Visual-vestibular interaction upon nystagmus slow phase velocity in man.

Acta Otolaryngol85: 397-410, 1978 VISUAGVESTIBULAR INTERACTION UPON NYSTAGMUS SLOW PHASE VELOCITY IN MAN E. Koenig,' J. H. J. Allum2 and J. Dichgans' From the Neurological Clinic, University of Freiburg, Freiburg irn Breisgau, BRD

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(Received August 18, 1977)

Abstract. The influence of vestibular and visual (optokinetic) stimuli on the nystagmus slow phase velocity (SPV) in man was studied using different combinations of visual horizon and/or passive body rotations (velocity trapezoids). The interactions of combined stimulation were evaluated in comparison to pure optokinetic and pure vestibular reactions. The results indicate that retinal image stabilization and vestibular systems simultaneously activate ocular reflexes during passive body accelerations in the light. Results: 1. Exclusive vestibular stimulation by passive body rotation in the dark yields a rather low gain of the vestibulo-ocular reflex (VOR) with respect to acceleration. 2. With optokinetic stimulation the gain depends on pattern velocity. It is close to unity at velocities below 30"lsec and progressively decreases with increasing pattern velocity. 3. During passive body rotation in the light (a concomitant visual and vestibular stimulation occurs) the form of the response profile suggests that both visual and vestibular inputs contribute to the response. Compared with pure optokinetic stimulation this results in a better correspondence of the SPV and stimulus velocity at higher accelerations and velocities. 4. When subjects viewed a surround rotating with constant relative velocity, the amount of enhancement or depression of SPV by the additional application of passive body rotation increased with the body acceleration and with surround velocity. With small surround velocities and high enhancing body accelerations the SPV may be faster than the relative surround velocity. Depressing vestibular stimuli cause a greater SPV modulation than enhancing of the stimuli sometimes even reversing the direction of nystagmus. The results indicate an interaction between optokinetic (visual) and vestibular inputs.

(Barr et al., 1976; Morasso et al., in prep.; Dodge et al., 1930; Mackensen, 1954) the question arises as to how the individual gains are adjusted in cases where both channels could be effective at the same time. Interaction between the two reflexes has earlier been demonstrated by a number of authors (Ohm, 1932; Ter Braak, 1936; Jung & Mittermaier, 1939; Jung, 1948; Giittich & Okamoto, 1964) but has never been thoroughly quantified. In this paper we have attempted to quantify the interaction between vestibular and visual (optokinetic) stimuli by examining nystagmus slow phase velocity (SPV) under quasi natural, and artificial conditions, with combinations of mutually enhancing and depressing stimuli, consisting of passive body rotations and visual surround motions. The results indicate that the signals created by the retinal image stabilization and vestibular reflex systems may be combined in a weighted sum by the Central nerVOUS System to produce a single S p v output. This interaction may Serve as a basis for the interpretation of clinical data on optokinetic nystagmus-SPV in patients with spontineous nystagmus due to peripheral vestibular lesions. The following paper (Brandt et al., 1978) presents the clinical data.

Visual (retinal image stabilization) and vestibular reflexes may initiate eye movements as the head is moved freely within a normally lit environment. Since it is known that both

This work was supported by the Deutsche Forschungsgemeinschaft sFB 70 r'Hirnforschung und physiologie"). i Presently at Neurological Clinic, Liebermeisterstr. 18, University of Tubingen. Presently at Institut fur Hirnforschung, - Universitat Zurich.

100Ps, if under Optimal conditions, can work at a gain close to unity

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398 E . Koenig et a / . METHODS


Subjects Four subjects (three male, one female) were selected from a group of 40 students on the basis of their stable slow phase velocity and regular nystagmus frequency in response to constant optokinetic stimulation. They had normal vestibular function and were familiar with our apparatus from previous experiments. Apparatus For the experiments, subjects were seated in a chair which rotated about the axis of a surrounding cylindrical drum, 1.5 m in diameter, the inner walls of which were covered with 48 alternating black and white vertical stripes each subtending 7.5 degrees of visual angle (Tonnies, Freiburg). The moving pattern filled the entire visual field. Both the chair and the drum could be rotated (independently or coupled) at servo-controlled velocities. Constant accelerations which ranged between 3 and 12”/sec2 were applied to either chair or drum, or both. The commanded relative displacement between chair and drum was verified by means of a photocell attached to the chair and placed facing the stripe pattern. Horizontal eye movements were recorded (Jung, 1953) using Beckman silver-silver chloride electrodes. After d.c. amplification, the eye movements and velocity signals from drum and chair were stored on FM magnetic tape for later analysis. Calibrations of eye movements were taken from voluntary saccades (four targets, at 15” and 30” left and right). These were repeated several times during each experiment. Experimental procedure Each subject was seated with his head restrained by a head holder and was asked to attentively pursue the stripe pattern. With pure vestibular stimulation in the dark the eyes were open. The stimuli used are schematically depicted in Fig. 1. They were veActu Otoluryngol85

