Orientational asymmetries in small-field optokinetic nystagmus in human infants

Behavioural Brain Research, 13 (1984) 217-230

217

Elsevier BBR 00379

ORIENTATIONAL ASYMMETRIES IN SMALL-FIELD OPTOKINETIC NYSTAGMUS IN H U M A N INFANTS

LOUISE HAINLINE, ELIZABETH LEMERISE, ISRAEL ABRAMOV and JOSEPH T U R K E L

Department of Psychology, Brooklyn College, Brooklyn, NY 11210, U.S.A. (Received March 15th, 1984) (Revised version received June 22nd, 1984) (Accepted July 3rd, 1984)

Key words: optokinetic nystagmus - eye movements - visual development - oculomotor development - infants

Optokinetic nystagmus (OKN) is a pattern of reflexive eye movements which occurs when portions of the visual field are in continuous motion. Gratings moving at 7 deg/s either horizontally (left or right) or vertically (up or down) were presented on a viewing screen subtending 30 ° by 22 °. Horizontal (HOKN) and vertical (VOKN) OKN were recorded under binocular viewing conditions from infants and adults. Eye movements were recorded by means of an infrared corneal reflection eye movement recorder. OKN to horizontal and vertical stimuli was different in pattern for infants. Infants' H O K N was of significantly higher frequency and lower amplitude than their VOKN. Infants below 4 months of age also showed an asymmetry within VOKN between upward and downward stimulus motion, with markedly lower gains and more variable slow phase following movements for downward moving stimuli. No differences were found in H O K N to the right and left. There was also no evidence of a build-up of slow phase velocity over time. Infants' fast phases showed peak velocity/amplitude relationships like those of adults, and like those of infant saccades recorded in a previous study of infants' fast eye movements. Across all directions of stimulus movement, infants had lower slow phase gains and OKN frequencies, and larger slow phase amplitudes than adults. The characteristics of infants' OKN are discussed in relation to those observed in other species and in adult clinical patients with eye movement disorders.

INTRODUCTION

Among the reflexive behaviors which can be elicited from the human neonate is optokinetic nystagmus (OKN)*. OKN is a response to visual movement which has evolved to maintain stability of the visual world. In its function, OKN is closely linked to the vestibular system~,38,54; consequently, the prototypical situation for OKN is movement of the organism through its environment. However, in the clinic and laboratory, O K N is more usually induced by moving a repetitive pattern past the stationary subject. OKN

consists of two phases - - a slow or following phase in the direction of stimulus movement, alternating with a fast or return phase opposite to stimulus movement, resulting in a characteristic "triangle" profile of eye position plotted versus time. OKN has been extensively studied because it is known to be a very sensitive indicator of the condition of the oculomotor system, both in clinical situations and in studies comparing across species. OKN, although simple to describe, is the result of a number of complex interacting oculomotor subsystems. Horizontal OKN (HOKN) has been

* Across the various disciplines concerned with measuring nystagmus, there are differences in the terminology used to describe OKN in different orientations. We have chosen to designate OKN by direction of the stimulus movement, and, thus, by the direction of the slow phase.

Correspondence: L. Hainline, Department of Psychology, Brooklyn College, Brooklyn, NY 11210, U.S.A. 0166-4328/84/$03.00 © 1984 Elsevier Science Publishers B.V.

