0042-6989/92 165.00+ 0.00 Copyright 0 1992 Pergamon Press Ltd

Vision Res. Vol. 32, No. 6, pp. 1115-1124, 1992 Printed in Great Britain. All rights reserved

Visual Remapping in Infantile Nystagmus HERSCHEL Received

P. GOLDSTEIN,*

IRENE GOTTLOB,*t

12 March 1991; in revised form 2 October

MICHAEL

G. FENDICK*

1991

The possibility that patients with idiopathic infantile nystagmus achieve spatial constancy by visual remapping was investigated by comparing subjective localization of flashed test targets to their absolute position in space and to their absolute position on the retina. Nystagmats first viewed a screen-stationary reference target that was followed by a test flash. A computer used eye movement feedback to precisely control the test flash position on the retina. AR six nystagmats detected test flashes throughout their nystagmus cycle. For three nystagmats test flashes (total N = 48) were delivered to the same retinal locus that were, at different times, to the right and left of the reference target. More than two-thirds of such crossover stimuli were correctly located in space: when only those stimuli at least 0.5 deg from the reference were considered, two of three subjects correctly located all stimuli. Taken together these results argue that our subjects could see throughout the nystagmus cycle and shifted their visual map in synchrony with their nystagmus as an explicit means of avoiding os42illopsia. Spatial constancy

Infantile nystagmus Visual direction

INTRODUCTION People with infantile nystagrnus$ (IN) rarely perceive motion of a stationary visual scene in spite of nearly incessant image motion on the retina. This maintenance of spatial constancy, in contrast, is lacking in subjects with mature onset nystagmus such as with down-beat nystagmus where perceived scene motion, called oscillopsia, adds to these subjects’ distress. The focus of most previous work with IN subjects has been to assess visual function. Subnormal visual acuity was found with continuously presented static eye charts (Nom, 1964) and subnormal visual resolution was found with continuously presented static gratings which was most significantly reduced when the grating was oriented perpendicular to the plane of the nystagmus (Abadi & Sandikcioglu, 1975). More recently, visual acuity was found to be correlated to the percentage of time during the nystagmus cycle when eye velocity was low (Abadi & Worfolk, 1989). The above data suggest that clearer vision is possible at those points during the nystagmus cycle where eye velocity is zero or near zero. It might be expected, therefore, that those clear images shifting back and forth during the nystagmus cycle would be perceived as back and forth motion of objects in space, similar to the

*The Foerderer Eye Movement Centre for Children, Wills Eye Hospital. Department of Ophthalmology, Jefferson Medical College of Thomas Jefferson University, Philadelphia, PA 19107, U.S.A. tsupported by the Max Kade Foundation. Yfhe term injiinfile nystugmus is preferred over congenital nystagmus because in most individuals the nystagmus begins in the first few months of life and is not present at birth (Reinecke, Guo & Goldstein, 1988).

Relative localization

Oscillopsia

perceptions of mature onset nystagmats. Importantly, this expectation remains even though the detection of target motion parallel with the nystagmus direction has been found to be reduced (Abadi & Sandikcioglu, 1975; Dieterich & Brandt, 1987). One must conclude that IN subjects rely on mechanisms besides lowered acuity and lowered motion detection for alleviation of oscillopsia. It is plausible that IN subjects sample the visual scene only during particular phases of their nystagmus cycle but supportive evidence is lacking, except to say that the positive correlation of foveation time and visual acuity mentioned above would be consistent with a sampling hypothesis. On the contrary, IN subjects do report oscillopsia when a continuous retinally stabilized target is presented either as an afterimage viewed along with a small roomstationary light or by electronic feedback of eye position to control target position (Leigh, Dell’Osso, Yaniglos & Thurston, 1988) which suggests that vision is continuously active throughout the nystagmus cycle. More direct evidence for the absence of sampling came from a preliminary study from this laboratory (Jin, Goldstein & Reinecke, 1989) wherein IN subjects easily detected 2 msec flashes of a retinally stabilized visual spot target during all nystagmus phases and across their entire nystagmus velocity range. That study also failed to find evidence that the quick reappearance of the stationary reference spot could backward mask the detection of the test flash. That oscillopsia can be reported with stabilized targets strongly suggests that a cancellation mechanism exists whereby an extra-retinal eye movement signal is combined with the retinal signal to effectively negate the retinal image motion before perception (Leigh et al.,

