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Smooth pursuit eye movements of normal and schizophrenic subjects tracking an unpredictable target
BIOL PSYCHIATRY 1990;28:705-720
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Smooth Pursuit Eye Movements of Normal and Schizophrenic Subjects Tracking an Unpredictable Target John S. Allen, Katsuya Matsunaga, Selim Hacisalihzade, and Lawrence Stark
An experimental paradigm employed by several workers in the field of schizophrenic eye movements has involved finding sequences of stimuli that induce saccadic smooth pursuit in the eye movements of normal individuals. It is hoped that the identification of such stimuli will lead to clues concerning the etiology or nature of eye tracking dysfunction in schizophrenia. In this study, the pursuit eye movements of normal and schizophrenic subjects tracking an unpredictable target (composed of summed sine waves) were examined. Eye tracking performance was evaluated both qualitatively and quantitatively using percent root-mean-square (%RMS) error and pursuit gain scores. Schizophrenics are capable of tracking an unpredictable target. Th;,s finding has implications for our understanding of schizophrenic information processing during visual tracking.
Introduction An experimental paradigm employed by several workers in the field of schizophrenic eye movements has involved finding sequences of stimuli that induce saccadic smooth pursuit in the eye movements of normal individuals (Brezinova and Kendell 1977; Lipton et al 1980; Mather and Puchat 1983; Mather 1986; Kaufman and Abel 1986). It is hoped that the identification of such stimuli will lead to clues concerning the etiology or nature of eye tracking dysfunction in schizophrenia. One way to induce low gain smooth pursuit and to increase the number of saccades in a normally tracking irldividual is to use an unpredictable target (Stark et al 1962; Michael and Jones 1966; Bahill, et al 1980). The smooth pursuit system employs "adaptive predictor that allows the system to overcome its innate delays upon exposure to a regular input pattern." (Stark et al 1962, p. 52). According to the Billheimer-Stark model (Stark 1971), learning a predictable targe~'s path involves a three-stage process: (1) a nonpredictive stage, during which the target is first encountered; (2) a transient
From the Department of Anthropology, University of California at Berkeley, Berkeley, California (J.S.A.), the Depadment of Psychology, Faculty of Literature, Kyushu Universiq', Fukuoka, Japan (K.M.), the Department of Control Engineering, ETH, Zurich, Switzerland (S.H.), and the Telembotics and Neurology Unit, University of California at Berkeley, Berkeley, California (S.H.; L.S.) Address reprint requests to D,'. John S. Allen, Pathology Research (i51B), Palo Alto VA Medical Center, Palo Alto, CA 94304. Received November 7, 1989; re~sed March 31, 1990. © 1990 Society of Biological Psychiatry
0006-3223/90/$03.50
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stage, during which learning takes place; and (3) a final steady stage, wherein the target motion is being tracked in a predictive fashion. The progress of the subject through these three stages can be followed and quantified using a five-state, partitioned Markov matrix. Bahill and McDonald (1983) found that humans can learn and accurately track any predictable waveform that is smooth and periodic. With an unpredictable target, the clues by which a tracking subject learns to make accurate predictions are by definition absent. Stark et al (1962) noted that the decrease in phase lag seen in subjects tracking a predictab!e rather than an unpredictable target was evidence for the existence of an "adaptive predictor." Although learning undoubtedly plays a role in the accurate anticipation of future target motion of a predictable target, for an unpredictable target, previous target motion is used without conscious thought or effort by subjects to generate expectations concerning the future motion of the target. Kowler et al (1984) found that through the use of a different finite-state Markov model, they could characterize the anticipatory eye movements of a subject who is track:~ng an unpredictable target. Thus it appears that there are two levels of prediction generation: during the tracking of a predictable target, the overall, periodic pattern of the target is learned, and accurate predictions of future target motion are made based on the learned pattern; for an unpredictable target, predictions (which will ultimately be inaccurate), or amicipations, are made based on immediate prior target motion, since there is no general pattern to learn. In this article, the eye movements of normal and schizophrenic subjects tracking an unpredictable target composed of six randomly summed sine waves will be described. The smooth movement of the unpredictable target used in this enperiment (see Figures 1 and 2 for examples of the target and typical subject responses) might be termed "continuous," as opposed to the unpredictable step-ramp target used by Levin et al (1988). Implications of these results for the more general problem of smooth pursuit dysfunction in schizophre, ia, with special reference to the issue of deficits in preregistration and/or postregistration information processing (Braff 1981; Braff and Saccuzzo 1985; Miller et al 1979), are examined in the discussion section.
Materials and M e t h o d s
Subjects Subjects consisted of 14 normal individuals [9 men, 5 women, mean age (_+ SD) 26.1 _ 7.3 years, range 20-47 years] and 16 chronic schizophrenics (11 men, 5 women, 36.9 -+ 6.1 years, range 29-46 years). Schizophr¢iii¢ :~.~bjects were recruited and examined at Motobu Kinen Psychiatric Hospital in Okinawa Prefecture, Japan. The diagnosis of schizophrenia was made by the hospital's clinical psychiatric staff and was based on Schneiderian criteria. Primary symptoms included auditory hallucinations (10 subjects), paranoid delusions (7 subjects), and hebephrenia (4 subjects). Normal subjects were recruited from the hospital staff and among the student population of Kyushu University, Fukuoka, Japan; they were screened for personal and familial histories of mental illness. Although the schizophrenic subjects in this experiment were older than the normal subjects, and the smooth pursuit system has been described as an "age-dependent motor system" (Sharpe and Sylvester 1978), no previous study has demonstrated a significant age-dependent decrease in smooth pui'suit ability in subjects below the age of 50 years. The oldest psychiatric subject in this study was only 46 years old, and thus age was
Eye Movements of Normal and Schizophrenic Subjects
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unlikely to have been an important contributor to observed differences in smooth pursuit performance between the two subject populations. All schizophrenic subjects were receiving standard (phenothiazines and/or haloperidol) antipsychotic medication. It has been demonstrated in numerous studies that these drugs do not affect smooth pursuit eye movements. In addition, patients received a small dose (30-40 mg) of phenobarbital with their bedtime medication. At least 12 hr passed between the administration of the bedtime medication and the examination of eye movements. Given the time course of the effects of barbiturates on smooth pursuit eye movements (Norris 1968), it is unlikely that these drugs had a significant effect on the sclofizophrenics' eye movements. In a larger study (Allen et al 1990) done in conjunction with the present experiment, a comparison between barbiturate-free schizophrenics and those who had received a small dose of the drug with their bedtime medication showed no significant differences in smooth pursuit performance between the two groups.
Experimental Task vnd Data Acquisition Subjects were required to track with their eyes a sinusoidal target moving across +_ 15 degrees of the visual field. The target, a white cursor (approximately 2 para across) of light against a dark background, was displayed using an oscilloscope driven by a wave generator. Four target frequencies were used: 0.2, 0.4, 0.6, and 0.8 Hz, plus th~ unpredictable target. These frequencies correspond to average velocities of 12, 24, 36, and 48 degrees/sec, respectively. The random target was generated by randomly summing six sine curves (0.2, 0.4, 0.6, 0.8, 1.0, and 1.2 Hz) on a computer, followed by digitalto-analog conversion of this file to tape. The tape was then input to the oscilloscope, where it would drive the cursor ir~ an unpredictable (to the subject) fashion. The target was actually pseudo-random, and it had a periodicity of about l0 sec. Subjects tracked for at least 30 sec at each target frequency. Subject performance was continuously monitored and verbal prompts (e.g., urging the subject not to blink and to attend to the tracking task) were made as nccessary. Frequent calibration trials were made using a slow (0.2Hz) square-wave target. Aftqr tracking the four predictable sinusoidal targets, the subject tracked the unpredictable target for approximately 30 sec. Eye movements were measured monocularly (left eye) using the high-resolution photoelectric method (infrared reflectometry) to directly record eye position (Stark et al 1962). Photocells were mounted on lensless eyeglass frames, and a chin rest was used to restrain head movement. Target and eye position signals were recorded simultaneously on a multitrack cassette data recorder. Chart recordings of the data were examined, and those portions of the eye movement signal without artifacts (blinks, etc.), along with the corresponding target signal, were digitized over 12 bits at 60 Hz and stored on disk for processing and quantitative analysis.