locity trapezoids each consisting of an initial stationary period, a constant acceleration period (3, 6, 9, 12”/sec2for 10 sec), a constant velocity period (30,60,90, 120”/secfor 40 sec), a constant deceleration period (3, 6, 9, 12”/ sec2 for 10 sec) and a final stationary period. Stimuli consisted either of ( a ) exclusive chair (body) rotation in the dark (vestibular stimulus), or ( b ) exclusive drum rotation (optokinetic stimulus). Suppression of vestibular nystagmus by the presence of a stationary pattern ( c ) was tested by moving the drum and the chair while they were mechanically coupled together (“fixation suppression”). Vestibular and optokinetic stimulation were combined in a natural way ( d ) by rotating the chair (body) in the light (“natural combination”). The vestibular modulation ( e ) of optokinetic nystagmus (OKN) in response to a constant velocity pattern motion (30, 60, 90, 120”/sec) was studied by the intermittent application of body accelerations and decelerations (3, 6, 9, 12”/sec2),which enhanced or depressed the SPV (“interaction trials”). The combination of four accelerations and four pattern velocities resulted in 16 trials for this experiment. After an initial period of pure optokinetic stimulation (drum rotation) lasting 20 sec, subjects were submitted to a 10 sec period of chair acceleration from rest in the opposite direction while the drum was decelerated at the same rate, thus keeping the optokinetic pattern speed-relative to the subject-constant. Thereafter for 40 sec the chair was rotated at constant speed while the relative velocity between drum and chair remained constant. Then a reverse acceleration of chair and drum was applied to reach the original velocity levels. The sequence of the trials was reversed for 2 of the 4 subjects. Data analysis The eye movements, recorded on tape, were analog to digital converted every 10 msec, stored on digital computer disks and analysed with a modified Fortran version of the computer program MITNYS I1 (Allum et al.,


Visual-vestibular interaction upon nystagmus slow phase velocity 399

e.

Fig. 1. Stimulus combinations of experiments a-e and the corresponding typical SPV-responses (schema).

1975). The program automatically computed for every 10 msec sample the slow phase velocity of nystagmus and the consecutive 2 sec average of SPV. The program used a linear calibration rather than a cubic or sinusoidal calibration, based on the voluntary saccades executed between targets at 0", 15" and 30" to right and left. Because of the limited storage capacity of the computer (8K IBM 1130) only 38 sec could be analysed at one time. Thus, ac-

celeration and deceleration periods had to be processed separately. Digital plots presented the original nystagmus together with the slow phase velocity time history. The values of 2 sec SPV averages employed for this paper were taken from the computer printouts. These values were used for the computation of the average maximum and minimum SPV of our 4 subjects. For computations concerning the average time history of SPV the computer Acta Otolaryngol85


400 E. Koenig et al.

-"I

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Fig. 2 . Time-course of SPV during pure vestibular stimulation ( 0 )and during natural combination of vestibular

and optokinetic stimulation (0)at different accelerations and corresponding plateau velocities.

2 sec average values were linearly interpolated with respect to acceleration or deceleration onset.

chair ( 3 , 6 , 9 , 12"/sec2)caused an increase in SPV of 1.2, 2.2, 2.9 and 4.0 degrees/sec2, respectively. The ratios between the corresponding values were employed as a measure of vestibulo-ocular reflex gain (0.41, 0.37, 0.32, 0.34). When the decay effect of the vestibulo-ocular reflex long time constant is accounted for, the true acceleration gain is 35 % greater than the value obtained by linear regression techniques. The decay can be observed after the end of acceleration but of course it is effective during the acceleration period too. Maximum SPV (Fig. 4) is reached at an average of 1 . 1 sec after the end of acceleration. This latency of the maximum SPV tended to decrease with increasing accelerations. The decline in SPV during steady chair rotation was fitted by a single exponential function which has an associated average time constant of 15.2 sec (S.D.=7.2). Deceleration of the chair elicited a nystagmic response in the opposite direction which was symmetrical to the response during the acceleration period.

RESULTS Pure vestibular stimulation Velocity trapezoids of body rotation in the dark (Fig. l a ) caused per- and post-rotatory vestibular nystagmus, the average time course of which is depicted in Fig. 2. Fig. 3 a shows a representative original recording with the corresponding computer plot. The increase of SPV during the 10 sec acceleration period is well fitted by a straight line (average coefficient of determination ( r 2 ) is 0.92; standard deviation (S.D.)=O. 15). With pure vestibular stimulation, the SPV always progressively lagged behind the increasing chair velocity as the vestibulo-ocular reflex (VOR) long time constant became more effective. The vestibular response latency was included in the regression calculations. The accelerations of the Actn Otolnryngol8.5

Visual-vestibular interaction upon nystagmus slow phase velocity 401 fig 3a

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of a stationary surrounding pattern, ( d ) acceleration and ( e ) deceleration phase during body rotation in the light (natural combination, note reversal of nystagmus by vestibular stimulus). Actu Otolaryngol85


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Fig. 4 . Averages of the four subjects for maximum SPV at the end of body acceleration in light (0),average optokinetic SPV during constant velocity pure optokinetic stimulation (D), averages of maximum SPV during pure vestibular stimulation by body rotation in the dark ( O ) , and averages of maximum SPV during the fixation suppression experiment (A).

