restrained, on a chair mounted on a chassis with four wheels (bogie) running on a linear track and powered by linear induction motors. The stimuli were velocity ramps accelerating the subject to 0.25 g in less than 80 ms (Fig. 1). The bogie reached a velocity of 1.5 m/s at approxi mately 600 ms before slowing down. The stimuli were dispensed unpredictably to the right or to the left.
For each condition, stimuli were first presented in the dark so that the subject would have less provocation to construct ‘imagi nary targets’.
LVOR in the dark
The eyes of the subject first rested on a rectangular matt-grey screen (120 cm xl20 cm) placed at a distance of 1.5 m, before the room lights were extinguished. The blank screen was used to pre vent the subject to fixate any particular point in space which could be taken as a reference point on which to construct an ‘imaginary target’. After 1 s the bogie moved. For each direction, at least five stimuli were dispensed (linear vestibulo-ocular reflex in the dark, LVORd).
LVOR in the light
The subject fixated the centre of an earth-fixed target consisting of a rectangular (79 cm wide, 55 cm high) flat board with black and white vertical stripes situated 60 cm from the eyes of the subject. A near target was chosen with the hope of boosting the otolith-oc ular reflex responses according to the theoretical demand.
Combined translational and angular head movements
The subjects were seated on a Barany chair with the head dis placed forwards 40 cm from the axis of rotation, the head and tor so being firmly fixed to the chair with clamps. The chair was driv en by a velocity servo-controlled, torque motor about a vertical ax is. It was accelerated at approximately 300°/s^ to 127°/s peak an gular velocity for 430 ms in either direction before being deceler
ated. The parameters of chair velocity were chosen to provide a profile of tangential acceleration, acting along the interaural axis, similar to that delivered on the bogie (Figs. 1, 2, third records from the top); the angular velocity was equal to (bogie veloci ty/distance between head and axis of rotation). For a rotation of
a°, a distance head-rotational axis a cm and an earth-fixed target at a+b cm from the rotational axis, the relative target displacement
{RTD) equals; a-i-arctan{asina/[b+asinatan(«/2)]}. The second term of this formula is due to the translational head movements occurring during eccentric rotation, as during centric rotation a=0
and RTD=a. For a=40 cm, 6=60 cm and a=10°, /?7’D=10°+6.54°.
For angles <10°, the RTD simplifies to cr+arctan(aa^aj)/6)
(=10°+6.64°). As angular velocityxa=l inear velocity, arc-
tan(ax«^gj/6) equals arctan(bogie position/6) which is the relative target displacement for pure linear acceleration on the bogie. Therefore, if the eye movements are compensatory for each testing condition, we expect the responses from eccentric rotation to be the sum of the responses evoked during centric rotation and during pure translation. Because of torque limitations, the tangential lin ear acceleration during the combined canal-otolith stimulation was of smaller magnitude for the first 130 ms after the onset of the movement (0.15 g at 80 ms). All measurements were made before 250 ms, at which point the angular velocity was 75°/s and the cen tripetal acceleration 0.69 m/s^.
After the ocular responses to five such stimuli in either direc tion in the dark (ALVORd) had been recorded, the procedure was repeated in the light (ALVORI).
For trials in darkness the subjects previewed the grey screen at 1.5 m, while in the light they fixated the target card at 60-cm dis tances, as for isolated linear motion.
The ocular responses to isolated canal stimulation (AVOR) were obtained with the head of the subject centred on the axis of rotation with the same angular motion stimuli as given with the head eccentric. The same protocol was followed for recording in the dark (AVORd) and in the light (AVORl).
Pursuit
Pursuit was assessed independently by linear motion of the target image, which was back-projected onto a tangent screen facing the stationary subject. The pursuit stimulus (PURS) had the same waveform as the linear vestibular stimulus on the bogie. This was achieved by feeding the mirror galvanometer with the position sig nal of the bogie, transformed to give an identical angular target trajectory: the mirror angular position was equal to arctan(bogie position/distance between mirror and screen). Target characteris tics were identical to those for VOR measurements in the light.