Data Analysis After linear transformation of the eye signal based on calibration results, the root-meansquare (RMS) error between target and eye position was determined. For the predictable targets, the RMS error was determined by overlapping 10-sec periods at l-sec intervals over the entire subject run (up to 30 sec) at each target frequency. The 10-sec period with the lowest position RMS score was saved on disk. For the unpredictable target, RMS position error scores were calculated over the entire 30-sec trials, rather than
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sampling the ten seconds with the lowest score. RMS scores were normalized by assigning a zero-eye-movement run (eye position fixed at zero degrees) an ewor score of 100%. Calculation of the gain was the same for predictable and unpredictable targets. A Fast Fourier Transform (FFT) was performed on the time functions of the stimulus, s(t), and the subject's response, r(t). This yielded the stimulus, S(w), and response, R(w), in the comr~lex frequency,domain. The gain in decibels at a given frequency, fl, was then defined as G(II) = 20 log
with IR(~)I and IS(fl) I denoting the amplitudes of the complex valued response and stimulus functions at the given frequency II (Oppenheim et al 1983). Before the gain was calculated, saccades were identified using a velocity threshold of 42 degrees/see and removed from the eye movement sig~.al; they were replaced by linear interpolations between the points immediately preceding and following the deleted saccades. At this velocity threshold, some small saccades (< 1 degree in amplitude) could have been missed by the filter, and thus higher velocity epochs may have been included :,n the calculation of gain. The eye movement signal was then smoothed, using a three-point moving average. The resulting gain score is perhaps better described as the "single-mode tracking gain" (Bahill et al 1980). Qualitative analyses of the predictable eye movements only were performed by two blind raters examining the complete (up to 30 see) 0.4-Hz chart recordings. A five-point scale (1 = good, 3 borderline, 5 -= poor) was used to score eye tracking performance. A subject's tracking was considered abnormal if it received an average score greater than 3. In the larger study (Allen et al 1990) done in conjunction with the present experiment, the eye movements of 88 schizophrenics and 37 normal subjects were qualitatively scored. Interrater reliability was high (r 2 = 0.81), and in 93.2% of the cases, the two raters gave identical scores or scores within 1 point of each other. The unpredictable eye movements were not qualitatively scored. Results Position plots of two normal subjects tracking the unpredictable stimulus are presented in Figures la and lb. Similar plots for two schizophrenic subjects are presented in Figures 2a and 2b. Note in all cases the saccadic nature of the pursuit. The normal subject in Figure l a demonstrates excellent tracking of the unpredictable target, although he overshoots the target consistently during rapid target direction reversals. The normal subject in Figure lb scored close to the average for %RMS error; her performance is characterized by an abundance of "catchup" and "look-ahead" (perhaps anticipatory) saccades. The eye movements of the schizophrenic subjects in Figures 2a and 2b are characterized by an abundance of catchup saccades and a relative lack of look-ahead saccades. Qualitative scoring on the basis of the 0.4-Hz chart record showed that 2 of i4 (14%) of the normal subjects and 14 of 16 (88%) of the schizophrenic subjects had abnormal smooth pursuit for a predictable target. The results of the %RMS score analysis are presented in Table 1. Schizophrenics scored significantly worse than normal (Mann-Whitney test, p < 0.01) at all target frequencies and for the unpredictable target. Note that the ratio of the schizophrenic to the normal score (Sc/N) decreased for the unpredictable target relative to the predictable
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Table 1. Mean (Standard Deviation) of %RMS Position Error Scores for Normal and Schizophrenic Subjects" %RMS position error
0.2 Hz Normal Schizophrenic Sc/N
14.4 (6.3) 26.9 (13.2) 1.9
0.4 Hz 14.3 (5.0) 26.7 (14.0) ! .9
0.6 Hz 21.0 (5.4) 38.7 (14.9) 1.8
0.8 Hz 27.4 (7.2) 51.8 (13.4) :..9
Unpredictable 39.8 (7.2) 66.2 (15.1) 1.7
°For all measures, at all predictable frequencies and for the unpredictabletarget, schizophrenics ~ored considerablyworse than normals (nonparametric Mann-Whitney Test, p < 0.01).
target scores. Although this statistic may not be a "real" value, when combined with an examination of the plots it is quite apparent that schizophrenics are capable of tracking the unpredictable target, and that the decrease in their performance is comparable to the decrease in the performance of normals. In Table 2, percentile equivalents of %RMS score for both nocmals and schizophrenics tracking the predictable target at 0.4 Hz and the unpredictable target are shown. Note that there is no overlap between normals and schiz,~phrenics for %RMS score during tracking of the unpredictable target. This confirms the results of Levin et al (1988), who showed no overlap in tracking performance (measured by steady-state gain) between normals and schizophrenics during tracking of an unpredictable step-ramp stimulus. The results of the single-mode tracking gain analysis are presented in Table 3 and Figure 3. Confirming the findings of Yee et al (1987), for the predictable target frequencies, normals showed higher gain pur~uit than did schizophrenics (Mann-Whimey test, 0.01 < p < 0.09); this was also true for the unpredictable target, although less significantly so (0.09 < p < 0.20). For both normal and schizophrenic subjects, gain scores for the unpredictable target were significantly lower than the corresponding frequency score for the predictable target (p ~< 0.01); the exception was at 0.8 Hz, where gain scores for predictable and unpredictable targets were not significantly different for either normals or schizophrenics. This is not surprising, given that while tracking a 0.8Hz predictable target, the eye movements of many normal subjects are saccadic, and single-mode pursuit gain obviously decreases. The average target velocity at 0.8 Hz is 48 degrees/see; peak velocities range up to about 70 degrees/see, a