Pure optokinetic stimulation With full field optokinetic stimulation elicited by rotating the striped drum around the subject (Fig. lb), SPV closely matched stimulus speed up to 30°/sec, for all accelerations tested except 12"/sec2.The gains for the SPV during the acceleration period were 0.78, 0.63, 0.68, 0.67. Periods at the end of the acceleration, where the SPV had saturated for higher pattern velocities, were excluded from the regression calculations. At higher pattern velocities, the SPV was progressively less than the stimulus speed. The maximal steady state SPV was reached at a pattern velocity of approximately 90"/sec and decreased at higher speeds (Fig. 4). It showed considerable interindividual variability (range 52-7l"lsec for 90"lsec stimulus, among our subjects). The maximum OKN-gain (maximum values of SPV divided Acta Otolaryngol85

by stimulus speed) decreased from unity at speeds of 30"lsec to a value of 0.5 at 120"/sec. The velocity gain (average values 0.91, 0.72, 0.63, 0.43 for 30, 60,90, 120"/sec respectively) was maintained throughout the constant velocity period. Maximum SPV of the individual trials was normally reached after the termination of the acceleration. Some waxing and waning of the SPV occurred during the constant velocity period (Fig. 3b). The standard deviation associated with this variability amounted to 6.6, 4.4, 5.8, 7.9% of the individual average SPV, respectively, for the,four stimulus velocities tested. During the deceleration phase, the SPV remained at the level acquired during constant velocity stimulation and only decreased when the stimulus speed was close to the level of the SPV. Once the SPV decreased, its gain during the deceleration period was 0.96, 0.82, 0.87, 0.85 (in order of increasing deceleration), thus being greater than the acceleration gains. Vestibular stimulation in the presence of a staionary optokinetic pattern fixation suppression) When chair and drum mechanically coupled together are accelerated at the same rate (Fig. l c ) the use of the retinal stabilization of the striped pattern which is stationary with respect to the chair dramatically decreased the nystagmus response caused by the vestibular stimulus. The effects of suppression lead to a highly variable maximum SPV which amounts, on average, to 13 % of the maximum SPV during pure vestibular stimulation. The variability of the SPV hampered any assessment of SPV decay time constants. For the accelerations we used, stable fixation in some cases could be recovered before or just after the end of the acceleration period, but in others nystagmus also persisted up to 20 sec after the end of acceleration. An original recording of a particularly pronounced nystagmus elicited by a body acceleration of 9"/sec2in the presence of a stationary pattern is shown in Fig. 3 c.

Visual-vestibular interaction upon nystagmus slow phase velocity 403 l2OYsec constant Wtdrinetic stimulation with 1 2 % enhancing ~ ~ vestibular stimulation

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Fig. 5 . Original recording of nystagmus and corresponding computer plots during a 12Oo/secconstant velocity optokinetic stimulation combined with ( a ) 12"/sec2 enhancing,

and ( b ) 120/sec2 depressing vestibular stimulation (note the increase in SPV and frequency of nystagmus in ( a ) and the reversal of nystagmus in ( b ) .

Natural combination of vestibular and optokinetic stimulation When velocity trapezoids are applied to subjects seated in a rotating chair while the illuminated drum is kept stationary (Fig. I d ) , vestibular and optokinetic stimuli are combined in a quasi-natural way (Fig. 3 4 . The gains of the SPV during the acceleration period (0.72, 0.64, 0.74, and 0.73) did not differ significantly from those obtained by optokinetic stimulation (excluding saturation effects). The average gain factors with respect to stimulus velocity, as calculated from the maximum SPV are 0.99, 0.80, 0.76, and 0.66 for the four velocities tested. Thus increasing vestibular stimulation results in a better transient response for all velocities compared with optokinetic stimulation. Nonetheless, the maximum SPV gain factors were less than one

would have expected from the sum of the corresponding individual gains for optokinetic and pure vestibular stimulation. The maximum SPV (2 sec average value) as for pure vestibular stimulation, was reached after termination of the acceleration period. The delay between acceleration and the maximum SPV decreased with increasing acceleration (5.6 sec, S.D. 1.6; 3.0 sec, S.D. 1.9; 0.4 sec, S.D. 0.9; 0.3, S.D. 1.0 for the four accelerations 3-1 2"/sec2 and the corresponding velocities 30-12Oo/sec tested). After its peak, the SPV decayed to an average plateau which, 23 sec after the end of acceleration, had a velocity gain of 0.72, 0.68, 0.53, and 0.40. The difference with respect to the optokinetic gain measured at the same time is not statistically significant. The time constant of the single exponential fit to the decay (11.6

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Fig. 6. Comparison of obtained and predicted maximum and minimum SPV values elicited by additional vestibular stimulation during constant velocity pattern motion. The SPV obtained with the combination of each pattern velocity and each acceleration is represented by 2 values marked by identical symbols. The value further on the right hand side for any given stimulus velocity shows the

experimentally obtained SPV. The experimentally obtained values are connected by lines. The value further on the left shows the SPV predicted on the basis of the formula given in the algebraic summation hypothesis. The amount of SPV modulation can be obtained by comparing the maximum and minimum SPV values with the SPV before acceleration onset.