1115

1116

HERSCHEL P. GOLDSTEIN et al

1988). Long ago, von Helmholtz (1926) suggested such a cancellation mechanism to explain spatial constancy during normal saccadic eye movement. Matin (1976) has noted, however, an asynchrony between the perceptual shift associated with a saccade and the saccade trajectory itself leading to the mislocation of visual targets flashed immediately before, during and immediately after saccades. We were interested in directly investigating the possible can~llation mechanism in IN and relating it to target localization during eye movements in normals. In addition, we sought to repeat the detection paradigm used in our earlier study with precise computer-archived data and to obtain evidence that detection of the small flashed targets was not the result of sampling either an afte~mage or any other ~tin~Iy-fixed persistence mechanism. METHODS AND SUBJECTS Eye position was registered using the magnetic search coil technique (Robinson, 1963). Subjects therefore wore on their viewing eye a contact annulus (Skalar) in which was embedded 9 turns of fine copper wire as described by Collewijn and colleagues (Collewijn, van der Mark & Jansen, 1975). The subject’s fellow eye was patched. ~m~ulation of the eye coil signal yielded a horizontal and vertical eye position with a 2OOHz bandwidth. Subjects sat within a frame, their heads comfortably stabilized with adjustable plastic restraints placed around the skull and under the chin. A green (543 nm)

laser spot target was projected onto a tangent screen i m in front of the subject. The screen material, Stewart Filmscreen Lumitlex SO/SO, was chosen for its wide angle of eq~l~nan~. The brightness of the spot was silently and virtually instantaneously (rise time lO-90% < 50 nsec, published specification) controlled by an acousto-optic modulator (IntraAction Carp AOM-80 and ME-80) while the spot was positioned in two dimensions by mirror galvanometers (Genera1 Scanning G325 and 6350). A microcomputer (DEC i Ii733 recorded eye movement and provided signals determining target brightness and position with 1 msec resolution but archived a data frame every 2 msec. By averaging two consecutive samples of eye position, signal noise was reduced to about 0.1 deg. At times, the computer stabilized the spot target on the retina by feeding back the eye position signals. The overall bandwidth of stabilization was 54 and 100 Hz in the horizontal and vertical channels, respectively. During experiments, target and eye position were monitored SimuIta~eousfy using an oscilloscope’s x-y display. To wash out any laser light leaking through the system and to reduce effects of dark adaptation, the entire tangent screen was diffusely illuminated (1 cd/m2j. The rationale behind our test is shown in Fig. 1. .4 typicaf subject with IN, when asked to look at the screen-stationary reference point XI instead of steadily fixating, gazes across the screen with, for example, the jerk waveform depicted in panel (A). The total nystagmus amplitude is a. The next two panels show the eye

c

FIGURE 1. Test rationale is shown schematically. Panel (A). When asked to attend the screen-stationary reference spot X, a subject with a right-beating jerk type nys~~~ woufd fovea& X at the end of the quick phase and then drift away from X. The total nystagmus ~pljtude is a. Panel (B). Geometry when eye foveatas X. Test &&es could occur at either points R, or R, on the retina which were adjusted to be half the nystagmus amplit& away from F. Points RL and R, correspond to screen positions L and A, rcqxctivcly. panel (C). Geometry when eye is at furthestexcursion away from X. getting the test flash angle to a/2 aligns the position L in (B) and the position R in (C). thus the same point in space will be imaged on different retina loci during the nystagmus cycle. A reasonable sampling mechanism would allow vision only when P is aligned with X, as when the eye is positioned as in panel (3). If the test tlash, however, occurred at R, whik the eye was positioned as in panel (C), a persistence mechanism, such as an afterimage, would be necessary to hold the tIash until vision became active again. Then the flash would be expected to be mislocalized at R as on panel (B), on the opposite side of X.

VISUAL REMAPPING

IN INFANTILE

at its extreme right position (B) and extreme left position (C) during the nystagmus cycle. When the eye is positioned as in (B), spot X is imaged at retinal position F. At each extreme eye position consider the relative positions of flashed targets L or R to X on the screen when the image positions of L and R on the retina, denoted R, and RR, have been set at a/2 deg to the left and right of F on the retina. In (B), a target imaged at R, will be to the left of X on the screen while a target imaged at R, will be to the right of X. In contrast, in (C) targets imaged at both RL and RR will be to the left of X on the screen. Importantly, note how retinal position R, corresponds in (B) to a screen position to the right of X but crosses over to the left of X in (C). These are called crossover stimuli and, as described in detail later, are critical for deciding whether IN subjects perceive target positions with respect to the retina or with respect to space. Subjects were asked to locate the test flashes relative to X. Before placing the search coil on the eye, subjects were given practice in observing test flashes and issuing responses. Subjects were then shown continuous screenstationary targets for all possible target brightnesses which, without exception, were perceived by all subjects as stationary. After application of topical anesthetic, the search coil was placed. Each recording session consisted of calibration followed by repeated flashed tests. Calibration proved to be the most difficult aspect of the experiment; especially the offset adjustment that at-

1117

NYSTAGMUS

tempted to align F with the fovea. By aligning F with the fovea, test flashes at RR and R, would then be equally distant from the fovea and, assuming our subjects have normal retinal sensitivity, would then be approximately equally detectable. First, each subject attended screenstationary targets spanning a +20 deg range horizontally and vertically; 0 deg was straight in front of the viewing eye. Over this range, the nystagmus of each subject included a quick phase which allowed eye movement gain and offset to be adjusted so that the mean position at the end of the quick phase aligned with the target position at each of the calibration positions. Because the null zone of some subjects was close to the 0 deg position, position X was usually shifted to the position within + 20 deg where the nystagmus amplitude was greatest. The responses to repeated flashed target presentations followed the timing of target brightness and position as shown in Fig. 2. The target first appeared at the reference position X for a random amount of time (1-3 set). The target was then blanked for 50 msec to allow enough time for the galvanometer mirrors to precisely track the eye but with a horizontal offset added on of approximately half the nystagmus amplitude. The direction of the offset was randomly chosen by the computer. Stabilization of position continued during the 2 msec test flash, The subjects were then given a period of time to press a double-throw momentary switch to the right or left to indicate their perceived position of the test flash relative