value that approaches the upper limit of pursuit velocity [about 100 degrees/sec, according to Meyer et al (1985)]; t:nder normal circumstances, the pursuit system does not try to follow a target moving faster than 30 degrees/see (Stari;, i983). Another explanation for the lack of a significant difference at 0.8 Hz may be that there was too little power in the input spectrum at that frequency. In Table 4, percentile equivalents for normals and schizophrenics for pursuit gain at 0.4 Hz for the predictable and unpredictable targets are preseW~'d. Unlike Levin et al (1988), we found that gain discriminates the two populations les., well than other quantitative measures of performance. One reason for this may be that the "gain(s)" being measured in the two experiments are sotnewhat different entities. In Levin et al (1988) the "gain" was a steady-state r,,ain calculated by taking the ,'atio of the eye and tat-get velocities while the eye passed through the primary position during tracking of the stimulus. The "gain" in this experiment was a single-mode pursuit gain calculated in the frequency domain by taking the FFT over the entire eyt: movement signal. By making
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Table 2. Percentile Equivalents for %RMS Error Scores for Normal and Schizophrenic Subjects Tracking the Predictable Target at 0.4 Hz and the Unpredictable Target
%RMS error
Percentiles at 0.4 Hz predictable N
Sc
Percentiles for the unpredictable target N
100 98 96 94 92 90 76 74 72 70 68 66 64 62 60 58 56 54 52 50 48 46 44 42 40 38 36 34 32 30 28 26 24 22 20 18 16 14 12 10 8 6 0
Sc
100 93.8
100
81.3 75.0
62.5 56.3 50.0 37.5 25.0 18.0 0 100 85.7 71.4 50.0
100 92.3 85.7 78.6 64.3 50.0 28.6 14.3 0
93.8
35.7
87.5 8i.3 75.0 62.5 50.0 43.8 37.5 25 18.8
28.6 15.3 7.1 0
6.3 0
Eye M o v e m e n t s o f N o r m a l and S c h i z o p h r e n i c Subjects
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Table 3. M e a n G a i n S c o r e s ( S t a n d a r d Deviation) for N o r m a l a n d S c h i z o p h r e n i c Subjects T r a c k i n g Predictable a n d U n p r e d i c t a b l e Targets" Predictable gains
Normal Schizophrenic Sc/N
0.2 Hz
0.4 Hz
0.6 Hz
0.8 Hz
- 0 . 2 (0.6) - 1.1 (1.2) 5.5
- 0 . 5 (0.6) - 1 . 0 (1.1) 2.0
- 1 . 9 (0.8) - 3 . 2 (1.8) 1.7
- 4 . 9 (1.4) - 6 . 7 (3.0) 1.4
p = 0.04
p = 0.09
p = 0.01
p = 0.04
Unpredictable gains
Normal SchizophrenicSc/N
0.2 Hz
0.4 Hz
0.6 Hz
0.8 Hz
- 2 . 7 (2.5) - 3.9 (4.1) !.4
- 1 . 8 (1.4) - 2.6 (2.6) 1.4
- 4 . 8 (1.3) - 5.1 (2.3) 1.1
- 4 . 1 (1.8) - 5.4 (2.7) 1.3
p = 0.09
p = 0.09
p = 0.20
p = 0.15
°For both normal and schizophrenic subjects, gains scores for the unpredictable target were significantly lower than the corresponding frequency score for the predictable target (Mann-Whitney test, p ~<0.01); the exception was at 0.8 Hz, where gains for predictable and unpredictable targets were not significantly different for either normals or schizophrenics. The statistical significances (derived from Mann-Whitney tests) for population diffc~nencesbetween normals and schizophrenics are listed below the appropriate columns.
use of the entire signal, the reduction in gain seen in schizophrenics relative to norraals may have been dampened due to the effects of incorporating periods of target reversal in the calculation of gain. Because the unpredictable target reversed directions more frequently than the predictable target, the dampening or averaging effect would be increased. In addition, the velocity filter used to eliminate saccades before the calculation
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0 Normal Predictable [] Normal Unpredictable
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0 SchizophrenicPredictable @ SchizophrenicUnpredictable
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0'.6
0'.8
Frequency (Hz) Figure 3. F r e q u e n c y versus m e a n gain for n o r m a l s a n d s c h i z o p h l e n i c s tracking the predictable and u n p r e d i c t a b l e targets. See text for discussion.
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Table 4. Percentile Equivalents for Pursuit Cain at 0.4 Hz for Normal and Schizophrenic Subjects Tracking the Predictable and Unpredictable Targets
Gain (dB)
Percentiles at 0.4 Hz (predictable) N
Sc
Perce-~,tiles at 0.4 Hz (unpredictable) N
100
2.6 2.0 1.4 1.2 i.0 0.8 0.6 0.4 0.2 0.0 -0.2 -0.4 -0.6 -0.8
93.8
100 100 93.8 100 92.9 736 64.3 57.1 ,~2.3
- !.0 - 1.2
14.3
- 1.4 - 1.6 -1.8
-2.0 -2.2 -2.4 -2.6 -2.8 -3.0 -3.2 -3.4 -3.6 -3.8 -4.0
Sc
88.0
87.5 75.0 62.5 56.3 50.0 43.8 37.5
7.1 0
92.9 85.7
78.6
81.3
71.4 64.3 25.0 12.5
6.3 0
57.1 42.9 35.7 28.6 14.3 7.1 0
75.0 68.8 62.5
31.3
-5.2
18.8
-5.6
12.5
-7.8 -8.0
6.3 0
of pursuit gain may have missed some very small saccades, and thus the presence of hlgher-velocity movements in the eye signal would result in higher pursuit gain scores. k~ain score ratios for each frequency were lower for the unpredictable than for the predic able target; again, it is apparen" that the unpredictable target leads to a decline in tracking t}erformance that is similar for both the normal and schizophrenic subjects. Figure 3 shows the typical reduction h~ gain with increasing target frequency seen in individuals tracking a predictable target (Bahill et al 1980; Stark et al 1962); it also illustrates that
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Table 5. Coefficients of Variation [CV = ± 100 x (SD/mean)] for %RMS Position Error Scores (Note That Unpredictable CVs Are Smaller Than Predictable CVs for Both Normal and Schizophrenic Subjects) CV for %RMS Position Error Score
0.2 Frequency (Hz) Normal Schizophrenic
44 49
0.4 0.6 (Predictable target) 35 52
26 38
0.8
Unpredictable target
26 26
18 23
low-gain pursuit distinguishes the eye movements of schizcphrenics from normals, albeit ~ess strongly than do measures that incorporate the effects of saccadic intrusions and saccadic smooth pursuit (Yee et al 1987). In Table 5, coefficients of variation [CV = +__ 100 x (SD/mean)] are given for %RMS position scores. The CVs for the unpredictable target are smaller for both populations and at all frequencies. Bahill et al (1980) noted that intersubjeet variability decreased when going from a predictable to unpredictable target. These CV data confirm this, and also show that the schizophrenic response is similar to that seeil in the control population.