218 studied most commonly (possibly because horizontal eye movements are easier to measure with techniques such as EOG, and horizontal O K N drums are easier to produce); however, O K N is also shown to stimuli drifting up or down. Since it has been studied less frequently, vertical O K N (VOKN) is much less well understood as a system, although most models of O K N 53"55 usually do not distinguish between mechanisms responsible for responses to horizontal and vertical patterns. Work on H O K N across species has found that there are several distinct subsystems responsible for producing OKN. The simplest, and probably phylogentically the oldest, system subserves O K N in lateral-eyed animals with no stereopsis and no clearly defined fovea, such as rabbit ~3-~5. The rabbit requires that a relatively large portion of the visual field be moving to trigger O K N (although the rabbit retina is not homogeneous as to which portions can trigger the response25). Rabbits also show a very marked build-up over time in the velocity of the O K N slow phase. Although rabbits are not reported to show VOKN asymmetries 8"16, they show a marked asymmetry to horizontally moving patterns; with monocular stimulation, stimulus movement in the nasal direction entrains OKN, while movement in the temporal direction does not. In animals with stereopsis and retinal regions of high acuity (as in the cat's area centralis and the primate fovea), another O K N subsystem emerges. This system has been variously termed 'voluntary', 'foveal', or 'cortical', and some have even identified it as the 'smooth pursuit' system, rather than an O K N system 15"54. In cat and primate, O K N can be elicited with much smaller fields than in rabbit. Build-up of O K N slow phase velocity over time becomes less obvious as one moves across species from cat to monkey to human. Normal adult cats, monkeys and humans are not reported to show monocular asymmetries in the horizontal orientation. However, in kittens 2s,6'~-vl, young monkeys, and human infants 4-5"5°, a monocular horizontal asymmetry like that of the rabbit's is found. This H O K N asymmetry normally declines with increasing age, presumably due to development of the fovea ~'4° and/or cortical structures responsible for stereop-

sis 9"31. Cats raised in conditions which interfere with the development of binocular function, such as monocular patching 29"39"vJ'v2 and adult cats whose cortices have been removed 49"7~ show the same horizontal asymmetry. A similar H O K N asymmetry has also been reported in some adult amblyopes 58 and afoveate adult humans 7. In addition, kittens show a strong asymmetry in vertical OKN, with downward movement eliciting poor O K N v~. The adult cat continues to show this strong vertical asymmetry, both binocularly and monocularly TM, although upward stimulus movement elicits good OKN. One study 37 reports that when kittens are raised for prolonged periods in darkness (approximately 1 year), the normal vertical asymmetry in cat VOKN is abolished, and downward stimulus movement elicits O K N as readily as upward movement does. In monkey, the degree of V O K N asymmetry found varies from study to study, probably influenced by the conditions of stimulation (position of the animal with respect to gravity, field size, and stimulus velocity). Most studies have reported that downward stimulation is less effective than upward as an elicitor o f V O K N ; whether stimulation is monocular or binocular does not appear to matter 12"46"51"64 Only Krieger and Bender 44, in an early study, reported vertical asymmetries opposite to those found by most others. Pasik, et al.sz reported that when the optic chiasma, the corpus callosum and other interhemispheric connections were sectioned, monkeys showed very marked reductions in O K N to downward drifting stimuli. These neurological data support the hypothesis that both sides of the brain must receive adequate visual input to result in normal VOKN. In normal adult humans, a vertical asymmetry has sometimes been reported 65 and sometimes not 63; at this point, it is not clear whether these discrepancies result from individual differences among normal adults 6°, or from the exact conditions of the stimulus used to elicit VOKN. In populations with visual disorders, VOKN asymmetries have been reported but the details are complex. Tychsen et al. 68 have recently reported that patients with early onset strabismus show reductions in downward OKN, whereas clinically similar

219 patients whose strabismus was of later onset do not show a marked V O K N asymmetry. On the other hand, Schor and Levi 59 found that some adult amblyopes show a vertical asymmetry in their non-amblyopic eye that is opposite to that normally found in cat and monkey, with upward stimulus movement eliciting poor O K N while downward O K N remains robust. The relationship of this finding to other V O K N asymmetries has not been established. The complexities of O K N as a system are well illustrated by examining the literature on oculomotor disorders, in which there are numerous reports of O K N irregularities19"23"42"45'74; some of these patients show disturbances of horizontal OKN, with normal vertical responses, and others show disturbances of vertical O K N with normal horizontal responses. In some patients, smallfield O K N is disturbed while whole-field O K N remains good, while for others, the opposite pattern is found. Orientation differences of all possible sorts have also been reported, presumably corresponding to selective damage in the complex neurological systems responsible for the various 'types' of O K N 1°'56. While large-field, binocular H O K N has frequently been reported to occur in young humans 4-5"47'5°, and has even been used as a measure of acuity 21'32, the conditions of recording (either observation or uncalibrated EOG) have not allowed a quantitative assessment of the parameters of the response such as slow phase velocity or build-up of slow phase velocity. O K N studies with human infants have used large-field stimulation (90-180 °), and have been exclusively in the horizontal orientation. Small-field stimulation, which is likely to engage the smooth pursuit system, has not been used with infants whose smooth pursuit abilities are minimal 3,2°,22,43,47,57,62. Given that the O K N system is a useful diagnostic as to the level of functioning of several different oculomotor systems, we were interested in measuring OKN to a smaller display than had been typically used with infants. Clinically, smaller fields can uncover differences which are not apparent with larger fields 24,58. Also, smaller field sizes may be more likely to uncover developmental differences in O K N because smaller displays