-d

>

TIME

l/2 Nystagmus Amplitude

TARGET POSITION I,

TIME FIGURE 2. The target position and target brightness profiles are shown as a function of time. At the beginning of a sequence a screen-staiionary reference target appears at position X (see Fig 1) and remains on for a random time between 1 and 3 sec. The target is then extinguished for SOmsec. At the same time the mirror galvanometers begin tracking the eye but with an offset of half the nystagmus either added on or subtracted off. After the 2 msec test flash occurs, the subject was given a post-stimulus interval without a visual target in which to indicate the laterality of the test flash with respect to X.

1118

HERSCHEL P. GOLDSTEIN er al.

to X before the target reappeared at X for the next computer calculated eye velocity using a 5 point nonpresentation. During a few practice presentations at the causal, linear-phase titer characterized by a ramp pulse beginning of the recording session, the post-flash time response. was adjusted for each subject to a comfortable value that Occasionally, a subject failed to respond to a run of did not rush or bore the subject and ranged between 2 stimuli. When this was noted during the recording and 4 sec. session, the session was temporarily suspended. In all Early in our experience we found that subjects, such cases subjects reported either that the spot target when expecting test Bashes after each di~p~ran~e had become blurry or that they were experiencing of X, became anxious when, for whatever reason, they some slight distracting discomfort with the search coii failed to detect a test flash. To alleviate this anxiety, annulus. Testing resumed after the~installation of artioccasionally the test flash was not presented after the ficial tears or anesthesia and only after subjects were target at X was extin~ish~; subjects were advised of comfortable. Immediately after resuming the session, this. response rates returned to the base level for that subject Analysis of the data started with off line display of which shows that the run of missed stimuli was caused each target presentation as in Fig. 3. A vertical cross hair by wearing the contact annulus and was not indicative was aligned with the flash occurrence, as shown, and of the subject’s normal capability. In light of this, we values for eye position, eye velocity, screen position of felt justified to delete from analysis the run of missed test flash and response were recorded. Each test flash was stimuli. then categorized as to true spatial laterality with respect All subjects were patients at the Foerderer Eye Moveto X, retinal laterality with respect to F and response ment Center. Because of the need to use the search coil according to the scheme shown in Fig. 4. For example, system, only adult subjects were considered. All subjects a label of the form (N 1L, R) or (N 1LR) means no gave informed consent and were naive to the concerns of response was given for a test Aash which occurred to the the experiment. Pertinent patient ~nfo~a~on is preIeft of X in space and at retinal position RR. The sented in Table I.

0 " TARGET BRIGHTNESS i-8.21

-10.07 v

TARGET POSITION

LEE'! RESPONSE RIGifT RESPONSE

I

0:

I

100

I

200

I

I

300

I

I

400

Tim

I

I

500

I

600

I

I

700

800

(MSEC)

FIGURE 3. Example of data record from subject WV as dispkyad during analysis. Hokmtal eye position (de& horizontal twas &Wary unita). Negative ‘pal- dsaote i&ward. eye v&city (de&%@,horizontal target position (de& and tar@% Also shown is the subject’s zwponr: a tightward rcapontroapps%rsin tha &WV at *F %ly data frOm th~,b@ming ofthc~p~tiIthecndcfthcpost~usintnval;ast~.Thac~~~iamsw;*rithO~~~~htbctwt flash.Thevalu#rofthetracesattimeO~notsdas~~~~mdrrqsoRwhbeacy.Af~s~u~~~atvalues

VISUAL REMAPPING

IN INFANTILE

SPACE R

SPACE L

Physical Stimulus

Perceptual Response

REAESP L RESP

R

REdbESP L RESP

REnNA R

RETINA L

RETINA R

RETINA L

t

1119

NYSTAGMUS

RE.d%ESP L RESP

R

Rdd.bSP L RESP

R

R

____________**___________*__*_*-*_____*___-_____*____--_*-_--_*-*----*-*DESIGNATION

RESPONS

(L/L,L)

(NJL.L) (R1L.L) (L/L,R) (N/LB)

(L1R.L) (NIRL)

(R1L.R)

fRIR,L) (L/R,R) (N/R,R) (RIR,R)

RETINA

fv SPACE

FIGURE 4. Response-stimulus combinations were labeled according to the partition shown. A label of the form (N / LR) would be read as “no response to a test flash to the left of X in space and at position R, on the retina.” As another example, Fig. 3 is an example of category (RIRL) -use the target flash position (-8.2 deg) was to the right of the reference X (- 10.0, not shown) but left of the eye’s position (-6.6 deg).