sec, S.D. 7.7) is not significantly less than the time constant obtained for body rotation in the dark. With the onset of deceleration, the vestibular component of the stimulus immediately depressed the SPV even though the relative motion of the optokinetic pattern, on the basis of the OKN deceleration response, would tend to maintain SPV at the plateau level (Fig. 2). The decrease of the SPV (-2.2, -3.6, -4.8, - 5 .9"/sec2)during deceleration, however, was more shallow than the increase of the SPV during the acceleration phase (2.2, 3.9, 6.7, 8. lo/sec2). A deceleration of 30/sec2, caused

nystagmus to cease once the rotating chair was at rest. With decelerations equal to or greater than 60/sec2, the direction of nystagmus frequently reversed (Fig. 3 e ) . This was seen in all 4 subjects with a deceleratibn of 12"/sec2. The reversal may even start before the end of the deceleration period. The amount of postrotatory nystagmus differed widely for our subjects. Subjects with high SPV during the constant velocity phase showed no or only little nystagmus reversal at the end of the deceleration phase. With slow SPV prior to deceleration subjects tended to show strong postrotatory nystagmus. A persisting inter-

Visual-vestibular interaction upon nystagmus slow phase velocity 405 tions combined with different pattern velocities. To evaluate the amount of modulation, the mean SPV before acceleration started is also shown. The figure clearly demonstrates that the extent of modulation increases not only with the body acceleration but also with higher pattern velocities, and that, on the average, depressing vestibular stimuli have greater effects than enhancing ones. The maxVestibular stimulation in the presence imum SPV was reached at an average of 1.2 of a constant velocity pattern sec after the end of acceleration, however, this In this group of experiments (Fig. l e ) , after delay varied considerably (S.D. 5.1). Occaeliciting optokinetic nystagmus by rotating the sionally SPV peaked several seconds before striped drum, subjects were accelerated in the the end of acceleration. The minimum SPV for opposite direction. This resulted in an en- depressing stimuli occurred, on average, 3.4 hancement of the SPV, even though the drum sec after acceleration had ended. The single exponential fit of the SPV decay was decelerated at the same rate, thereby keeping constant the relative surround motion after the SPV maximum during depress and and, therefore, the optokinetic stimulus speed enhance trials has an average time constant of (see original recordings in Fig. 5 a ) . On re- 15.9 sec. For the trials using small acceleraversing the procedure by decelerating the sub- tions and small pattern velocities, it was not jects, SPV was depressed (see Fig. 1e ) . Com- possible to assess the time constant, because plete suppression of OKN or even reversal in of spontaneous fluctuations in the SPV from nystagmus direction was observed in 2 of the which a clear acceleration related SPV modusubjects with depressing accelerations of 9 and lation was difficult to discriminate. Because of 12”/sec and pattern velocities of 90 and 120”/ the small difference of this time constant comsec (Fig. 5 b ) . With suitable stimulus condi- pared with that for pure vestibular stimulation tions (30”/sec pattern velocity and 12”/sec2 we concluded that, at least for high acceleravestibular acceleration), enhancement may tions and high pattern speeds, the time course lead to a SPV that over several seconds (aver- of the vestibular modulation of OKN is deterage 7.0, S.D.k4.7) exceeded pattern speed by mined by the dynamics of the vestibulo-ocular a few degrees per second. This overshoot re- reflex. versed the direction of retinal image motion. It is possible for calibration errors in eye moveDISCUSSION ments to cause such small differences. This artifact, however, was excluded as a possible The aim of this study was to determine the cause when 6 additional subjects observed a interactions of two reflex systems, the optoretinal after-image motion faster than the pat- kinetic’(retina1 image stabilization) system and tern velocity. Normal optokinetic stimulation the vestibulo-ocular reflex (VOR) which conyields an after-image motion slower than the verge to produce nystagmus as a common response. The experimental conditions were stimulus velocity. Both the rate of change in SPV during the arranged to activate either reflex alone or both acceleration phase and the maximum SPV in- together. The data from the pure vestibular creased with vestibular acceleration rate and and the pure optokinetic trials served as a the optokinetic pattern velocity. Fig. 6 shows basis for the evaluation of the trials, where the averages for the maximum and minimum both reflexes interact. The results of the vestibular stimulation by SPV for different accelerations and decelera-


action between the optokinetic and vestibular system became apparent after the chair had come to rest. During this period the reversed nystagmus decayed to zero velocity with an average time constant of 6.7 sec (S.D. 1.0) which is shorter than the vestibule-ocular reflex time constant as determined by body rotation in the dark.