will engage both O K N systems. We were also interested in addressing the issue of vertical asymmetries which have been seen in animals, but never studied in infants. Since monocular H O K N has already been studied, we chose to study binocular responses. METHOD

Subjects Out of a total of 34 infants tested, data were obtained from 16 babies between the ages of 22 and 389 days. Information from the remaining infants could not be used either because subjects were too fidgety or because of equipment failure. Two subjects were observed longitudinally, one over 13 sessions and the other over 5. Data from only the first session from each of the infants were included in the 'cross-sectional' sample, the primary set analyzed; infants in this set ranged from 22 to 114 days. In addition, to provide a baseline measure of adult O K N using our equipment, data were collected from 7 adults aged 18-36 years. Data from the longitudinal subjects (at ages between 121 and 389 days) have been used to supplement information about developmental differences between the cross-sectional infants and adults.

Apparatus Eye movements of infants and adults were recorded with an infrared corneal reflection videosystem which has been fully described elsewhere 33. The entire system as assembled in our laboratory is shown schematically in Fig. 1. Briefly, the subject's optic axis and eye movements were calculated by an eye tracker (Applied Sciences Laboratories, Model 1994) which, at a 60 Hz rate, analyzed the position of the corneal reflection of an infrared source from the right eye in relation to pupil diameter. The eye movement recorder provided a digital output of horizontal eye position, vertical eye position, and pupil diameter. These data were simultaneously fed into a larger computer (PDP 8/e) which provided mass storage and stimulus control. Infant subjects were held against the shoulder of an experimenter who stabilized the infant's head by pressing it against his neck and cheek;

220

f Fac

Sc

3

Face camera

~

u je~t

I

Dlitter

4___

--"hlR-Dass

[

~

[ ~BI~J tracker ~ ~

Scene monitor

Eye

filter

Pattern

I generator

illuminator

o out r,

data storage

J

Fig. 1. A schematic representation of the eye movement recording system designed for use with infants.

while some subjects are too active to allow data collection, most infants can be kept sufficiently still by this method to give valid estimates of eye position. Adult subjects were seated comfortably and used a chin rest. The system is able to compensate for small head movements, and it can detect eye movements of less than half a degree. During eye movement recording, adult subjects could not see the infrared source and the recording system was unobtrusive. Stimuli were presented on a large cathode ray tube (CRT) screen in front of the subject, who viewed the display through a beam splitter that transmitted the visible wavelengths from the display and reflected the infrared wavelengths from the eye tracker's illuminator. Calibration Instrument calibrations for the eye tracker are of two types, one dealing with positional accuracy

or static calibration (correct specification of where on the stimulus the eye is pointed), and the other with dynamic accuracy (correct reproduction of eye velocities). Static calibration methods and correction procedures have been described in detail elsewhere 36. Briefly, the method for static calibration involves collecting fixation data to small flashing targets, and then generating a calibration polynomial to map obtained eye positions onto the actual fixation locations. Using our normal instrument settings, the average adult or infant subject gives uncalibrated estimates of eye position which are within + 2 ° of the actual spatial position of regard in the visual field, although the equipment can detect changes in eye position of less than 0.5 ° . In individual calibration polynomials with this apparatus, most subjects require primarily a DC-offset term to correct for optical misalignments in the recording situation. There is also usually a small