RESULTS Detection

Figure 5 shows how several of our subjects responded flashes over their entire range of eye velocity. Because the test flashes occurred independently of the ongoing nystagmus, the count in each histogram bin reflects the velocity profile of the nystagmus. Figure 6 depicts the d~st~bution within the nysta~~ cycle of stimuli in a phase-plane plot. The density of stimuli detected (solid squares) approximated the density of stimuli missed (open squares) throughout the nystagmus cycle implying that stimuli were not systematically missed during a particular nystagmus phase. Subjects clearly detected stimuli during the nysta~us quick phase when eye velocity could exceed 100 deg/sec [see Fig. 6(B)], although, for some subjects, somewhat lower response rates were found with higher eye velocity. Table 2 summarizes the data according to the scheme of Fig. 4. To make specific points, subsets of the same to test

data are presented in Tables 3-6. Table 3 gives an overall summary of responses devoid of all position information. Except for subject RM the response rate to the flash stimuli was at least 0.80. When the reference spot was not followed by a test flash subjects hardly ever responded (only 2 false positives out of 67 possibilities). This strongly suggests that the disappearance of the reference spot at X did not cue a response and therefore an issued response can be taken, with high probability, as a detection of the flash stimulus. Table 4 summarizes A 80

60

TABLE 1. Patient information

Patient cc

HC BG

DH

RM

WV

Age Sex (yr) F

M M

M

M

M

20

55 18

25

30

60

Waveform at position tested Left-beating jerk with increasing velocity slow phase alternating with small amplitude right jerk

Position tested (dag)

Stimulus eccentricity (deg)

0

2.0

EYE VELOCITY (DEGISEC)

B 60 50

0.93

n

N3RESFcNSE

< -40

-401-20

40

P~ud~ycioid Right-beating jerk with biphasic slow phase

0 Right I5

1.5 2.0

Left-beating jerk with biphasic slow phase

Left 15

Right-beating jerk with extended foveation

Right 20

2.0

Left-beating jerk with increasing velocity slow phase

Left 10

1.5

$ 5 0

30 20

1.0

t0 0 -20/o

0120

20140

> 40

EYE VELOCITY (DEG/SEC) FIGURE 5. Histograms of responses with respect to eye velocity when stimulus was delivered for subjects CC (A) and BG (B). Numbers atop histogrambars are fraction of stimuli eliciting a response. Responses were made for stimuli occurring in all velocity ranges, including quick phases.

1120

HERSCHEL

P. GOLDSTEIN

et ul.

A

Relative Eye Positlon (dag)

-6

-4

-2

0

2

4

6

-5.0

-2.5

Relative Eye Position (dag/aac)

0.0

2.5

5.0

Baiatlve Eye Posltbn (deg/sec)

FIGURE 6. Phase-plane plots showing stimuli presentations for subjects CC (A), DH (B) and WV (C). Solid squares mark stimuli detected and open squares mark stimuli missed. Except for the absence of missed stimuli in the upper right quadrant for subject CC, missed stimuli appear uniformly distributed throughout the nystagmus cycle.

the data as a function of right or left retinal stimulus position. Except for subjects RM and DH, the frequency of detection did not appear to have been related to which retinal locus, RL or RR, was stimulated. Table 5 summarizes the data with respect to the test flash position in space relative to the reference position. Except for RM and WV, subjects responded equally to targets flashed either to the right or left of X.

given retinal locus and whether the visual direction of a retinal locus changes during the nystagmus cycle. Two mutually exclusive hypotheses will be considered: (1) subjects localized the flashed targets according to the retinal locus stimulated, the retina hypothesis; or (2) subjects localized the flashed targets according to the target’s position in space relative to X, the space hypothesis. Considering the scheme of Fig. I and refting to Table 2, response--stimuli pairs (L} LL) and {RI RR) would be true if either the retina or space hypothesis held and are therefore not helpful in distinguishing between them. In contrast, predicted responses to the crossover stimuli (*1RL) or (*1LR) would depend on hypothesis.

Localization Given that IN subjects readily detect flashed targets throughout their nystagmus cycle it is appropriate to wonder what perceived visual direction corresponds to a

TABLE 2. ResDonse count to test flashes Subject

LlLL

NlLL

RiLL

LlLR

NlLR

RiLR

LiRL

NlRL

RlRL

LlRR

NlRR

RlRR

LlN

NiN

R/N

CC HC BG DH RM WV

61 49 46 22 30 16

3 3 0 7 0 12

0 0 0 1 0 5

5 0 1 0

2 2 0 0

I

0

0 0 2 IO 1 0

1 0 I 6 0 24

0 0 0 0 1 0

3 0 4 2 22 0

62 39 51 43 R 68

13 19 14 0 5

0 0 0 0 0

1

0 0 0 2 0 7

0 0 0 0 1

0

2 0 2 1 1 0

1

15

0

L and R mean left and right, respectively. N means either no response or no test flash. A label of the form NlLR means those trials no response was given for a test flash to the left of the X in space and located at position R, on the retina (see Fig. 1).