Discussion In a broad sense, this examination of eye movements of schizophrenics while tracking an unpredictable target belongs to the general body of work done on attention and schizophrenic eye movements. The earliest studies in this area (Shagass et al 1976, followed by Holzman et al 1976; see Holzman 1987 for a more recent discussion) attempted to study the "engagement of attention," and target characteristics were varied (e.g., requiring subjects to read a number superimposed on a smooth pursuit targe0 in an ~ttempt to enhance attention and smooth oursuit performance. In general, it was concluded that schizophrenics do not track poorly because of voluntary inattention, but because of a "failure of cognitive centering, in spite of a desire to do the task" (Holzman et al 1976). Another possible way to learn something about the effects of attention on schizophrenic eye movements is to identify circumstances in which the performance of a normal individual can be made to resemble that of a schizophrenic. For example, Brezinova and Kendell (1977) found that normals distracted by a serial subtraction task or whose attention was impaired by prolonged eye tracking produced eye tracking abnormalities that they could not distinguish (using a five-point qualitative scale) from those found ir schizophrenics. They suggested that (p. 63) "the deviant eye tracking observed in mm~y schizophrenics is simply a reflection of their decreased ability to focus and attend in a consistent manner, and so of no greater aetiological significance than their other psychomotor deficits." This work prompted a response by Lipton et al (1980), who in replicating Brezinova and Kende!l's experiment, found that they could easily, using both quantitative (the velocity arrest score) and qualitative (blind raters could classify the eye movements of normal, normal-distracted, and schizophrenic subjects into their respective categories) methods, distinguish t~,~ eye movements of distracted no~'mals from those of ~;chizo-
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pba-enics. Mather (1986) found that normals making saccadic eye movements in the dark produced results similar [i.e., overshoots of target position, larger second saccadic movements, and a greater proportion of "double saccades'; see Levin et al (1982) for a more precise characterization ef ~accadic eye movements in schizophrenia] to those observed in schizophrenics making saccadic eye movements to targets they could see (Mather and Putchat 1983). She saw this as support for the contention that schizophrenics are inefficient in processing visual information, and that they have "difficulty with judgments about where eye movements should go." Kaufman and Abel (1986) looked at eye movements of normal subjects viewing a target against a distracting background, which constituted, according to them, a more accurate (than usual) simulation of real life. They found that with a distracting background, pursuit gain was reduced ~nd the number of "anticipatory saccades" increased. Lipton et al (1980), in their critique of Brezinova and Kendell (1977), wrote (p. 166): "The logic of the Brezinova and Kendell (1977) s t u d y . . , appears faulty: the demonstration that normals, when distracted, produce tracking patterns indistinguishable from schizophrenics' would not constitute evidence that distraction produced the deficit in schizophrenics, for eye tracking may be impaired by a variety of causes and the imposition of distracting stimuli may be one cause, but not the only one." This, of course, is a general criticism, not limited only to induced smooth pursuit dysfunction via distraction. The claim that it is very unlikely that a single experiment in which norma~s are stressed to the point that they exhibit smooth pursuit dysfunction will reveal the true nature of those dysfunctions in schizophrenics, is undoubtedly true. However, experiments concerning target nature and other experimentally variable conditions may contribute specifically to our understanding of various aspects of the smooth p~:,rsuit marker. This study demonstrates that both normal subjects and schizophrenics show a decrease in smooth pursuit performance (as measured by %RMS error and single-mode tracking gain) when following an unpredictable rather than predictable target. Indeed, by using a global measure of pursuit performance (%RMS error), the suggestion (bas,~d on results from only five subjects) by Levin et al (1988) that unpredictable rather than predictable targets are more useful for discrimin~ating between normals and schizophrenics is generally supported. In their discussion, Levin et al point out that their schizophrenic subjects showed less anticipation than did normal subjects, and suggest that this may be further evidence of frontal lobe impairmenlt in schizophrenics (Levin 1984). Despite the group differences between normais and schizophrenics in tracking the unpredictable target, our results indicate that schizophrenics are indeed capable of tracking a continuous unpredictable target, and that they show a comparable decrease in individual performance relative to that seen in normals. This is not to say that they track such targets as well as normals, but the fact that they can do it at all has potential implications for understanding the eye movement deficit in schizophrenics. Although it is so easy to demonstr:te that at some level schizophrenics "have difficulty with judgments about where eye movements should go" (Mather 1986), i: can be rather difficult to determine at what (visual or information processing) level things actually begin to go wrong. As mentioned above, Kowler et al (1984) have argued that in tracking a moving target, a subject not only "learns," in a broad sense, the motion of the target if it is predictable, but :~.lsogenerates expectations based on immediate prior target motion if the t~rget is unpredictable. In order to track an unpredictable target with any semblance of accuracy, the subject must be able to very quickly ascertain tl~e nature of target motion during the ~rief periods when velocity and direction are constant. Schizophrenics are c~.pable of tracki~Jg an unpredictable target. This indicates that processual mechanisms
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necessary for making predictions concerning gross target motion are intact (although they may be impaired), thus indicating that at one level, schizophrenics do not have difficulty making iudgments about where eye movements should go. Bahill et ai (1980) found less variability among individuals tracking an unpredictable rather than predictable target; d~ey labeled this finding "paradoxical." As seen in the CVs for %RMS error in Table 5, a similar result was found in this study for both normals and schizophrenics. Bahill et al (p. 930) explained the loss of variability in the following manner: "The use of an internal model, or predictive capability, may be the cause of this variability. The internal model is a high order process that is not stereotyped in all i n d i v i d u a l s . . , if the target movements are unpredictable, then the subject cannot use the internal model and a possible source of variability is removed." The data concerning schizophrenics presented in this article are consistent with a loss of the internal model due to the nature of the target, not with an absence of the model that would signify a constitutional difference between schizophrenics and normals. However, the qualitative observation that schizophrenics tracking the unpredictable target tended to make fewer look-ahead saccades than normals may indicate a difference in the formulation of the predictive model, and supports the suggestion of Levin et al (1988) that schizophrenics are less anticipatory in their tracking than are normals. In a series of experiments, Braff and his colleagues (Braff 1981; Braff and Saccuzzo 1985; Mitler et al 1979) have used a backward masking task to demonstrate that schizophrenics have an information-processing dysfunction at interstimulus intervals greater than 60 msec and less than 500 msec. graft and Saccuzzo (1985, p. 173) pointed out that smooth pursuit dysfunction in schizophrenics is "interpretable in terms of impaired information proce~;sing in the several hundred milliseconds following stimulus registration. Holzman's work indicates that the smooth, serial processing .ff visual information seems to be disrupted with schizophrenic individuals." Although the results presented in this article do not bear directly on this issue, they do indicate that schizophrenics are capable of generating an internal model (or of learning a gross, repetitive pattern) for predicting the future path of predictable target movements and that they are also capable of very quickly making estimations of future target motion based on immediate prior target motion while they are trackiing an unpredictable target. Thus eye tracking dysfunction in schizophrenia may be due to postregistration (as evidenced in the backward masking studies) rather than preregist~,aon infcnnati:m processing deficits. Of course, in the tracking of a continuous target, postregistration information processing deficits may cause some interference in the ability to anticipate future target motion. .I.S. Allen was supported by a graduate fellowship from the National Science Foundation and by the Scottish Rite Schizophrenia Research Program, N.M .I., U.S.A.S. S Hacisalihzade was partially supported by Swiss National Science Foundatiori grant 5.521.330.615/7. We thank Margaret Wong and Tom Schoenemann for help with data analysis.
Reference Allen JS, Matsunaga K, Nakamura T, et al (1990): Schizophrenia, eye movements, and biocultural heterogeneity. Hum Biol (in press). Bahill AT, McDonald JD (1983): Smooth pursuit eye movements in response to predictable t~get motions. Vision Res 23:1573-1583. Bahill AT, landolo MJ, Troost BT (1980): Smooth pursuit eye movements in response to unpredictable target waveforms. Vision Res 20:923-931.