221 multiplicative gain term, but the average value is similar for adults and infants 2. Due to the length of the experiment, individual static calibrations were not possible with all infants. However, our analysis of the use of corneal reflection methods with infants and adults confirms that changes in corneal curvature and physical growth of the eyeball with age, two factors which are important in estimates of point of regard using corneal reflection, essentially compensate for one another during growth 2'9. Thus infant and adult data may be directly compared. However, since calibrations were not performed for each subject, measures of amplitude, velocity, and gain are best viewed as relative measures. Analyses also take account of the fact that the gain of our system is slightly asymmetric between the horizontal and vertical axes and adjust all the data for this constant difference. Dynamic calibration procedures for analyzing OKN fast phases have been developed in order to compensate for the relatively low bandwidth of our television-based recording system 35. Briefly an artificial eye2 was used to emulate fast eye movements; the eye was rotated at various velocities through a series of saccades of different amplitudes. Using these known inputs and the corresponding measured outputs, nomograms were created for correcting measured peak velocities. Application of these correction nomograms to adult peak velocities results in values close to those reported in the adult eye movement literature 34.

S timufi Sinusoidal and square wave gratings were generated by a series of microprocessors (Visual Stimulus Generator V2-R2; Electronics Shop, The Rockefeller University; (see ref. 48)) on a large CRT display screen (Hewlett-Packard, Model 1310A) which was viewed from a distance of 78 cm. The field subtended 30 ° horizontally and 22 ° vertically, with the result that the number of cycles of grating visible on the screen for horizontally drifting gratings was slightly higher than the number visible for vertically drifting stimuli. All stimuli were of high contrast (approximately 70~o) with a spatial frequency of 0.3 cycles/deg.

The type of stimulus set was varied between subjects. In both, vertical gratings were presented moving rightward or leftward and horizontal gratings were presented moving upward or downward, with direction of movement alternated within an orientation. All gratings had a mean luminance of approximately 4 nits measured with a U D T photometer (Model i l i A ) and appropriate lens. In one stimulus set, stimuli were either sinusoidal or square wave patterns all presented at a velocity of 7 deg/s with a trial length of 20 s, while in the other set stimuli were all sinusoidal gratings, with a trial length of 15 s. In the second stimulus set, some faster velocities were included but only the 7 deg/s data are being presented here. With both stimulus sets, two trials of each combination of stimulus direction and velocity were presented with an inter-trial interval of 5 s during which the CRT was maintained at mean luminance. In order to encourage involuntary OKN 44, adults were instructed to 'stare at the center of the screen and keep the moving bars visible'. Since we, as others 6°, found no differences related to type of grating, data from both sinusoidal and square wave gratings have been combined.

Data analysis Initial data reduction was done using an interactive computer procedure in which an operator could display portions of an OKN record on a CRT screen and, by adjusting cursors on the screen face, select segments of the record for measurement. In this way, each OKN slow phase was individually measured by a program which determined the movement's duration, total amplitude, and velocity (by calculating the slope of a linear regression line through the data points). Gain of slow phases was calculated by dividing this velocity by the velocity of the stimulus movement. Fast phases were analyzed for measures of amplitude and peak velocity. Identification of slow and fast phases in these data sets was relatively easy and frequent checks showed high inter-observer reliability. Following this initial reduction, data were stored on a large computer and further analysis was done using standard statistical packages (BMDP; SAS).

n

Tracking angle

Oblique ratio

Tracking correlation

Gain

Frequency

Duration

Slow phase amplitude

Measure

Down

P

4.68 (1.56) 1.04 (0.34) 0.42 (0.25) 0.66 (0.28) 0.88 (0.05) 0.11 (0.26) 4.90 (7.16) 14

4.00 (1.10) 1.23 (0.24) 0.22 (0.10) 0.40 (0.12) 0.79 (0.09) 0.61 (2.16) 1.76 (22.73) 9 n.s.

n.s.