where

VISUAL REMAPPING

IN INFA~ILE

TABLE 5. Summary of response rates: Spatial laterahty stimulated

TABLE 3. Overall summary of response rates I. Subject

Response rate

CC HC BG DH RM WV

0.94 0.95 0.94 0.80 0.64 0.90

count

Right

Left

Test flash absent

Test flash present

1121

NYSTAGMUS

Response rate

Count

Subject

Response rate

Count

Response rate

Count

0.00 0.00 0.00 -

13 19 14 0 6 16

cc HC BG DH RM WV

0.93 0.90 1.00 0.77

73 54 49 31 32 33

0.95 1.00 0.90 0.81 0.28 1.00

66 39 58 63 32 99

139 93 IO? 94 64 133

0.17 0.07

TABLE 4. Summary of response rates: retinal laterahty

1,oo 0.61

a remarkable ability in the latter group to constancy despite the almost complete instability of retina1 images. Several mechanisms might be postulated to alleviate the oscillospia. First, patients could sample the visual scene only during a particular phase of the nystagmus cycle and suppress vision at other times. Logically the sampling period would correspond to a nystagmus phase where eye velocity was low, such as at those times indicated in Fig. 7 by solid arrows. Such a sampling m~hanism would be consistent with the finding of higher visual acuity in association with higher percentage of low eye velocity during the nystagmus cycle (Abadi & Worfolk, 1989). Furthermore, acuity is improved by extended periods of low eye velocity where the target is imaged near the fovea (Dell’osso & Daroff, 1975). Subjects with IN have been found to have decreased motion perception for movement in the same direction of their nystagmus, either to gratings (Abadi & Sandikcioglu, 1975) or single spots of light (Dieterich & Brandt, 1987). Although helpful in reducing motion cues leading to oscillopsia, decreased motion perception, per se. cannot explain the absence of oscillopsia. At least twice during every nystagmus cycle the eye comes to rest (consider solid and open arrows in Fig. 7). The image of a stationary world would be stationary on the retina at these times. Thus the visual system would need to contend with a sequence of alternating displacements which too should lead, but does not, to perception of motion in IN subjects. How the reported suppression of displacement in association with saccades (Bridgeman, Hendry & Stark, 1975) might relate to alleviation of oscillopsia in IN subjects is not known. So, barring any mechanism other than sampling, only the sampling scheme depicted by the solid arrows in Fig. 7 would alleviate oscillopsia. Clearly, the first step of investigation would be to establish a sampling mechanism if demonstrating

Retinal locus stimulated RR

RL

Subject cc HC BG DH RM WV

maintain

Response rate 0.95 0.94 0.96 0.65 0.97 0.99

COWIt

Response rate

Count

65 52 49 48 31 69

0.93 0.95 0.93 0.96 0.33 0.81

74 41 58 46 33 64

Specifically, responses (L) LR) and (R 1RL) support the space hypothesis while responses (L(RL) and (RI LR) support the retina hypothesis. Crossover stimuli were difficult to achieve but occurred at least five times in subjects CC, WV, and DH. The results are summarized in Table 6. Although the data do not exclusively follow either localization hypothesis, the space hypothesis is favored. When the stimuli occurring within 0.5 deg of X were removed from the analysis, however, the space hypothesis was even more strongly favored, exclusively so in two of these three subjects. This finding suggests that our subjects found it difficult to locate flashes occurring near X, an idea further supported by the near even (0.43:0.57) odds our subjects showed for locating the crossover stimuli within 0.5 deg of X with respect to the space and retina hypotheses.

DISCUSSION Pathological nystagmus is characterized by involuntary eye movement. When of mature onset, the nystagmus is always accompanied by oscillopsia which is in sharp contrast to those patients either born with nystagmus or whose nystagmus developed during infancy where oscillopsia is rarely a problem. thus

spatial

TABLE 6. Summary of response rates to crossover stimuli Crossover All

Control Eccentric only

All

Eccentric only

Subject

Space

Retina

Count

Space

Retina

Count

Correct

Count

Correct

Count

CC DH WV

0.75 0.67 0.77

0.25 0.33 0.23

8 9 31

1.00 1.00 0.84

0.00 0.00 0.16

4 5 26

I.00 0.95 0.76

123 22 21

1.00 0.92 0.84

116 14 I5

In general, the crossover/space column includes (L/ LR) and (RI RL) responses, the cr~sover/retina column includes (RI LR) and (LI RL) responses and the control/correct column includes (Lf LL) and (R] RR) responses. Controls are for the space hypothesis only. Eccentric stimuli were at least 0.5 deg away from the reference spot in space.