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Braff DL (1981): Impaired speed of information processing in nonmedicated schizotypal patients. Schizophr Bull 7:499-508. Braff D, Saccuzzo DP (1985): The time course of information-processing deficits in schizophrenia. Am J Psychiatry 142:170-174. Brezinova V, Kendell RE (1977): Smooth pursuit eye movements of schizophrenics and normal ~ople under stress. Br J Psychiatry 130:59-63. Hoizman PS (1987): Recent studies of psychophysiology in schizophrenia. Schizophr Bull 13:4976. Holzman PS, Levy DL, Proctor LR (1976): Smooth pursuit eye movements, attention, and schizophrenia. Arch Gen Psychiatry 33:1415-1420. Kaufman SR, Abel LA (1986): The effects of distraction on smooth pursuit in normal subjects. Acta Otolaryngol (Stockh) 102:57-64. Kowler E, Martins AJ, Pavel M (1984): The effect of expectations on slow oculomotor control. IV. Anticipatory smooth eye movements depend on prior target motions. Vision Res 24:197210. Levin S (1984): Frontal lobe dysfunctions in schizophrenia. I. Eye movement impairments. J Psychiatry Res 18:27-55. Levin S, Jones A, Stark L, Men'in EL, Holzman PS (1982): Saccadic eye trovements of schizophrenic patients measured by reflected light technique. Biol Psychiatry 17:1277-1287. Levin S, Luebke A, Zee DS, Hain TC, Robinson DA, Holzman PS (1988): Smooth pursuit eye movements in schizophrenics: Quantitative measurements with the search-coil technique. J Psychiatry Res 22:195-206. Lipton RB, Frost LA, Holzm~ri nS (1980): Smooth pursuit eye movements, schizophrenia, and distraction. P erceFt 3rotor Skills 50:159-167. Mather J (1986): Saccadic eye movements to seen and unseen targets: Oculomotor errors in normal subjects resembling those of schizophrenics. J Psychiatr Res 20:1-8. Mather JA, Putchat C (1983): Motor control of schizophrenics. I. Oculomotor control of schizophrenics: A deficit in sensory processing, not strictly in motor control. J Psychiatry Res 17:343360. Meyer CH, Lasker AG, Robinson DA (1985): The upper limit of hum,~a smooth pursuit velocity. V~sl.r,n ICes 25:561-563. Michael JA, Jones GM (1966): Dependence of visual tiacking capability upon stimulus prediictability. Vision Res 6:707-716. Miller S, Saccuzzo D, Braff D (1979): Information processing deficits in remitted schmophrenics. J Abnorm Psychol 88:446-449. Norris H (1968): The time course of barbiturate action in man investigated by measurement of smoeth tracking eye movement. Br J Pharmacol Chemother 33:117-128. Oppenheim AV, Wilsby AS, Young IT (1983): Signals and Systems. Englewood Cliffs, NJ: P~entice Hall. Shagass C, Roemer RA, A~adeo M (1976): Eye-~a¢ldng performance and engagemeW, of attention. Arch Gen Psychiatry 33:i21-125. Sharpe JA, Sylvester TO (1978): Effect of aging on horiz¢ntal smooth purs:~it. Invest Ophthalmol Visual Sci 17:465-468. Stark L (1971). The control systew, for versional eye movements. In Bach-y-Rita P, Collins CC (eds), The Control of Eye Movements. New York: Academic, pp 363-428. Stark L (1983): Abnormal pattens of normal eye movements in schizophrenia. Schizophr Bull 9:55-72. Stark L, Vossius G, Young LR (1962): Predictive control of eye tracking mg'~,ements. IRE Trans Prof Group Hum Fac Electron 3:52-57. Yee RD, Beloh RW, Marder SR, Levy DL, Sekaia SM, Honrubia V (1987): Eye movements in schizophrenia, lm,est Ophthalmol Visual Sci 28:366-374.
705
Smooth Pursuit Eye Movements of Normal and Schizophrenic Subjects Tracking an Unpredictable Target John S. Allen, Katsuya Matsunaga, Selim Hacisalihzade, and Lawrence Stark
An experimental paradigm employed by several workers in the field of schizophrenic eye movements has involved finding sequences of stimuli that induce saccadic smooth pursuit in the eye movements of normal individuals. It is hoped that the identification of such stimuli will lead to clues concerning the etiology or nature of eye tracking dysfunction in schizophrenia. In this study, the pursuit eye movements of normal and schizophrenic subjects tracking an unpredictable target (composed of summed sine waves) were examined. Eye tracking performance was evaluated both qualitatively and quantitatively using percent root-mean-square (%RMS) error and pursuit gain scores. Schizophrenics are capable of tracking an unpredictable target. Th;,s finding has implications for our understanding of schizophrenic information processing during visual tracking.
Introduction An experimental paradigm employed by several workers in the field of schizophrenic eye movements has involved finding sequences of stimuli that induce saccadic smooth pursuit in the eye movements of normal individuals (Brezinova and Kendell 1977; Lipton et al 1980; Mather and Puchat 1983; Mather 1986; Kaufman and Abel 1986). It is hoped that the identification of such stimuli will lead to clues concerning the etiology or nature of eye tracking dysfunction in schizophrenia. One way to induce low gain smooth pursuit and to increase the number of saccades in a normally tracking irldividual is to use an unpredictable target (Stark et al 1962; Michael and Jones 1966; Bahill, et al 1980). The smooth pursuit system employs "adaptive predictor that allows the system to overcome its innate delays upon exposure to a regular input pattern." (Stark et al 1962, p. 52). According to the Billheimer-Stark model (Stark 1971), learning a predictable targe~'s path involves a three-stage process: (1) a nonpredictive stage, during which the target is first encountered; (2) a transient
From the Department of Anthropology, University of California at Berkeley, Berkeley, California (J.S.A.), the Depadment of Psychology, Faculty of Literature, Kyushu Universiq', Fukuoka, Japan (K.M.), the Department of Control Engineering, ETH, Zurich, Switzerland (S.H.), and the Telembotics and Neurology Unit, University of California at Berkeley, Berkeley, California (S.H.; L.S.) Address reprint requests to D,'. John S. Allen, Pathology Research (i51B), Palo Alto VA Medical Center, Palo Alto, CA 94304. Received November 7, 1989; re~sed March 31, 1990. © 1990 Society of Biological Psychiatry
0006-3223/90/$03.50
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stage, during which learning takes place; and (3) a final steady stage, wherein the target motion is being tracked in a predictive fashion. The progress of the subject through these three stages can be followed and quantified using a five-state, partitioned Markov matrix. Bahill and McDonald (1983) found that humans can learn and accurately track any predictable waveform that is smooth and periodic. With an unpredictable target, the clues by which a tracking subject learns to make accurate predictions are by definition absent. Stark et al (1962) noted that the decrease in phase lag seen in subjects tracking a predictab!e rather than an unpredictable target was evidence for the existence of an "adaptive predictor." Although learning undoubtedly plays a role in the accurate anticipation of future target motion of a predictable target, for an unpredictable target, previous target motion is used without conscious thought or effort by subjects to generate expectations concerning the future motion of the target. Kowler et al (1984) found that through the use of a different finite-state Markov model, they could characterize the anticipatory eye movements of a subject who is track:~ng an unpredictable target. Thus it appears that there are two levels of prediction generation: during the tracking of a predictable target, the overall, periodic pattern of the target is learned, and accurate predictions of future target motion are made based on the learned pattern; for an unpredictable target, predictions (which will ultimately be inaccurate), or amicipations, are made based on immediate prior target motion, since there is no general pattern to learn. In this article, the eye movements of normal and schizophrenic subjects tracking an unpredictable target composed of six randomly summed sine waves will be described. The smooth movement of the unpredictable target used in this enperiment (see Figures 1 and 2 for examples of the target and typical subject responses) might be termed "continuous," as opposed to the unpredictable step-ramp target used by Levin et al (1988). Implications of these results for the more general problem of smooth pursuit dysfunction in schizophre, ia, with special reference to the issue of deficits in preregistration and/or postregistration information processing (Braff 1981; Braff and Saccuzzo 1985; Miller et al 1979), are examined in the discussion section.