< 0.001

< 0.001

< 0.01

< 0.001

< 0.001

2.69 (1.99) 0.69 (0.59) 1.40 (0.92) 0.62 (0.08) 0.90 (0.06) - 0.06 (0.22) - 3.43 (8.41) 7

2.21 (1.00) 0.49 (0.30) 1.38 (0.68) 0.65 (0.23) 0.88 (0.07) - 0.03 (0.40) 2.32 (13.04) 7

3.22 (1.67) 0.54 (0.35) 1.08 (0.54) 0.82 (0.13) 0.88 (0.06) 0.07 (0.18) 0.46 (6.76) 7

2.97 (2.00) 0.50 (0.37) 1.04 (0.57) 0.92 (0.14) 0.87 (0.06) 0.02 (0.10) - 0.47 (3.95) 7

n.s.

n.s.

n.s.

< 0.001

n.s.

n.s.

n.s.

n.s.

n.s.

<0.001

< 0.002

< 0.001

< 0.001

< 0.001

2.90 (0.87) 0.76 (0.46) 0.58 (0.59) 0.72 (0.36) 0.85 (0.06) 0.09 (0.35) 5.62 (12.22) 12

Up

2.99 (1.32) 0.82 (0.40) 0.55 (0.79) 0.64 (0.42) 0.84 (0.13) 0.24 (0.84) 6.42 (28.04) 11

Left

P

P

Right

Down

Left

Right

Up

Infant~adult

Adults

Infants

Values in parentheses are standard deviations.

Means for OKN variables - - infants and adults

TABLE I

t~

223 RESULTS

Infants' OKN slow phases and stimulus orientation OKN to horizontally and vertically moving stimuli was very different in pattern for infants. H O K N showed a high frequency/low amplitude pattern, while VOKN had lower frequency and larger amplitude. Amplitude and duration of slow phases was significantly less for horizontal (right or left) stimulus movement than for vertical (up or down). (See Table I.) OKN frequency was assessed by counting the number of slow phases in the total valid data time in a period. (Calculating frequency from fast phases gave equivalent results, so, for the sake of brevity, only slow phase values have been reported.) OKN frequency was significantly greater for horizontal than vertical stimuli. Fig. 2 shows examples of these differences between horizontal and vertical OKN for infants. Slow phase gain was greater for horizontal than for vertical stimulus movement, but a repeated measures one-way analysis of variance indicated that this orientation difference was caused by a significantly lower slow phase gain for the down condition. Within VOKN, there were marginal, but non-significant tendencies for downward slow phases to be of smaller amplitude (P < 0.10), but longer duration than upward ones ( P < 0.06). There were also more infants who showed no behaviors categorized as slow or fast phases of OKN in the down-OKN condition,

suggesting that for some infants, gain of downward O K N was so low that the behavior could not be reliably scored in the records. It should be noted that in such cases, the infants' mean eye position generally continued to be close to the center of the visual field. The failure to observe measurable downward OKN did not result from a tendency for the infants to follow the pattern to the lower edge of the screen and remain at this lowered position for the rest of the trial. Fig. 3 illustrates the up-down asymmetry in vertical OKN for infants. To test whether there was a difference in the quality of smooth pursuit across orientations, velocity of individual slow phase episodes was estimated by fitting a linear regression to the data points in each episode. An estimate of how well the points fit the regression line could be found in the correlation coefficient resulting from this calculation. Individual R values were weighted by the duration of the episode (since, theoretically, it was easier to achieve a good linear fit with shorter periods than larger ones), and were transformed into Z scores by Fisher's Z (r) transform 27. The Z values, or tracking correlations, for downward stimuli were significantly lower than those for other directions, indicating that pursuit for the downward direction was more variable than for right, left or up (see Table I). In many infant records, we saw evidence that OKN in one direction was 'contaminated' by

Small-field Michael L . , 6 5 days Rightward drifting grating

OKN

N., 1 1 3 days Upward drifting grating

T., adult Leftward drifting g r a t i n g

Leron

Joe

Right

~

H

Left

f w V Down

Stimulus: drifting grating, 7 d e g / s e c ,

0.3

cy/deg

5deg 1 OV

~ 2sec

Fig. 2. Typical examples of H O K N and VOKN for infants and an adult. The individual eye tracings show the simultaneous horizontal and vertical positions of the eye, each plotted versus time. Direction of stimulus moVement is indicated above each pair of tracings. The scales shown for amplitude and time can be used to calculate slow phase velocity.