1122

HERSCHEL

P. GOLDSTEIN

one existed. Although our previous work argued against the existence of a sampling process, the experimental design failed to eliminate the possibility that the image of a test Aash occurring during a visual suppression phase could persist, perhaps as an afterimage, and be appreciated at a later phase when vision was not suppressed (Jin et al., 1989). The present study addresses this issue. We first con&m our previous conclusion that IN subjects see flashed targets presented throughout their nystagmus cycle and then argue that our localization data contradicts any kind of sampling mechanism. Visibility of targets and retinal stabilization There were two reasons why these experiments were not done with a dark background. Firstly, it was not possible to eliminate all leakage of laser light on the screen. Leakage arose from light scattered amongst optical eiements on our optical rail and from stray t~nsmission through the acoustic-optic modulator. The brightest leakage measured about 0.01 cd/m*. Secondly, oscillopsia is absent at photopic viewing conditions and thus an illuminated background was preferred to avoid dark adaptation. Using a bright background luminance, however, made detecting flashes more difficult. In our previous experience (Jin et al., 1989), subjects showed great variability in contrast sensitivity. In the end, we compromised on a constant mesopic background luminance of 1 cd/m2 that would suit all of our subjects. Test flash luminance was 1 kcd/m*, a full 3 log units above b~kgro~d and was the brightest Aash possible, This level was about a log unit brighter than the reference spot. Although keeping all targets equiltinent seems desirable, on one hand, subjects tended to feel the reference target at 1 kcd/m’ un~omfortabiy bright but, on the other hand, subjects found test flashes at 100 cd/m* were more difficult to detect. In any case, al1 subjects were shown continuous, screen-stationary targets of each brightness used and all subjects reported the targets as stationary. A test flash duration of 2 msec was chosen because it was the shortest reliable duration we could obtain using

-

-6

8 F -7 iii ,o -6 !z w -9

0

500

1000

1500

MSEC

FIGURE 7. In a jerk nystagmus, sampling the visual Scene at the times indicated by the solid arrows would go a long way to alleviate osciliopsia as the eye is close to the same position at these times. If the sampling included other times during the cycie having low eye velocity (indicated by the open arrows), the image would appear to jump back and forth.

et al.

our software. Short duration flashes confined the stimuli to narrow velocity ranges and minimized any image smear caused by eye movement. Specifically, the image of a 2 msec flash would be smeared 0.2 deg on the retina during a IOOdeglsec nystagmus quick phase. This is approximately the diameter of the spot itself. For eye movement less than 20deg/sec, the predominate case, image smear would not exceed 0.04 deg (2.4 min ax) which is about 5 photoreceptors at the fovea. Furthermore, the 10 msec rise time of mirror movement preeluded electronic feedback of eye position to effectively reduce the stimulus smear, despite active feedback during the stimulus. It is important to note that retinal stabilization of the test flashes was not intended to reduce retinal image smear but to control the loci of retinal positions stimulated, that is, to place all stimuli at R, or R, irrespective of eye position. For example, subject BG’s eye position varied over a range that exceeded 10 deg. No direct method was available to measure the overall precision of stabilization but stabilizing the target under viewing conditions identical to the test conditions caused fading in one of the authors (MF. no nysta~us~. Eflects of miscalibration During calibration we attempted to align point F as defined in Fig. 1 to the fovea. This was done by ass~ing that the nystagmus quick phase brought the target-s image on the fovea as was noted by Dell;Osso, Daroff and Troost (1989). The normal sensitivity vs fovea1 eccentricity curve is steep and approximately symmetric within O-5 deg of the fovea centralis. Assuming normal sensitivity in our subjects, aligning F with the fovea would minimize differences in retinal ~nsitivity between the two test positions RL and RR. The asymmetrical detection rate in subject RM and DH, in fact, most likely reflects our failure to precisely make this alignment. Do note, however, that any conclusion based on changed visual direction is not affected by any consistent misalignment of F and the fovea. ~etert~on The data of Table 3 clearly shows that all our subjects responded to most of the test flashes and Fig. 5 shows that those responses did not depend much on eye velocity during the nysta~us cycle. That only 2 false positive responses were registered out of 67 trials in which no test flash occurred further supports our conclusion that the test flashes were truly detected and not merely surmised by the disappearance of the reference spot. Indeed, test flashes were even detected during quick phases but because of the bright fiashes used, it was not possible to evaluate the degree to which the detection threshold might increase during the quick phase as has been noted during saccades. It would be of interest to assess visual suppression during quick phases given the similarity of quick phases and saccades (Abadi 8z Worfolk, 1989) and that visual suppression during voluntary saccades has been reported to be approx. 0.5 log units (Volkmann, 1962).

VISUAL REMAPPING

IN INFANTILE

For all subjects except subject RM overall response rates exceeded 75% and for subjects CC, HC and RG response rates exceeded 90%. We can speculate why our subjects failed to respond after some stimuli. One obvious possibility is that the subject happened to blink during the flash presentation but such instances could be identified from the vertical eye movement channel. We also know from our previous work that the contrast ratio between the test flash and the background needed for detection varied from subject to subject. Some subjects easily saw target flashes that other subjects. under identical viewing conditions, found difficult to detect. It is also probable that the subject’s level of attention would influence the detection rate. Although we encouraged our subjects throughout each recording session, momentary lapses of concentration on the part of our subjects leading to missed detections could not be avoided. As noted previously, the search coil distracted subjects somewhat. In addition, when queried after the recording session, some subjects, reported that occasionally, even though they saw a test flash, they did not respond in the allotted time because they were unable to decide where to locate the test flash. Indirect, but striking, evidence supporting the last claim could be found in the data of subject WV where, curiously, in most all trials where test flashes elicited a response, the nystagmus pattern abruptly changed during the short time interval prior to the response. In these cases, a quick phase was apparently delayed which exposed an extended slow phase or even cascaded slow phases without a change in eye movement direction. The ensuing quick phase, which was larger than usual, evidently reflected the increased slow phase excursion. By contrast, in trials without test flashes, the nystagmus continued without change. We surmise that the nystagmus change indicated the subject’s shift of attention from detecting flashes to deciding how to respond. Using this indirect means to assess detection, of the 13 flash trials subject WV did not respond to, 4 were probably detected. Interestingly, these 4 appeared within 0.66 deg of the reference position and therefore might have been difficult to locate in the time allotted. Three other subjects showed idiosyncratic but more subtle nystagmus changes after detection: for example, subject CC’s bidirectional nystagmus changed to a unilateral one. The nystagmus of subjects HC and DH showed no obvious changes. Localization