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406 E . Koenig et al. passive body rotation in the dark are in agree- suppression that is weakest above 1 Hz when ment with the findings of Brown & Crampton the VOR frequency response increases (Barr (1964). The gain obtained with trapezoid ve- et al., 1976; Benson, 1970) and the optokinetic locity profiles does not differ significantly frequency response decreases (Fender & Nye, from gain values (0.4-0.6) obtained when sub- 1961; Yasui, 1974). jects are rotated sinusoidally in the dark at a frequency of 0.1 Hz (Meiry, 1971; Sugie & Natural combination and interaction trials Melvill Jones, 1971; Barr et al., 1976). All In the natural combination experiments and in these studies, including ours, indicate a low the interaction trials the VOR and the retinal gain for the passive VOR at low frequencies. image stabilization reflex are both activated. In contrast, the passive VOR gain rises to Three possibilities of how both reflexes, when unity for high frequency rotation of 3 Hz (Ben- active at the same time, could contribute to the son, 1970) or sharp transients (Barr et al., nystagmus response have to be taken into ac1976). Thus the low value of the VOR obtained count: a switching mechanism, a weighted with passive head movements may not be a summation, or an algebraic summation. Switching Hypothesis. The switching hypofunctional deficit unless active head rotations have significant components at low frequen- thesis (Waespe & Henn, 1977) assumes that cies. The dependency of the optokinetic nys- either the visual or the vestibular input is tagmus gain upon pattern velocity found in the causing the SPV, the activity from the other pure optokinetic experiments agrees with ear- input being suppressed. From the SPV relier findings of Griittner (1939), Mackensen sponse observed in the natural combination (1954), Honrubia et al. (1968) and Dichgans et experiment we conclude that a switching canal. (1973). An increasing mismatch between not be the underlying mechanism. The higher stimulus and eye velocities appears in a similar gains during the acceleration phase compared range for pursuit-movements (Dodge et al., with pure vestibular stimulation suggest a 1930). This correspondence between opto- contribution of the visual input. Also, SPV at kinetic and pursuit systems, apparent in the the end of body accelerations in the natural similar frequency responses and latencies to combination experiment is faster than that obsudden changes in stimulus velocity, has been served for pure optokinetic stimulation. The emphasised by Yasui (1974). decline of SPV after the end of acceleration in the natural combination experiments occurs VOR-suppression” with a time constant similar to the vestibular Our results, for conditions when the visual decay and indicates that the vestibular input surround rotates with the subject, show that contributed to the response. A further arguthe VOR-SPV response is not simply cancelled ment against the switching hypothesis is given by the presence of a stationary pattern. The ir- by the vestibularly induced modulation of regularity of the response suggests that the SPV in the “interaction trials” which should degree of suppression is dependent on the at- be absent if a switching mechanism were actention paid to the stationary contrasts. Our tive. The observed SPV-profiles can be exexperiments with a stereotyped visual sur- plained on the basis of the two other hyporound, with numerous equal contrasts possibly theses which suggest different concepts of being fixated on, are not identical with experi- how sensory signals are combined at prements using one small fixation mark. Our ves- motor structures to produce a single SPV outtibular stimulus is not to be compared with put. Weighted Summation. During body acrepetitive sinusoidal rotations because of their higher predictability. Experiments with sinus- celeration in the presence of a stationary visual oidal stimulation show a much better VOR surround retinal image stabilization reflexes “

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Visual-vestibular interaction upon nystagmus slow phase velocity 407 and VOR are simultaneously active. With this kind of combined stimulation the question arises as to the input controlling the retinal image stabilization reflex. In contrast with the algebraic summation hypothesis discussed later, the weighted summation hypothesis assumes that the input controlling the optokinetic contribution of the retinal image stabilization reflex is proportional to surround velocity. Testing this assumption by adding the SPV's obtained during separate optokinetic and vestibular stimulation shows that the effects of the combined stimulation are not purely additive, especially during acceleration phases when the added gains for separate stimulation are, on the average, 47% greater than the combined stimulation gains. One explanation for the observed effects could be that a gain modification of either one or both reflex signals occurs before they are combined, i.e. a weighted summation, so that a SPV exceeding the stimulus speed is prevented. A similar non-additive result for the SPV has been observed in a non-foveate animal, the rabbit, using sinusoidal stimulation (Baarsma & Collewijn, 1974). The scaling down of the vestibular input could be elicited by the presence of retinal error, whereas the optokinetic input to the SPV could be reduced by the presence of body rotation. From the natural combination experiments one may conclude that the reduction of the optokinetic gain induced by the vestibular stimulus is relatively minor. In these experiments the SPV at constant velocity body rotation progressively decreases with ceasing vestibular excitation to equal the SPV during pure optokinetic stimulation. On examining the results for interaction trials (Fig. 6) an idea can be obtained of how the vestibular weighting factors may change with stimulus magnitude. As relative stripe velocity is increased, the vestibular weighting factor for the same vestibular stimulation would increase, i.e. the optokinetic input would influence the vestibular gain weighting. The advantage of the increase in the weight-

ing factors with stimulus magnitude is apparent from the body rotation in the light trials. With separate stimulation the gain of each reflex tends to decrease with stimulus acceleration. If, however, the weighting factor of each reflex in the weighted summation on combined stimulation were to increase with stimulus magnitude, the effect of gain decrease on the separate reflexes would be minimized and a more linear response result. In fact, acceleration gains in the natural combination experiments are constant throughout the accelerations tested. The question arises as to whether retinal error velocity alone is the controlling input to the optokinetic component of the SPV during natural stimulation and the interaction trials. Two of our results indicate that this is probably not the case. Firstly, the enhancement and depression of SPV occurs for periods of several seconds during the interaction trials. Secondly, the time constant associated with the decay of SPV during the natural stimulation constant velocity period is close to that corresponding to pure vestibular stimulation. A priori, one would have expected the retinal image stabilization reflex, from its known response latency to error velocity (Rashbass, 1961; Robinson, 1965), to have compensated for the retinal error after its latency (100-200 msec) in these two experiments. These results, however, can be explained if one assumes that surround velocity is represented in the central nervous system and is controlling the optokinetic contribution to the SPV. This representation would consist of a positive feedback of eye velocity added to the retinal error velocity signal. In this case one should assume that the steady state gain of the eye velocity signal and the retinal error velocity signal when summed are less than unity, thus explaining the reduced pursuit tracking ability above 25 to 30"/sec (Young, 1971). With the representation of surround velocity in the central nervous system as an input to SPV, the mechanism of enhancement and depression of SPV for the interaction trials can Acfu Otoluryngol85