224

Asymmetry in Vertical OKN Stimulus: drifting grating, 7deg/sec, 0.3cy/deg Steven Z. 28days

Ricki R. 36days

Michael L. 65days

E E > 0

Down'll A

UJ 0

Joshua L. 73days

0 C 0 e~

E

up

0

Daniel R. 114days

Meagan R. 78days

U

0

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n

~

5deg ] 0

2sec

Fig. 3. Examples of up and down VOKN from infants of ages 28-114 days. The examples show only the vertical trace; horizontal traces have been omitted in order to facilitate comparison of up and down stimulus motion.

movements in the orthogonal dimension. A ratio of the amplitude of the orthogonal component of a movement to the amplitude of the component in the direction of the stimulus was calculated and compared across orientations. There were no significant differences across directions, although there was a non-significant tendency for down to show greater 'cross-talk' than the other directions (Table I). The angular deviation of the eye's tracking direction from the direction of stimulus movement was also calculated. Infants were highly variable in how closely their slow phase tracking matched the stimulus direction (see Table I). There were no significant differences in tracking angle across directions for infants. Infants' differences from adults on these measures are described below. Given the reportedly poor smooth pursuit in infants of this age, we were interested in whether O K N in this situation would show a build-up

phenomenon similar to that found in animals without a good pursuit system (such as rabbit). Velocity of individual slow phase episodes was plotted versus the time of that episode in the stimulus period for each subject, and linear regression lines fit to the data. The individual plots were also inspected to check for the presence of non-linear trends. There was no tendency, regardless of subject's age or direction of stimulus movement, for slow phase velocity to build up over stimulation. Like those of adults, infant velocities reached their final level very shortly after stimulus onset. Whether a build-up might be shown for stimulation lasting longer than 15 s cannot, of course, be determined in the present study.

Infants' OKN fast phases and stimulus orientation Data on fast phases confirmed the horizontal and vertical differences described above on the

225 analyses of slow phase amplitude and frequency, so these means have not been presented. Main sequences relating individual fast phase peak velocities to fast phase amplitudes 6 were plotted for each subject. In our research on saccades in infants, we have learned that main sequences tend to be unstable and often non-significant if they are based on fewer than about 10 points. Most subjects had enough data to allow separate estimates of main sequence slope for horizontal and vertical stimulus motion as well as for both dimensions combined. The value of the main sequence slope was corrected by a calibration nomogram which compensated for the reduction in velocities imposed by the limited bandwidth of our TV-based recording system 35. Since there were no significant differences in main sequence slopes for either infants or adults as a function of orientation, main sequence slopes were derived for data collapsed over orientation. Fig. 4 shows examples of main sequence plots for an infant and an adult subject. The mean corrected main sequence slope for infants was 24.3 with a standard error of 3.18. The adults' mean slope was 26.7 with a standard

error of 3.06. These values are similar to those we have reported for saccades from adults and alert infants 34.

Developmental change in OKN characteristics In order to test whether any of the O K N variables show developmental change over the age range included here, linear regressions regressing a dependent measure on infant age were done, and the significance of the regression tested. The regressions were also plotted and visually inspected for possible non-linear trends. For downward stimulus motion, slow phase amplitude significantly increased from 22 to 114 days. Slow phase gain in the downward direction also showed a tendency to increase with age, but the trend did not reach significance (P < 0.09). The Z value which was used as a measure of the smoothness of pursuit significantly increased over the same age interval for downward stimulus movement, indicating that pursuit in the downward direction was improving with age. No age trends were demonstrated for slow phase duration or O K N frequency. Similarly there was no

OKN: Fast Phases Stimulus: drifting grating, 7 d e g / s e c , O . 3 c y / d e g "~300-

•

Leron N., 113 days

1400

300~

-400 '~
Cindy H., adult Q

,

-300 ..-.~200.