In three subjects (CC, DH and WV) we obtained at least 5 responses to crossover stimuli. Although not exclusively so. our subjects more consistently localized the test flashes according to the space hypothesis rather than the retina hypothesis. Thus, our subjects associated stimulation of a single retinal locus with at least two different perceived spatial locations depending on eye position during the nystagmus cycle. In visual psychophysics, the perceived spatial position corresponding to a particular retinal position lies along the visual direction associated with that retinal locus. Hence, in those terms, our subjects clearly demonstrated an ability to dynami-

NYSTAGMUS

1123

cally alter visual direction. Information leading to the alteration of visual direction can either come from the retina or from an extraretinal source. Classically, localization of objects in a visual scene is based on the notion of local signs which says that neighboring points in the physical scene maintain their neighborliness and their directional relations as the information is processed within the visual system. This is equal to saying that the light distribution maps conformally throughout the visual system. How our subjects could alternatively make use of local signs to localize the test flash with respect to the reference spot is not at all clear. Normal subjects with good fixation can easily remember the position of the reference spot, thereby providing an internal reference to which the position of a test flash can be compared. Visual persistence of the reference spot would also aid the process. Nystagmats, however, image the reference spot over a range of retinal loci offering. in contrast to normals, an indistinct retinal area to which the position of the test flash might be compared. Test flashes followed the offset of the reference spot by only 50 msec and thus occurred while the image of the reference spot would be expected to have persisted assuming that visual persistence in nystagmats was normal, an issue yet to be investigated. In this short amount of time the shift in eye position was typically less than 1 deg. Thus it is possible that the test flash was referred to the last visibility of the reference spot. But this seems unlikely for if local sign were the only basis for locating the test flash, the same local sign information would be expected to cause the reference spot to be perceived, not as a spot, but as a streak reflecting the smearing of the spot’s image on the retina. On the contrary, all of our subjects reported the test spot to be about the same size as the reference spot despite the 4 deg typical smearing of the reference spot during the nystagmus cycle. Certainly, the perceived target motion when a spot is stabilized on the retina is incompatible with a local sign hypothesis given that an unchanging retinal stimulation would not provide sufficient local sign information. This issue can be further studied in the future with trials having a longer delay between the offset of the reference spot and the occurrence of the test flash. In summary, if subjects used local signs exclusively then they must have sampled the scene, and if they sampled they would have mislocalized the test flashes in space, i.e favored the retina hypothesis. That they usually localized the flash stimuli correctly in space argues against the sampling hypothesis. Instead of using local signs our subjects, more likely, used an extraretinal source of information to modify the visual direction of the retinal loci stimulated. Whether the extraretinal information came from inflow or outflow was not addressed in our study and the following discussion leaves open the possible source. An extraretinal source is consistent with the oscillopsia reported with stabilized images and circumvents the problems of visual persistence and smear complicating the local sign hypothesis. The use of extraretinal information to modify visual

1124

HERSCHEL

P. GOLDSTEIN

direction has long been suggested as the mechanism of spatial constancy during saccades. Two points preclude the assumption that this is simply the same mechanism used by nystagmats to alleviate their oscillopsia. First the shift of visual direction during a saccade does not follow the saccade trajectory but instead begins at least 100 msec before the saccade and ends hundreds of msec after the saccade (Matin, 1976). The precision with which our subjects could localize implies a closer temporal match between eye position and the shift in visual direction. Secondly, visual localization during slow eye movement need not involve extraretinal info~ation. For example, the iocalization of visual targets during pursuit eye movement apparently follows local sign rather than using extraretinal information (Festinger, Sedgwick & Holtzrnan, 1976). On the other hand, visual localization during vestibularly induced slow eye movement does make use of the extraretinal vestibular signal. In any case, if the visual persistence of our nystagmats proves normal then one must assume that the cancellation mechanism is applied further along in visual processing than the persistence mechanism. When test flashes occurring within .OS deg of the reference spot were ignored (Table 6), the space hypothesis was increasingly favored suggesting that locating test flashes near the reference spot was less precise. Image blur caused by wearing the scleral coil probably was a factor but we did not assess vision after the recording session.

et a/.

jerk waveforms have been shown to be metrically similar to saccades and thus have been likened to corrective saccades (Yee, Wang, Baloh & Honrubia, 1976), SO it would be surprising if the waveform generator actually coded the saccades. More likely, the generator sources a smooth eye position or eye velocity leaving the quick phases to be generated by the brainstem, presumably as refixating saccades or as resetting saccades akin to the quick phases of vestibular or optokinetic nystagmus. The changed nystagmus in the poststimulus period, as noted above, would support this claim.