408 E. Koenig et al. be explained. For the enhancement trials the vestibular signal together with the positive feedback of eye velocity seems to override any correcting influence of the retinal error velocity signal. The overshoot of eye velocity continued for as long as the vestibular signal reinforced by positive feedback exists. The enhancement is greater with increasing optokinetic stimulation magnitudes because of the increase in the weighting factors of the vestibular reflex contributing to the total SPV response. Similarly for the depression of SPV by the vestibular stimulation the effect of positive eye velocity feedback maintains the depression. The eye velocity signal and the vestibular signal are greater than the correcting signal proportional to retinal error velocity. Algebraic Summation. At the onset of the natural combination experiments the vestibularly induced SPV is thought to decrease retinal slip and thereby the optokinetic input after a short latency of a few milliseconds, before eye movements on the basis of the optokinetic stimulation have been elicited (latency 100-200 msec, Robinson, 1965). This leads to the assumption that the optokinetic input might be the difference between surround velocity and a vestibularly induced SPV component. The vestibularly induced SPV component is assumed to be identical with the SPV response to pure vestibular stimulation in the dark by the respective chair acceleration. On the basis of these assumptions the SPV during the combined vestibular and optokinetic trials was predicted from the SPV observed during separate optokinetic and vestibular stimulation using the following formula:

D =drum velocity C =chair velocity

D-C=optokinetic surround velocity, i.e. drum vel. -chair vel. g, =gain during pure vestibular stimulation g,C=SPV during pure vestibular stimulation= vestibular component Actu Otolarynjiol8.5

(D-C)-g,C=effective optokinetic input, i.e. stimulus velocity minus VOR induced SPV go=velocity dependent gain as determined during pure optokinetic stimulation go((D-C)-g,C)=OKN component of SPV as expected from the effective optokinetic input on the basis of the velocity dependent gain observed during pure optokinetic stimulation g ,,((D-C) -g, C)+g, C =predicted SPV, i.e. summation of the optokinetic and the vestibular component. For the trials with vestibular decelerations the signs for the vestibular component had to be reversed. The predicted maximum SPV (average for our 4 subjects) in the natural combination experiments are 28.4, 51.8,71.2 and 89.4"/sec for the four accelerations and velocities. To compare them with the observed maximum values (29.5, 48.5, 68.6, 78.7) we used the ratios (observed value/predicted value) which are 1.04, 0.93, 0.96, 0.88. Although the optokinetic stimulation preceded the vestibular stimulation in the "interaction trials" the same method of predicting the maximum SPV from separate vestibular and optokinetic stimulation was used because the retinal image motion was also changed in these experiments by the vestibular stimulus. Fig. 6 compares the observed SPV values to the expected maxima. For enhancing stimulation the observed values are on the average 0.6"/sec higher than the expected values. Of particular interest is the finding of a SPV faster than the stimulus when a 12"/sec2 vestibular acceleration was combined with a 30"/ sec pattern motion. A priori one would have assumed that the reversed retinal image motion, elicited by the SPV faster than the pattern motion, should have decreased the SPV via the optokinetic input after a latency of about 100-200 msec. The reason for the observed overshoot of SPV over the stimulus speed for several seconds could be long-lasting effects of the preceding optokinetic stimulus


Visual-vestibular interaction upon nystagmus slow phase velocity 409

that summed with the VOR. Such long-lasting effects have been demonstrated by Ohm (1921), Mackensen et al. (1961), Brandt et al. (1974), Cohen et al. (1977) as optokinetic afternystagmus (OKAN). A tonic modulation of the vestibular neurons discharge rate that outlasts the visual stimulus may be the neurophysiological basis (Dichgans & Brandt, 1972; Dichgans et al., 1973; Henn et al., 1974; Allum et al., 1977) for these phenomena. In trials with depressing vestibular stimulation the hypothesis assumes that the vestibular stimulus elicits a hypothetical SPV opposite to the optokinetic SPV. Thereby the difference between the vestibular SPV and the optokinetic pattern velocity becomes greater than the actual pattern velocity. Thus the OKN gain is decreased because of its velocity dependency. Nevertheless the observed minimum SPV values are on the average 7.2"/sec slower than the predicted SPV (Fig. 6). A possible explanation could be that a storage mechanism in the brain stem, the activity of which gives rise to optokinetic afternystagmus and is necessary for a high SPV of OKN with high pattern velocities (Cohn et al., 1973), is discharged by the vestibular stimulus to the opposite side. The indirect effect of the discharge of this OKAN-storage mechanism on OKN-SPV, combined with the direct effect of the vestibular stimulus to the opposite side, could account for the strong inhibition we observed. Our experiments may be the basis for the understanding of clinical data on OKN abnormalities in patients with vestibular lesions. These data will be discussed in the subsequent paper by Brandt et al. (1977). ACKNOWLEDGEMENT We thank Mrs U. Rommelt for Assistance with graphics.