200-

0

•

•

-200

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•

~

. • °

oo •

100.

.100

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•

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0.) n

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•

•

ee

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•

•

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,0 0

=

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,5

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,

i

u

110 Amplitude

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15 of E y e

u

~

i

i

~

e Movement

i

|

i

~

I

'

'

'

o

'

lO (deg)

Fig. 4. Examples of typical main sequences for peak velocity versus amplitude. The left ordinate shows measured, uncorrected values for peak velocity. The right ordinate shows corrected peak velocity for each individual's main sequence (see text). The solid lines are the result of a linear regression fit to the data. Corrected main sequence slope for the infant is 23.03, R = 0.85; for the adult, the corrected slope is 24.98, R = 0.85.

226

significant change in the main sequence slope of fast phases over age, for any direction of stimulus movement. The data suggest that there is a significant change in O K N to downward moving stimuli over the course of the first 4 months. Data for all of the other directions of stimulus movement showed no evidence of change during the age interval we studied in our cross-sectional sample. Between the ages of 121 and 389 days, the two subjects tested longitudinally showed no evidence of any further age trend in down-OKN. However, O K N of these infants still did not resemble adult OKN, described in the next section.

Comparisons between infants and adults In comparing data from cross-sectional infants and adults, two-way analyses of variance with repeated measures were done. Since infant differences as a function of orientation have already been presented, results will focus on main effects of the age variable; means are presented in Table I. Like infants, adults did not show differences between left and right stimulus movement. Unlike infants, they also did not show up-down differences. Adults had significantly higher gains for slow phases than did infants. The values we measured for adult O K N slow phase gain compare favorably with those reported by Schor and Narayan 6° for fields of this size with stimuli moving at a similar velocity. Adults' velocity for vertical was significantly higher than that to horizontal, a pattern opposite to that of infants. Collins, et al. 17 also reported that adults had higher gains for vertical O K N at low stimulus velocities, although not all studies find this pattern6O. (,s. Adult slow phase amplitude was significantly smaller than that of infants, although for adults, as for infants, vertical amplitude was slightly greater than horizontal. Adults' slow phase durations were also significantly shorter than those of infants. The frequency of O K N was about twice as fast for adults as for infants, averaging over direction. Infants were significantly more likely than adults to have involvement on the dimension orthogonal to that of stimulus movement. For no direction did adult tracking differ significantly from the angle of stimulus motion. Quality of smooth pursuit had a significantly

lower average value for infants (0.84) than for adults (0.88), but this difference was caused by infants' poor following for down; for left, right and up, infants' smooth pursuit was equivalent to adults'. The significance test for this effect was performed using the Z-transformed tracking correlations that were the result of the linear regressions fit to each slow phase. DISCUSSION

One of the major findings of the present study is that with binocular viewing of a relatively small field, there are noticeable differences in how infants show O K N in the horizontal compared with the vertical plane. Beat frequency is higher and amplitude is smaller for H O K N . In an earlier, preliminary report based on an observational analysis of these O K N data 6v, we came to the conclusion that H O K N was very poor in young infants, because the H O K N is not as distinctive a pattern in the plotted records as the higher amplitude, longer duration, vertical movements; this error on our part reinforces the need to supplement observational reports of infant O K N with careful quantitative analyses. The differences between the infants' two patterns of O K N for horizontal and vertical are reminiscent of differences described for adults given different instructions while O K N was being recorded 4~. If adults were instructed to 'stare' at the screen, their O K N was of the low amplitude/high frequency type shown by our adults for all orientations and for the infants to horizontal stimulus movement (although the infants' absolute frequency was lower). If adults were instructed to 'look' at the pattern, their O K N developed a larger amplitude/lower frequency pattern. This distinction is similar to that of Ter Braak 66 who differentiated the two types of O K N by the terms' Stier' a n d ' Schau' nystagmus. ' Stier' or stare nystagmus was presumed to be mediated by the older, reflexive, peripheral O K N system, while 'Schau' or look nystagmus was believed to involve contributions of the evolutionarily newer, voluntary, foveal O K N system related to smooth pursuit. Whether the difference between orientations in infants is related to these distinctions is