REFERENCIES Abadi, R. V. & Sandikcioglu, M, (1975). Visual resolution in congenital pendular nystagmus. Americun Journal afQp~ome~ry and Physiological Optics, 52, 573-58 1. Abadi, R. V. & Worfolk, R. (1989). Retinal slip velocities m congenital nystagmus. Vision Research, 29. 195-205. BAseman, B., Hendry, D. & Stark, L. (19751. Failure to detect dispIacement of the visual world during saccadic eye movements. Vision Research, 15, 719-722. Collewijn, H., van der Mark, F. & Jansen, T. C. (1975). Precise recording of human eye movements. k’ision Research, I5, 447-150. Dell’Osso, L. F. & Daroff, R. B. (1975). Congenital nys~~~ waveforms and foveation strategy. Documenta Ophthalmology. 39, 155-182. Dell’Osso, L. F. & Leigh, R. J. (199Ot. Foveation periods and oscillopsia in congenital nysta~us. ~n~e.~r~gur~ve Ophi~atagy and Visual Science, 31, 122. Dell’Osso. L. F. & Leigh, R. J. (1991). Required ocuiar motor conditions for visual constancy. Imlesrigarive Ophthulmotogy and Visual Science, 3.2, 901.

Synthesis Maintenance of spatial constancy during eye movement confronts all animals. When one, for example makes saccades in iooking around a constant room scene the brain does not misinterpret the persaccadic image smear and sudden image shift as a shift of the world but properly associates the retinal stimulation with an eye movement. Our results suggest a similar mechanism is used by IN subjects as one means to alleviate their oscillopsia. Plausibly, the output of the IN waveform generator feeds into both a preoculomotor area and perception center or, alternatively, the output of the IN waveform generator feeds into only the preoculomotor area. In the latter case, the signal informing the perception center about eye position could come from either a central copy of oculomotor output, so-called efference copy, or from orbital proprioception. Either mechanism would automati~lly compensate for every nystagmus pattern. But recently reported cases seems to suggest that the final motor output or orbital proprioception is not the source. Dell’Osso and Leigh reported that the transient development of oscillopsia in nystagmats corresponded to an abruptiy changed nystagmus pattern (Dell’Osso & Leigh, 1990, 1991). Therefore, subjects could not perceptually compensate all nystapus patterns. Because of the often complex IN waveform it S@mS unlikely that the IN waveform generator directly drives the motoneurons. Specifically, the quick phases rn

Dell’Osso, L. F., DaroIT, R. B. Br Troost, f3. T. (1989). Nystagmus and saccadic intrusions and oscillations. In Jaeger, E. (Ed.) Clinical ophthalmology. Philadelphia: Lippincott. Dieterich, M. & Brandt, T. (1987). Impaired motion perception in congenital nysta~us and acquired ocular motor palsy. C&tic& Vision Sciences, I. 337-345. Festinger, L., Sedgwick, H. A. & Holtzman J. D. (1976). Visual perception during smooth pursuit eye movements. Vision Research, 14, 703-7 11.

von Helmholtz, H. (1926). P~~siotogicat optics. (3rd Edn) translated by Southall, J. P. C. New York: Dover. Jin, Y. H., Goldstein, H. P. % Reinecke, R. D. (1489). Absence of visual sampling in infantile nystagmus. Komun J. Opttdai. 3,28-32. Leigh, R. J., Dell’Osso, L. F., Yaniglos, S. S. % Thurston, S. E. (1988). Oscillopsia, retinal image stabilization and congenital nystagmus. Investigative Ophrhatmology and Visual Science. 29, 279-282. Matin, L. (1976). Saccades and extraretinal signal for visual direction. In Monty, R. A. & Senders, J. W. (Ed@, E_ve ma~emenrs and ps~chotagjcat processes. Hill~aIe, NJ.: Erlbaum. Nom, M. S. (1964). Congenital idiopathic nystagmus. Acra Ophthatmologica, 42, 889-896.

Reinecke, R. D.. Guo, S. & Goldstein. Ii. P. (1988) Waveform evolution in infantile nysta~us: An ei~tr~ulo-chin study of 35 cases. Binocutar Vision, 3. 191-202

Robinson, D. A, (1963). A method for measuring eye movement using a scleral search coil in a magnetic field. IEEE Xransacrions on Bio-Medical Electronics, IO. 137-145. Volkmann, F. C, (1962). Vision during voluntary sifccaddic eye movements. Journat of Opricat Society of America, 52 571-578. Yce, R. D., Wong, E. K., Baloh. R. W. & Honrubia, V. (1976). A St&Y of congenital nystagmus: Waveforms. Neurofogv. 26, 326-333.

,&/cnowtedgcmenrs-The authors wish to thank Drs R. Reineckeand _i_. BIumenfeId _.~~~ for their comments on the manusniPt.