Materials and M e t h o d s
Subjects Subjects consisted of 14 normal individuals [9 men, 5 women, mean age (_+ SD) 26.1 _ 7.3 years, range 20-47 years] and 16 chronic schizophrenics (11 men, 5 women, 36.9 -+ 6.1 years, range 29-46 years). Schizophr¢iii¢ :~.~bjects were recruited and examined at Motobu Kinen Psychiatric Hospital in Okinawa Prefecture, Japan. The diagnosis of schizophrenia was made by the hospital's clinical psychiatric staff and was based on Schneiderian criteria. Primary symptoms included auditory hallucinations (10 subjects), paranoid delusions (7 subjects), and hebephrenia (4 subjects). Normal subjects were recruited from the hospital staff and among the student population of Kyushu University, Fukuoka, Japan; they were screened for personal and familial histories of mental illness. Although the schizophrenic subjects in this experiment were older than the normal subjects, and the smooth pursuit system has been described as an "age-dependent motor system" (Sharpe and Sylvester 1978), no previous study has demonstrated a significant age-dependent decrease in smooth pui'suit ability in subjects below the age of 50 years. The oldest psychiatric subject in this study was only 46 years old, and thus age was
Eye Movements of Normal and Schizophrenic Subjects
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unlikely to have been an important contributor to observed differences in smooth pursuit performance between the two subject populations. All schizophrenic subjects were receiving standard (phenothiazines and/or haloperidol) antipsychotic medication. It has been demonstrated in numerous studies that these drugs do not affect smooth pursuit eye movements. In addition, patients received a small dose (30-40 mg) of phenobarbital with their bedtime medication. At least 12 hr passed between the administration of the bedtime medication and the examination of eye movements. Given the time course of the effects of barbiturates on smooth pursuit eye movements (Norris 1968), it is unlikely that these drugs had a significant effect on the sclofizophrenics' eye movements. In a larger study (Allen et al 1990) done in conjunction with the present experiment, a comparison between barbiturate-free schizophrenics and those who had received a small dose of the drug with their bedtime medication showed no significant differences in smooth pursuit performance between the two groups.
Experimental Task vnd Data Acquisition Subjects were required to track with their eyes a sinusoidal target moving across +_ 15 degrees of the visual field. The target, a white cursor (approximately 2 para across) of light against a dark background, was displayed using an oscilloscope driven by a wave generator. Four target frequencies were used: 0.2, 0.4, 0.6, and 0.8 Hz, plus th~ unpredictable target. These frequencies correspond to average velocities of 12, 24, 36, and 48 degrees/sec, respectively. The random target was generated by randomly summing six sine curves (0.2, 0.4, 0.6, 0.8, 1.0, and 1.2 Hz) on a computer, followed by digitalto-analog conversion of this file to tape. The tape was then input to the oscilloscope, where it would drive the cursor ir~ an unpredictable (to the subject) fashion. The target was actually pseudo-random, and it had a periodicity of about l0 sec. Subjects tracked for at least 30 sec at each target frequency. Subject performance was continuously monitored and verbal prompts (e.g., urging the subject not to blink and to attend to the tracking task) were made as nccessary. Frequent calibration trials were made using a slow (0.2Hz) square-wave target. Aftqr tracking the four predictable sinusoidal targets, the subject tracked the unpredictable target for approximately 30 sec. Eye movements were measured monocularly (left eye) using the high-resolution photoelectric method (infrared reflectometry) to directly record eye position (Stark et al 1962). Photocells were mounted on lensless eyeglass frames, and a chin rest was used to restrain head movement. Target and eye position signals were recorded simultaneously on a multitrack cassette data recorder. Chart recordings of the data were examined, and those portions of the eye movement signal without artifacts (blinks, etc.), along with the corresponding target signal, were digitized over 12 bits at 60 Hz and stored on disk for processing and quantitative analysis.
Data Analysis After linear transformation of the eye signal based on calibration results, the root-meansquare (RMS) error between target and eye position was determined. For the predictable targets, the RMS error was determined by overlapping 10-sec periods at l-sec intervals over the entire subject run (up to 30 sec) at each target frequency. The 10-sec period with the lowest position RMS score was saved on disk. For the unpredictable target, RMS position error scores were calculated over the entire 30-sec trials, rather than
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sampling the ten seconds with the lowest score. RMS scores were normalized by assigning a zero-eye-movement run (eye position fixed at zero degrees) an ewor score of 100%. Calculation of the gain was the same for predictable and unpredictable targets. A Fast Fourier Transform (FFT) was performed on the time functions of the stimulus, s(t), and the subject's response, r(t). This yielded the stimulus, S(w), and response, R(w), in the comr~lex frequency,domain. The gain in decibels at a given frequency, fl, was then defined as G(II) = 20 log
with IR(~)I and IS(fl) I denoting the amplitudes of the complex valued response and stimulus functions at the given frequency II (Oppenheim et al 1983). Before the gain was calculated, saccades were identified using a velocity threshold of 42 degrees/see and removed from the eye movement sig~.al; they were replaced by linear interpolations between the points immediately preceding and following the deleted saccades. At this velocity threshold, some small saccades (< 1 degree in amplitude) could have been missed by the filter, and thus higher velocity epochs may have been included :,n the calculation of gain. The eye movement signal was then smoothed, using a three-point moving average. The resulting gain score is perhaps better described as the "single-mode tracking gain" (Bahill et al 1980). Qualitative analyses of the predictable eye movements only were performed by two blind raters examining the complete (up to 30 see) 0.4-Hz chart recordings. A five-point scale (1 = good, 3 borderline, 5 -= poor) was used to score eye tracking performance. A subject's tracking was considered abnormal if it received an average score greater than 3. In the larger study (Allen et al 1990) done in conjunction with the present experiment, the eye movements of 88 schizophrenics and 37 normal subjects were qualitatively scored. Interrater reliability was high (r 2 = 0.81), and in 93.2% of the cases, the two raters gave identical scores or scores within 1 point of each other. The unpredictable eye movements were not qualitatively scored. Results Position plots of two normal subjects tracking the unpredictable stimulus are presented in Figures la and lb. Similar plots for two schizophrenic subjects are presented in Figures 2a and 2b. Note in all cases the saccadic nature of the pursuit. The normal subject in Figure l a demonstrates excellent tracking of the unpredictable target, although he overshoots the target consistently during rapid target direction reversals. The normal subject in Figure lb scored close to the average for %RMS error; her performance is characterized by an abundance of "catchup" and "look-ahead" (perhaps anticipatory) saccades. The eye movements of the schizophrenic subjects in Figures 2a and 2b are characterized by an abundance of catchup saccades and a relative lack of look-ahead saccades. Qualitative scoring on the basis of the 0.4-Hz chart record showed that 2 of i4 (14%) of the normal subjects and 14 of 16 (88%) of the schizophrenic subjects had abnormal smooth pursuit for a predictable target. The results of the %RMS score analysis are presented in Table 1. Schizophrenics scored significantly worse than normal (Mann-Whitney test, p < 0.01) at all target frequencies and for the unpredictable target. Note that the ratio of the schizophrenic to the normal score (Sc/N) decreased for the unpredictable target relative to the predictable
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Table 1. Mean (Standard Deviation) of %RMS Position Error Scores for Normal and Schizophrenic Subjects" %RMS position error
0.2 Hz Normal Schizophrenic Sc/N
14.4 (6.3) 26.9 (13.2) 1.9
0.4 Hz 14.3 (5.0) 26.7 (14.0) ! .9
0.6 Hz 21.0 (5.4) 38.7 (14.9) 1.8
0.8 Hz 27.4 (7.2) 51.8 (13.4) :..9
Unpredictable 39.8 (7.2) 66.2 (15.1) 1.7
°For all measures, at all predictable frequencies and for the unpredictabletarget, schizophrenics ~ored considerablyworse than normals (nonparametric Mann-Whitney Test, p < 0.01).