Instructions
Knowledge of target distance and correspondingly vergence were controlled by using constant fixation targets at a constant distance. To control vergence angle for trials in darkness, the subjects’ eyes were initially in primary gaze focused on the grey screen, but no instructions were given to try to track its relative motion when put into darkness. In preliminary experiments, changes of the ver gence angle were measured with a binocular infrared system (Iris, Scalar). The vergence changed within 1 s after the room lights were switched off and thereafter attained a constant phoria which was idiosyncratic for each subject. For trials in the light with a tar get, subjects were instructed to maintain fixation on a central ‘bull’s-eye’ on the target card, which subtended 0.2°.
Eye movement measurements
Lateral eye movements were recorded using bitemporal direct coupled electro-oculography (EOG) with a flat response to 80 Hz. EOG was used because pilot studies with infrared corneal reflec tion oculography showed that the helmet and mask support for the sensors used in this latter device caused slippage and artefacts.
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even with the use of a biteboard, during the sharp onset accelera tion deployed in our study. The duration of the experiment, typi cally 2 h, precluded the use of scleral-coil recordings.
EOG recordings transduced lateral movements as a ‘cyclopean eye’, as separate eye recordings had higher noise levels and drift, which hindered precise measurement. At the beginning and fol lowing each stimulus condition calibrations were made using re fixation saccades of 12° marks about the centre of the target card. The mean of the pre- and post-trial calibrations was used for as sessing the amplitude of eye movements during the trial. Pre- and post-trial calibrations did not vary significantly even for experi ments in the dark. After each stimulus, the bogie was repositioned in the light in front of the grey screen so that subjects were only in darkness for a few seconds at a time and did not dark-adapt.
Stimulus transduction
Tachometer recordings were also taken of the linear velocity of the bogie and of the angular velocity of the Barany chair. The laterally directed translational linear acceleration of the head was trans duced by a precision piezoresistive accelerometer mounted with surgical tape on the forehead. Signals were acquired at 250 Hz sampling rate. Relative target displacement during body motion was obtained by digitally integrating tachometer signals and ap propriate geometrical transformations.
Demands on ocular following imposed by the motion stimuli As measured at 240 ms, pure translational motion resulted in an approximately parabolic target displacement attaining 5°±0.2 SD and a relative angular velocity of 45°/s. Pure angular motion re sulted in a target displacement of 6.6°±0.5 SD and a velocity of 67°/s. Head eccentric angular motion resulted in a target displace ment of 10.7°±0.7 SD and a velocity of 109°/s. The translational component of head eccentric motion was responsible for a target displacement of 4.1 ° at a velocity of 42/s°.
Subjects
Twelve healthy humans (aged 24—48 years) with normal vision and vestibular function gave their informed consent to the study according to the guidelines of the local ethics committee.
Four subjects underwent the studies commencing on the rotat ing chair whilst the remainder commenced on the linear accelera tor. On the angular chair the order of conditions was eccentric,
centred and pursuit as determined by decreasing order of discom
fort. Linear and angular studies were spaced by a rest period of at least 20 min whilst the subjects switched apparatus. No order ef fects were observed.
Results
Responses in the dark
VOR to isolated linear motion
Examples o f raw responses to isolated linear acceleration in darkness are given in Fig. 1. Compensatory, slow phase horizontal eye movements of small amplitude in terrupted by occasional saccades in the opposite direc tion were evoked: such eye movement has been termed ‘1-nystagmus’. (Fig. 1, LVORd). Figure 2 (upper record) shows the mean eye angular displacement for all subjects with 1 SD. The average amplitude of the slow phase eye movements reached 0.7° at 180 ms from stimulus onset. Their velocity increased with time approaching an as ymptote of approximately 10°/s at about 250 ms after stimulus onset (Table 1).
