Changes in eye tracking during clinical stabilization in Schizophrenia

P.s,vchiurr_v

31

Rwurc~h, 28, 3 I-39

Elsevier

Changes in Eye Tracking Schizophrenia

During

Margaret M. Rea, John A. Sweeney, Allen Frances

Clinical

Carla M. Solomon,

Stabil‘ization

in

Virginia Walsh, and

Received April 18, 1988; revised version received October 3.1988;accepted

December 19.1988.

Abstract. Eye tracking abnormalities have been proposed as a trait marker for schizophrenia on the basis of their familial prevalence and the consistency of tracking over time in clinically stable patients. However, few studies have examined stability through acute episodes of illness, and most studies have not analyzed changes in different forms of eye movements. Therefore, the authors examined eye tracking, clinical state, and neuroleptic dose during 4 consecutive weeks in nine recently hospitalized schizophrenic patients. For the patients and controls, qualitative ratings of pursuit accuracy remained relatively stable over time. In contrast, saccade frequency increased significantly, with a 57% increase in small saccades and a 77% reduction in larger saccades. In comparison with cross-sectional studies which have found no correlation between neuroleptic dose and tracking performance, a reduction in large saccades was strongly correlated with increase in neuroleptic dose. The findings suggest that pursuit accuracy may be a trait characteristic of schizophrenia, while the frequency and size of saccades are state dependent characteristics. Key Words. Schizophrenia,

eye movements,

attention.

There is a high prevalence of eye tracking impairment in schizophrenia. Rates of the abnormality typically range from 55% to 85% in schizophrenic patients as compared to 6% to 10% in the normal population (Holzman et al., 1974; Holzman, 1987). Deviant eye tracking in schizophrenia is of major interest, especially because of its familial prevalence (40% to 50% of first degree relatives) and possible genetic significance (Holzman, 1987). For eye tracking abnormalities to serve as a valid traitlike psychobiological marker for schizophrenia, it is important that they be stable over time (Iacono and Lykken, 1981). However, few studies have directly assessed the stability of this abnormality during acute phases of illness to determine whether changes in clinical state affect performance on eye tracking tasks. There are several reasons for concern that some aspects of eye tracking abnormalities might be state dependent. First, state-related changes in the ability to allocate attention (Silberschatz, 1978) have been described in schizophrenia and could lead to variability in eye tracking performance. Several studies (Holzman et al., 1976; Shagass et al., 1976; Lipton et al., 1980; Cegalis and Sweeney, 1981) have demonstrated that

Margaret M. Rea, Ph.D., is Fellow in Psychology, Department of Psychology, University of California, Los Angeles. John A. Sweeney, Ph.D., is Assistant Professor of Psychiatry; Carla M. Solomon, Ph.D., is Research Associate in Psychiatry; Virginia Walsh, B.S., is Research Assistant; and Allen Frances, M.D., is Professor of Psychiatry, Department of Psychiatry, Payne Whitney Clinic, New York Hospital-Cornell Medical Center, New York, NY. (Reprint requests to Dr. M.M. Rea, Dept. of Psychology. 1283A Franz Hall, UCLA, Los Angeles, CA 90024-1563, USA.) 0165-1781/89/$03.50

Q 1989 Elsevier Scientific

Publishers

Ireland Ltd.

32 involuntary attentional factors are important in determining quality of tracking. Second, neuroleptic treatment might affect tracking performance. Although crosssectional studies have not found correlations between oral neuroleptic dose and global measures of tracking performance (Holzman et al., 1974; Shagass et al., 1974; Cegalis and Sweeney, 1979), acute changes in neuroleptic dose might either impair tracking performance as a result of neuromuscular side effects, or improve tracking by reducing the attentional disturbances associated with acute psychosis. The few previous studies of eye tracking in schizophrenic patients over time have failed to demonstrate changes in tracking performance either as a result of change in clinical state or change in neuroleptic dose. Levy et al. (1983) evaluated eye tracking in eight initially unmedicated schizophrenic patients over a 4-week course of neuroleptic treatment. Holzman et al. (1974) retested 10 chronic patients 10 days after discontinuation of neuroleptic medication. Siever et al. (1986) studied eight schizophrenic patients before and after a 2-week neuroleptic trial. No global changes in overall tracking quality were found in any of the three studies. In a more recent study, Spohn et al. (1988) reported that tracking performance of 100 schizophrenic patients worsened slightly over a IO-week period of biweekly retesting, but no differences were found between medicated and neuroleptic-withdrawn patients, or between relapsed and clinically stable patients. Previous studies might have been subject to Type II error because they failed to systematically assess correlations between clinical state and eye tracking, did not examine the stability of different dimensions of eye tracking performance over time, and some did not include comparison groups. We therefore administered eye tracking tests weekly for 4 weeks to nine acutely ill recently hospitalized schizophrenic patients. We separately analyzed pursuit accuracy and the frequency of saccadic eye movements during the eye tracking task and examined whether the different eye tracking measures were related to changes in clinical state and/or neuroleptic dose. Methods Subjects included nine inpatients meeting DSM-III criteria for schizophrenia (American Psychiatric Association, 1980) who had been hospitalized for acute care within the preceding week.