target scores. Although this statistic may not be a "real" value, when combined with an examination of the plots it is quite apparent that schizophrenics are capable of tracking the unpredictable target, and that the decrease in their performance is comparable to the decrease in the performance of normals. In Table 2, percentile equivalents of %RMS score for both nocmals and schizophrenics tracking the predictable target at 0.4 Hz and the unpredictable target are shown. Note that there is no overlap between normals and schiz,~phrenics for %RMS score during tracking of the unpredictable target. This confirms the results of Levin et al (1988), who showed no overlap in tracking performance (measured by steady-state gain) between normals and schizophrenics during tracking of an unpredictable step-ramp stimulus. The results of the single-mode tracking gain analysis are presented in Table 3 and Figure 3. Confirming the findings of Yee et al (1987), for the predictable target frequencies, normals showed higher gain pur~uit than did schizophrenics (Mann-Whimey test, 0.01 < p < 0.09); this was also true for the unpredictable target, although less significantly so (0.09 < p < 0.20). For both normal and schizophrenic subjects, gain scores for the unpredictable target were significantly lower than the corresponding frequency score for the predictable target (p ~< 0.01); the exception was at 0.8 Hz, where gain scores for predictable and unpredictable targets were not significantly different for either normals or schizophrenics. This is not surprising, given that while tracking a 0.8Hz predictable target, the eye movements of many normal subjects are saccadic, and single-mode pursuit gain obviously decreases. The average target velocity at 0.8 Hz is 48 degrees/see; peak velocities range up to about 70 degrees/see, a value that approaches the upper limit of pursuit velocity [about 100 degrees/sec, according to Meyer et al (1985)]; t:nder normal circumstances, the pursuit system does not try to follow a target moving faster than 30 degrees/see (Stari;, i983). Another explanation for the lack of a significant difference at 0.8 Hz may be that there was too little power in the input spectrum at that frequency. In Table 4, percentile equivalents for normals and schizophrenics for pursuit gain at 0.4 Hz for the predictable and unpredictable targets are preseW~'d. Unlike Levin et al (1988), we found that gain discriminates the two populations les., well than other quantitative measures of performance. One reason for this may be that the "gain(s)" being measured in the two experiments are sotnewhat different entities. In Levin et al (1988) the "gain" was a steady-state r,,ain calculated by taking the ,'atio of the eye and tat-get velocities while the eye passed through the primary position during tracking of the stimulus. The "gain" in this experiment was a single-mode pursuit gain calculated in the frequency domain by taking the FFT over the entire eyt: movement signal. By making
714
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Table 2. Percentile Equivalents for %RMS Error Scores for Normal and Schizophrenic Subjects Tracking the Predictable Target at 0.4 Hz and the Unpredictable Target
%RMS error
Percentiles at 0.4 Hz predictable N
Sc
Percentiles for the unpredictable target N
100 98 96 94 92 90 76 74 72 70 68 66 64 62 60 58 56 54 52 50 48 46 44 42 40 38 36 34 32 30 28 26 24 22 20 18 16 14 12 10 8 6 0
Sc
100 93.8
100
81.3 75.0
62.5 56.3 50.0 37.5 25.0 18.0 0 100 85.7 71.4 50.0
100 92.3 85.7 78.6 64.3 50.0 28.6 14.3 0
93.8
35.7
87.5 8i.3 75.0 62.5 50.0 43.8 37.5 25 18.8
28.6 15.3 7.1 0
6.3 0
Eye M o v e m e n t s o f N o r m a l and S c h i z o p h r e n i c Subjects
BIOL PSYCHIATRY 1990;28:705-720
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Table 3. M e a n G a i n S c o r e s ( S t a n d a r d Deviation) for N o r m a l a n d S c h i z o p h r e n i c Subjects T r a c k i n g Predictable a n d U n p r e d i c t a b l e Targets" Predictable gains
Normal Schizophrenic Sc/N
0.2 Hz
0.4 Hz
0.6 Hz
0.8 Hz
- 0 . 2 (0.6) - 1.1 (1.2) 5.5
- 0 . 5 (0.6) - 1 . 0 (1.1) 2.0
- 1 . 9 (0.8) - 3 . 2 (1.8) 1.7
- 4 . 9 (1.4) - 6 . 7 (3.0) 1.4
p = 0.04
p = 0.09
p = 0.01
p = 0.04
Unpredictable gains
Normal SchizophrenicSc/N
0.2 Hz
0.4 Hz
0.6 Hz
0.8 Hz
- 2 . 7 (2.5) - 3.9 (4.1) !.4
- 1 . 8 (1.4) - 2.6 (2.6) 1.4
- 4 . 8 (1.3) - 5.1 (2.3) 1.1
- 4 . 1 (1.8) - 5.4 (2.7) 1.3
p = 0.09
p = 0.09
p = 0.20
p = 0.15
°For both normal and schizophrenic subjects, gains scores for the unpredictable target were significantly lower than the corresponding frequency score for the predictable target (Mann-Whitney test, p ~<0.01); the exception was at 0.8 Hz, where gains for predictable and unpredictable targets were not significantly different for either normals or schizophrenics. The statistical significances (derived from Mann-Whitney tests) for population diffc~nencesbetween normals and schizophrenics are listed below the appropriate columns.
use of the entire signal, the reduction in gain seen in schizophrenics relative to norraals may have been dampened due to the effects of incorporating periods of target reversal in the calculation of gain. Because the unpredictable target reversed directions more frequently than the predictable target, the dampening or averaging effect would be increased. In addition, the velocity filter used to eliminate saccades before the calculation
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Frequency (Hz) Figure 3. F r e q u e n c y versus m e a n gain for n o r m a l s a n d s c h i z o p h l e n i c s tracking the predictable and u n p r e d i c t a b l e targets. See text for discussion.
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Table 4. Percentile Equivalents for Pursuit Cain at 0.4 Hz for Normal and Schizophrenic Subjects Tracking the Predictable and Unpredictable Targets
Gain (dB)
Percentiles at 0.4 Hz (predictable) N
Sc
Perce-~,tiles at 0.4 Hz (unpredictable) N
100
2.6 2.0 1.4 1.2 i.0 0.8 0.6 0.4 0.2 0.0 -0.2 -0.4 -0.6 -0.8
93.8
100 100 93.8 100 92.9 736 64.3 57.1 ,~2.3
- !.0 - 1.2
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Sc
88.0
87.5 75.0 62.5 56.3 50.0 43.8 37.5
7.1 0
92.9 85.7
78.6
81.3
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6.3 0
57.1 42.9 35.7 28.6 14.3 7.1 0
75.0 68.8 62.5
31.3
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18.8
-5.6
12.5
-7.8 -8.0
6.3 0
of pursuit gain may have missed some very small saccades, and thus the presence of hlgher-velocity movements in the eye signal would result in higher pursuit gain scores. k~ain score ratios for each frequency were lower for the unpredictable than for the predic able target; again, it is apparen" that the unpredictable target leads to a decline in tracking t}erformance that is similar for both the normal and schizophrenic subjects. Figure 3 shows the typical reduction h~ gain with increasing target frequency seen in individuals tracking a predictable target (Bahill et al 1980; Stark et al 1962); it also illustrates that
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Table 5. Coefficients of Variation [CV = ± 100 x (SD/mean)] for %RMS Position Error Scores (Note That Unpredictable CVs Are Smaller Than Predictable CVs for Both Normal and Schizophrenic Subjects) CV for %RMS Position Error Score
0.2 Frequency (Hz) Normal Schizophrenic
44 49
0.4 0.6 (Predictable target) 35 52
26 38
0.8
Unpredictable target
26 26
18 23
low-gain pursuit distinguishes the eye movements of schizcphrenics from normals, albeit ~ess strongly than do measures that incorporate the effects of saccadic intrusions and saccadic smooth pursuit (Yee et al 1987). In Table 5, coefficients of variation [CV = +__ 100 x (SD/mean)] are given for %RMS position scores. The CVs for the unpredictable target are smaller for both populations and at all frequencies. Bahill et al (1980) noted that intersubjeet variability decreased when going from a predictable to unpredictable target. These CV data confirm this, and also show that the schizophrenic response is similar to that seeil in the control population.