ZUSAMMENFASSUNG Der Einfluss vestibularer Beschleunigungsreize auf die Geschwindigkeit der langsamen Phase (SPV) des optokinetischen Nystagmus (OKN) wurde mit verschiedenen

Kombinationen von Umwelt- und passiven Korperrotationen untersucht. Zum Vergleich dienten rein vestibularer und rein optokinetischer Nystagmus. Ergebnisse: 1) Wahrend rein vestibularer Reizung im Dunkeln ergab sich ein Verstarkungsfaktor 0 , 3 4 , 4 fur den vestibulookularen Reflex im Verhaltnis zur Beschleunigung. 2 ) Wahrend rein optokinetischer Reizung hangt der Verstarkungsfaktor von der Reizmustergeschwindigkeit ab. Bis zu Geschwindigkeiten von 30"/sec ist er nahezu I und nimmt dann mit zunehmender Reizmustergeschwindigkeit ab. 3) Wurde die Versuchsperson im Hellen bei stationarem Horizont beschleunigt (naturliche Kombination vestibularer und optokinetischer Reize), so fiihrte die zusatzliche vestibulare Reizung bei hohen Reizmustergeschwindigkeiten im Vergleich zu der unter 2 beschriebenen Versuchsanordnung zu einer schnelleren SPV und damit zu einer besseren Ubereinstimmung zwischen SPV und Mustergeschwindigkeit. 4) Bei konstanter optokinetischer Reizmustergeschwindigkeit nahm die SPV-Modulation durch intermittierende zusatzliche vestibulare Reize mit der Starke der Beschleunigung und fur zunehmende Reizmustergeschwindigkeiten zu. Bei niedrigen Reizmustergeschwindigkeiten fiihrten starke Beschleunigungen dazu, dass die SPV fur mehrere Sekunden die Reizmustergeschwindigkeit uberstieg. Den OKN hemmende vestibulare Reize verursachten eine starkere Modulation der SPV als aktivierende Reize. Hemmende Reize konnten den OKN unterdriicken und voriibergehend einen vestibularen Nystagmus in Gegenrichtung auslosen. Die Ergebnisse lassen auf eine Interaktion von optokinetischen (visuellen) und vestibularen Einflussen schliessen.

REFERENCES Allum, J. H. J., Graf, W., Dichgans, J . & Schmidt, C. L. 1977. Visual-vestibular interactions in the vestibular nuclei of the goldfish. Exp Brain Res 26, 463. Allum, J. H. J., Tole, R. & Weiss, A. D. 1975. MITNYS: a digital program for on-line analysis of nystagmus. IEEE Trans on Biomedical Engineering 22, 3, 196. Baarsma, E . A. & Collewijn, H. 1974. Vestibulo-ocular and optokinetic reactions to rotation and their interaction in the rabbit. JPhysiol (Lond)238, 603. Barr, C. C., Schultheis, L . W. & Robinson, D. A. 1976. Voluntary, non-visual control of the human vestibularocular reflex. Acia Otolaryngol (Stockh) 81, 365. Benson, A. J. 1970. Interactions between semicircular canals and graviceptors. In Receni Advances in Aerospace Medicine (ed. D. E. Busby). D. Reidel, Dordrecht. Brandt, Th., Allum, J. H. J. & Dichgans, J. 1978. Computer analysis of optokinetic nystagmus in patients with spontaneous nystagmus of peripheral vestibular origin. Acra Otolaryngol (Stockh) 85, 5-6. Brandt, Th., Dichgans, J. & Biichele, W. 1974. Motion habituation: Inverted self-motion perception and optokinetic after-nystagmus. Exp Brain Res 21, 337. Aclu Otolaryngol85


410 E. Koenig et al. Brown, J . H. & Crampton, G. H. 1964. Quantification of the human nystagmic response to angular acceleration. Prediction formulae and nomograph. Acta Otolaryngol (Stockh) 58, 555. Cohen, B., Matsuo, V. & Raphan, T. 1977. Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic afternystagmus. J Physiol (Lond)2, 1. Cohen, B., Uemura, T. & Takemori, S. 1973. Effects of labyrinthectomy on optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN). Equilibrium R e s 3 , 88. Dichgans, J. & Brandt, Th. 1972. Visual-vestibular interaction and motion perception. In Cerebral Control of Eye Movements and Motion Perception (ed. J. Dichgans & E Bizzi). Bibl. Ophthal., Vol. 82, p. 327. S. Karger, Basel, New York. Dichgans, J., Nauck, B. & Wolpert, E. 1973. The influence of attention, vigilance and stimulus area on optokinetic and vestibular nystagmus and voluntary saccades. In The Oculomotor System and Brain Functions (ed. V. Zikmund). Buttenvorths, London. Dichgans, J., Schmidt, C. L. & Graf, W. 1973. Visual input improves the speedometer functions of the vestibular nuclei in goldfish. Exp Brain Res 28, 3 19. Dodge, R., Travis, R. C. & Fox, J. C. 1930. Optic nystagmus. 111. Characteristics of the slow phase. Arch Neurol Psychiat (Chic)24, 21. Fender, D. H. & Nye, P. W. 1961. An investigation of the mechanisms of eye movement control. Kybernetik 2 , 81. Griittner, R. 1939. Experimentelle Untersuchungen iiber den optokinetischen Nystagmus. Z . Sinnesphysiol 68, 1. Giittich, H. & Okamoto, K. 1964. Kombinierte thermischoptokinetische Priifung bei Normalpersonen und optokinetischer Nystagmus bei einseitigem Labyrinthausfall. HNO Wegweiser 12, 251. Henn, V . , Young, L. R. & Finley, C. 1974. Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brain Res 71, 144. Honrubia, V., Doeney, D. P., Mitchell, B. A. & Ward, P. H. 1968. Experimental studies on optokinetic nystagmus. 11. Normal humans. Acta Otolaryngol (Stockh) 65, 441. Jung, R. 1948. Die Registrierung des postrotatorischen und optokinetischen Nystagmus und die optischvestibulare Integration beim Menschen. Acta Otolaryngol (Stockh)36, 199. - 1953. Nystagmographie: Zur Physiologie und Pathologie des optisch-vestibularen Systems beim Menschen. In Handbuch der Inneren Medizin (ed. G. von Bergmann, W. Frey & H . Schwiegk), 4th edn., Part V /l , p. 1325. Springer-Verlag, Berlin, Gottingen, Heidelberg.