227 not known. It is known that horizontal smooth pursuit is poor in young infants 3,43, consistent with HOKN caused by the older reflexive OKN system. Shea and Aslin 62 have recently reported that vertical smooth pursuit develops even more slowly than horizontal pursuit; this finding may imply that the lower frequency of VOKN in the present study compared with that for HOKN is correlated with the level of development in the smooth pursuit system. Frequency of vestibular nystagmus has been used as a measure of maturity in infants 26, with higher frequencies shown by infants with higher developmental status. It has not been established whether beat frequency in infant OKN is related to 'maturity', but adults had beat frequencies about twice those of infants and higher gains overall. Consistent with this interpretation of the OKN beat frequency, Schor et al. 61 report a lower frequency for infant HOKN compared with adult OKN, with full-field stimulation. The size of their stimulus field, and the presence in the infant records of optokinetic afternystagrnus (OKAN) imply that the infant OKN in that study was of the reflexive type. Thus, both infant reflexive, 'Stier' and pursuit or 'Schau' OKN have lower beat frequencies than adults. At the same time, infants' OKN showed no evidence of slow phase gain build-up in either orientation; this observation is at odds with the reports of poor smooth pursuit in infants, since in adults the absence of build-up of eye velocity is usually attributed to contributions from the smooth pursuit system. Whether infants would show a slow-phase build-up to higher velocities of stimulus motion or longer stimulus presentations needs to be explored. A r e c e n t s t u d y 57 has found evidence of good smooth pursuit in infants as young as 1 month, but only at a relatively low target velocity (10 deg/s); other studies reporting on infants' smooth pursuit (e.g. refs. 3, 43, 62) have used faster velocities. Within the vertical orientation, there is a developmental trend in the effectiveness of downward stimulation in eliciting OKN, similar to the VOKN asymmetry shown by cats, monkeys and congenital strabismics. For the youngest infants, OKN to downward moving stimuli showed lower

frequency, greater variability, and a tendency for lower gain. Based on the findings that sectioning of interhemispheric connections can create, in monkey, exaggerated versions of the infants' vertical asymmetry, we postulate that the VOKN asymmetry in infants may be due to an immaturity in the coordination between the two hemispheres. Such interconnections are important for coordinating the retinal images of the two visual fields created by partial decussation. By 3 months, the vertical asymmetry is much less marked, so presumably by that time, the two halves of the brain may be working together in the generation of vertical OKN. Unfortunately, we know of no other data on the development of other forms of vertical eye movements to confirm the generality of this effect with infants. However, the finding that age of onset of strabismus influences whether a VOKN asymmetry is evident68 supports the hypothesis that the systems responsible for VOKN develop in early infancy, and are susceptible to modification as a function of early visual experience. The present results, like those on monocular asymmetries in HOKN, confirm that careful examination of the response of OKN may be a useful method for evaluating the functioning of the infant's visual system, and possibly for diagnosing visual problems at an early stage. For example, strabismus and amblyopia are frequent concomitants of prematurity 3°. Analysis of OKN responses in prematures may be a useful clinical tool for detecting those disorders at an early age. ACKNOWLEDGEMENTS

The research reported here was supported by NIH Grants HD08706 and EY03957, and Awards 13484, 661078, and 662199 from the PSC-CUNY Research Award Program of C.U.N.Y. Facilities for data analysis were provided by the C.U.N.Y. University Computer Center. We gratefully acknowledge the assistance of Max Lilling, M.D., David Kliot, M.D. and Downstate Medical Center of S.U.N.Y. for their help in recruiting parents of infants. We also thank the parents of our infant subjects for their interest and cooperation.

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