Discussion In a broad sense, this examination of eye movements of schizophrenics while tracking an unpredictable target belongs to the general body of work done on attention and schizophrenic eye movements. The earliest studies in this area (Shagass et al 1976, followed by Holzman et al 1976; see Holzman 1987 for a more recent discussion) attempted to study the "engagement of attention," and target characteristics were varied (e.g., requiring subjects to read a number superimposed on a smooth pursuit targe0 in an ~ttempt to enhance attention and smooth oursuit performance. In general, it was concluded that schizophrenics do not track poorly because of voluntary inattention, but because of a "failure of cognitive centering, in spite of a desire to do the task" (Holzman et al 1976). Another possible way to learn something about the effects of attention on schizophrenic eye movements is to identify circumstances in which the performance of a normal individual can be made to resemble that of a schizophrenic. For example, Brezinova and Kendell (1977) found that normals distracted by a serial subtraction task or whose attention was impaired by prolonged eye tracking produced eye tracking abnormalities that they could not distinguish (using a five-point qualitative scale) from those found ir schizophrenics. They suggested that (p. 63) "the deviant eye tracking observed in mm~y schizophrenics is simply a reflection of their decreased ability to focus and attend in a consistent manner, and so of no greater aetiological significance than their other psychomotor deficits." This work prompted a response by Lipton et al (1980), who in replicating Brezinova and Kende!l's experiment, found that they could easily, using both quantitative (the velocity arrest score) and qualitative (blind raters could classify the eye movements of normal, normal-distracted, and schizophrenic subjects into their respective categories) methods, distinguish t~,~ eye movements of distracted no~'mals from those of ~;chizo-
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pba-enics. Mather (1986) found that normals making saccadic eye movements in the dark produced results similar [i.e., overshoots of target position, larger second saccadic movements, and a greater proportion of "double saccades'; see Levin et al (1982) for a more precise characterization ef ~accadic eye movements in schizophrenia] to those observed in schizophrenics making saccadic eye movements to targets they could see (Mather and Putchat 1983). She saw this as support for the contention that schizophrenics are inefficient in processing visual information, and that they have "difficulty with judgments about where eye movements should go." Kaufman and Abel (1986) looked at eye movements of normal subjects viewing a target against a distracting background, which constituted, according to them, a more accurate (than usual) simulation of real life. They found that with a distracting background, pursuit gain was reduced ~nd the number of "anticipatory saccades" increased. Lipton et al (1980), in their critique of Brezinova and Kendell (1977), wrote (p. 166): "The logic of the Brezinova and Kendell (1977) s t u d y . . , appears faulty: the demonstration that normals, when distracted, produce tracking patterns indistinguishable from schizophrenics' would not constitute evidence that distraction produced the deficit in schizophrenics, for eye tracking may be impaired by a variety of causes and the imposition of distracting stimuli may be one cause, but not the only one." This, of course, is a general criticism, not limited only to induced smooth pursuit dysfunction via distraction. The claim that it is very unlikely that a single experiment in which norma~s are stressed to the point that they exhibit smooth pursuit dysfunction will reveal the true nature of those dysfunctions in schizophrenics, is undoubtedly true. However, experiments concerning target nature and other experimentally variable conditions may contribute specifically to our understanding of various aspects of the smooth p~:,rsuit marker. This study demonstrates that both normal subjects and schizophrenics show a decrease in smooth pursuit performance (as measured by %RMS error and single-mode tracking gain) when following an unpredictable rather than predictable target. Indeed, by using a global measure of pursuit performance (%RMS error), the suggestion (bas,~d on results from only five subjects) by Levin et al (1988) that unpredictable rather than predictable targets are more useful for discrimin~ating between normals and schizophrenics is generally supported. In their discussion, Levin et al point out that their schizophrenic subjects showed less anticipation than did normal subjects, and suggest that this may be further evidence of frontal lobe impairmenlt in schizophrenics (Levin 1984). Despite the group differences between normais and schizophrenics in tracking the unpredictable target, our results indicate that schizophrenics are indeed capable of tracking a continuous unpredictable target, and that they show a comparable decrease in individual performance relative to that seen in normals. This is not to say that they track such targets as well as normals, but the fact that they can do it at all has potential implications for understanding the eye movement deficit in schizophrenics. Although it is so easy to demonstr:te that at some level schizophrenics "have difficulty with judgments about where eye movements should go" (Mather 1986), i: can be rather difficult to determine at what (visual or information processing) level things actually begin to go wrong. As mentioned above, Kowler et al (1984) have argued that in tracking a moving target, a subject not only "learns," in a broad sense, the motion of the target if it is predictable, but :~.lsogenerates expectations based on immediate prior target motion if the t~rget is unpredictable. In order to track an unpredictable target with any semblance of accuracy, the subject must be able to very quickly ascertain tl~e nature of target motion during the ~rief periods when velocity and direction are constant. Schizophrenics are c~.pable of tracki~Jg an unpredictable target. This indicates that processual mechanisms
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necessary for making predictions concerning gross target motion are intact (although they may be impaired), thus indicating that at one level, schizophrenics do not have difficulty making iudgments about where eye movements should go. Bahill et ai (1980) found less variability among individuals tracking an unpredictable rather than predictable target; d~ey labeled this finding "paradoxical." As seen in the CVs for %RMS error in Table 5, a similar result was found in this study for both normals and schizophrenics. Bahill et al (p. 930) explained the loss of variability in the following manner: "The use of an internal model, or predictive capability, may be the cause of this variability. The internal model is a high order process that is not stereotyped in all i n d i v i d u a l s . . , if the target movements are unpredictable, then the subject cannot use the internal model and a possible source of variability is removed." The data concerning schizophrenics presented in this article are consistent with a loss of the internal model due to the nature of the target, not with an absence of the model that would signify a constitutional difference between schizophrenics and normals. However, the qualitative observation that schizophrenics tracking the unpredictable target tended to make fewer look-ahead saccades than normals may indicate a difference in the formulation of the predictive model, and supports the suggestion of Levin et al (1988) that schizophrenics are less anticipatory in their tracking than are normals. In a series of experiments, Braff and his colleagues (Braff 1981; Braff and Saccuzzo 1985; Mitler et al 1979) have used a backward masking task to demonstrate that schizophrenics have an information-processing dysfunction at interstimulus intervals greater than 60 msec and less than 500 msec. graft and Saccuzzo (1985, p. 173) pointed out that smooth pursuit dysfunction in schizophrenics is "interpretable in terms of impaired information proce~;sing in the several hundred milliseconds following stimulus registration. Holzman's work indicates that the smooth, serial processing .ff visual information seems to be disrupted with schizophrenic individuals." Although the results presented in this article do not bear directly on this issue, they do indicate that schizophrenics are capable of generating an internal model (or of learning a gross, repetitive pattern) for predicting the future path of predictable target movements and that they are also capable of very quickly making estimations of future target motion based on immediate prior target motion while they are trackiing an unpredictable target. Thus eye tracking dysfunction in schizophrenia may be due to postregistration (as evidenced in the backward masking studies) rather than preregist~,aon infcnnati:m processing deficits. Of course, in the tracking of a continuous target, postregistration information processing deficits may cause some interference in the ability to anticipate future target motion. .I.S. Allen was supported by a graduate fellowship from the National Science Foundation and by the Scottish Rite Schizophrenia Research Program, N.M .I., U.S.A.S. S Hacisalihzade was partially supported by Swiss National Science Foundatiori grant 5.521.330.615/7. We thank Margaret Wong and Tom Schoenemann for help with data analysis.
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