Analysis
For each condition, subjects gave ten responses for each right/left stimulus direction. Traces containing fast phase resettings of dura tion longer than 40 ms during the first 200 ms after the onset of the stimulus were rejected because they were thought to hinder slow phase interpolation, as its velocity was not expected to change linearly with time. Responses associated with blinks were also excluded. The position signal of the eye movement was dif ferentiated, and saccades of less than 40 ms duration were re moved, with interpolation of a straight line between the beginning and the end of the saccade. This resulted in between five and ten data records from each subject for each stimulus. The signals were averaged using the time of onset of the bogie, chair or pursuit stimulus for synchronisation. Leftward and rightward responses were combined, as no asymmetry was observed. The individual averages were pooled together to obtain seven grand averages cor responding to the various experimental conditions. Each grand av erage was derived from approximately 100 trials.
For velocity measurements at a chosen time interval after stim ulus onset, a function was fitted following a least-square method to approximately 20 data points of the slow phase grand average around that time. In most cases a two-order polynomial function gave; a fit with high correlation. The mean of the R values of the estimates of the fittings for the calculation of the instantaneous slow phase eye velocities given in Table 1 was 0.97 (n=12)and that in Table 2, 0.98 (n=14). Substituting the time at the first derivative of this function yielded the instantaneous velocity at the particular time interval.
VOR gains were based on the computation of relative target position or velocity. Thus displacement gains at specified times were; defined as (eye position/relative target displacement). An analogous ratio was used for velocity gains.
VOR to angular and to com bined angular and linear m otion
The eye movement responses to rotation on the Barany chair consisted mainly of a compensatory slow phase, followed after a variable interval o f about 250 ms by a fast phase resetting of eye position (Fig. 1). Averages with 1 SD are shown in Fig. 2, upper records (ALVORd and AVORd). The velocities of compensatory eye move ments evoked with the head eccentric were slightly greater than those evoked with the head centred (Table 1).
The difference between the amplitudes and velocities of the responses with head eccentric and head centred was greater than the amplitudes and velocities of slow phase eye movements obtained on the bogie. This is shown in Fig. 3 (upper records), where the upper trace is the result of subtraction o f the grand average of slow phase eye movements obtained during AVORd from the grand average produced by the desaccaded eye position signal during ALVORd. The lower trace shows the aver age of the slow phase eye movements recorded on the bogie. While the latter would be compensatory for a tar get set at approximately 2.9 m, the slow phase ocular movements obtained during ALVORd would compensate for a target at about 1.6 m.
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Fig. 1 E x a m p les o f raw data sh o w in g angular e y e d isp la c e ment ( u p p e r r e c o r d s ) recorded during pure linear acceleration
( le f t c o lu m n ) , co m b in e d canal- otolith stim ulation ( m i d d le c o l
u m n ), and isolated canal stim u
lation ( r i g h t c o lu m n ) . T he s c h e - m a t i c at the l o p sh o w s the three different stim u li. L V O R d , A L V
O R d and A V O R d are v e stib u lo
ocu lar resp o n ses evok ed in the dark w h ile L V O R l, A L V O R I and
A V O R l are resp o n ses obtained
in the light to linear, co m b in ed angular and linear, and angular m otion , resp ectively. T he u p p e r t r a c e s o f the l o w e r r e c o r d s
sh ow the p rofile o f the linear a cceleration alon g the inter-au ral a x is as recorded from the forehead o f the subject and the
l o w e s t t r a c e s , the b o g ie and chair linear and angular v e lo c i ty resp ectively. S light vibra tions o f the b o g ie and interfer en ce from the linear induction m otors produced the o s c illa tions ob served on raw acceler a tion and e y e m ovem ent records for linear m otion. H ow ever, this interference w as reduced during the averaging p rocess
LVOR d ALVOR d 3 deg ALVOR LVOR 3 deg
III
AVOR d AVOR I 0.25 g 20 deg/s 20 cm /s ' 50 msR esp o n ses in the light
VOR to iso la te d lin ea r m otion
E x am p les o f raw d ata are given in Fig. 1, and the average