Acta Otoluryngol8.5

Jung, R. & Mittermaier, K. 1939. Zur objektiven Registrierung und Analyse verschiedener Nystagmusformen: Vestibularer, optokinetischer und spontaner Nystagmus in ihren Wechselbeziehungen. Arch Ohren Nasen Kehlkopjheilkd 146, 410. Mackensen, G. 1954. Untersuchungen zur Physiologie des optokinetischen Nystagmus. Graefes Arch Ophthalmoll55, 284. Mackensen, G., Kommerell, G. & Silbereisen, D. 1961. Untersuchungen zur Physiologie des optokinetischen Nachnystagmus. 11. Mitteilung. Individuelle Unterschiede des Nachnystagmus, die Abhangigkeit des optokinetischen Nachnystagmus von der Reizdauer. Graefes Arch Ophthalmol263, 170. Meiry, J. L . 1971. Vestibular and proprioceptive stabilization of eye movements. In The Control of Eye Movements (ed. P. Bach-y-Rita, C. A. Collins & J. E. Hyde), p. 483. Academic Press, New York, London. Morasso, P., Sandini, G., Tagliasco, V. & Zaccaria, R. In prep. Eye-head coordination: Role of the vestibuloocular reflex. Ohm, J. 1921. Uber optischen Drehnystagmus. Klin Monatsbl Augenheilkd 68, 234. - 1932. Uber die Beziehungen zwischen willkiirlichen, optischen und vestibularen Augenbewegungen. 2 Hals-Nasen-Ohrenheilkd 32, 234. Rashbass, C. 1961. The relationship between saccadic and smooth tracking eye movements. J Physiol (Lond) 159, 326. Robinson, D. A. 1965. The mechanics of human smooth pursuit eye movement. J Physiol (Lond) 180, 569. Sugie, N. & Melvill Jones, G. 1971. A model of eye movements induced by head rotation. IEEE Transactions on Systems, Man, and Cybernetics SMC-1, 251. Ter Braak, J. W. 1936. Untersuchungen iiber den optokinetischen Nystagmus. Arch Neurol Physiol21, 309. Waespe, W. & Henn, V. 1977. Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 27, 523. Yasui, S. 1974. Nystagmus generation, oculomotor tracking and visual motion perception. Ph.D. thesis, Dept. of Aeronautics, MIT, Mass. Young, L. R. 1971. Pursuit eye tracking movements. In The Control of Eye Movements (ed. P. Bach-y-Rita, C. C. Collins & J. E. Hyde), p. 429. Academic Press, New York, London.

E. Koenig, M . D . Neurological Clinic University of Tubingen Lieberrneister str. 18 74 Tiibingen, FRG.

Horizontal and vertical optokinetic nystagmus in man.

Facilitation of agonist motoneurons upon initiation of rapid and slow voluntary movements in man.

Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus.

Slow and fast phase velocities of optokinetic nystagmus induced by the optokinetic pattern test in infratentorial lesions.

Scleroderma heart disease with slow flow velocity in coronary arteries.

Postnatal evolution of slow variability in cerebral blood flow velocity.

Quick phase programming and saccadic re-orientation in congenital nystagmus.

Phasic left ventricular blood velocity alternans in man.

Carotid blood velocity during cough studies in man.

Hypnosis in man and very slow brain electrical activity.

Slow cord dorsum potentials elicited by descending volleys in man.

Short nystagmus duration of velocity step response as an indicator of labyrinthine defects.

Thresholds for self-motion perception in roll without and with visual fixation target--the visualvestibular interaction effect.

Interaction between levamisole and aspirin in man.

Interaction between carbamazepine and propoxyphene in man.

The effect of eye closure upon the pathological vestibular spontaneous nystagmus.

Velocity-dependent quantum phase slips in 1D atomic superfluids.

Nystagmus in childhood.

Rovibronic structure in slow photoelectron velocity-map imaging spectroscopy of CH2CN⁻ and CD2CN⁻.

A multielectrode array microchannel platform reveals both transient and slow changes in axonal conduction velocity.

Effect of oxygen in graded concentrations upon tracheal mucous velocity. A study in anesthetized dogs.

Afternystagmus in darkness after suppression of optokinetic nystagmus: an interaction of motion aftereffect and retinal afterimages.

Interaction of active and passive slow eye movement systems.

The interaction between methotrexate and probenecid in man [proceedings].