Diagnoses were based on the Structured Clinical Interview for DSM-III @CID) (Spitzer and Williams, 1985). Six patients were female and three were male. Mean age was 28.3 years (SD q 7.7). Patients with a known history of head trauma, electroconvulsive therapy, neurological disease, significant substance abuse, or facial tardive dyskinesia were excluded. Patients did not receive benzodiazepines, carbamazepine, or lithium carbonate during the study. All patients received neuroleptic and psychosocial treatments that were not under experimental control. The mean 18-item Brief Psychiatric Rating Scale (BPRS) (Overall and Gorham, 1962) score at admission was 51.8 (SD = 9.2) and significantly decreased to 41.3 (SD = 9.23) at week 4 of hospitalization (t = 4.58, df= 8,~ < 0.001). Mean chlorpromazine-equivalent neuroleptic dose was 748 (SD = 790) at admission, and dosages increased significantly to 1,470 (SD = 959) by week 4 of hospitalization (t = 2.43, d’= 8, p < 0.04). To obtain a single index of rate of change in symptom severity (BPRS) and neuroleptic dose (chlorpromazine-equivalent), slopes representing change on these measures were calculated. The average weekly change in BPRS score was -5. I I (SD = 3.72) and in chlorpromazine-equivalent dose was 246 (SD = 290). There wasa fairly wide range in neuroleptic dosing as indicated in the plot of neuroleptic dose for each patient over 4 weeks following admission depicted in Fig. 1.

33 Fig. 1. Neuroleptic dose (chlorpromazine-equivalent) patients during 4 weeks of hbspitalization-

for schizophrenic

2700

0

1

2

3

4

WEEKS AFTER ADMISSION

On admission and for 4 consecutive weeks, the subjects’ eye movements and clinical state (as measured by the BPRS) were assessed. Schizophrenic subjects were compared to eight age- and sex-matched normal control subjects assessed on two occasions, 4 weeks apart. Subjects were asked to track a slowly moving cursor on a Wavetek Model 1903 display oscilloscope with a medium fast decay P4 phosphor. The target, driven by a function generator, moved across the horizontal plane at 0.4 Hz with an excursion of 28 ’ of visual angle. Subjects performed four 50-see trials during which the cursor moved in a sinusoidal pattern across the display screen, Between trials, subjects rested with their eyes closed. A chin rest and forehead restraint were used to minimize head movement. Eye movements were assessed using an electro-oculographic (EOG) technique. Recordings were made with Beckman Ag-AgCL electrodes placed at the external canthus of each eye. Electrodes were also placed above and below the left eye for recording blinks. Signals were recorded on a NarcoBio systems NarcoTrace 40 polygraph with DC-coupled amplifiers. To rate the subject’s optimal tracking capacity, the 30-set segment during the trial with the fewest blinks and best overall tracking performance was selected for quantitative analysis. If at any point during the trial subjects discontinued tracking, they were immediately re-alerted and their performance during this time was not included in the analysis. Only performance during time when the subject maintained a continued focus on the target was included in the analyses of tracking performance. This ensured that any potential changes in tracking accuracy could not be attributed to marked variations in compliance with the task. Tracking accuracy was measured on a S-point qualitative scale based on how closely the subject’s tracking conformed to the target’s uniform sinusoidal pattern. A score of I (worst possible) to 5 (best possible) was assigned. For ratings of a larger sample of 35 schizophrenic patients and 20 normal controls, interrater reliability for pursuit accuracy was high (ICC = 0.86). Saccades were identified visually by selecting eye movements with a velocity > 60 o of visual angle, set (determined by the slope of the position change). Calibration signals for each subject

34 were used to identify the magnitude of changes on the polygraph recording associated with eye movements of various sizes. These calibration values were used to determine the size of each saccade which was recorded in degrees of visual angle. Only saccades > 3 ’ of visual angle were included as smaller saccades are difficult to distinguish from extraneous biopotentials such as electromyographic and electroencephalographic artifacts (Iacono and Koenig, 1983). Test-retest reliabilities of saccades of 3 ‘, 4 ’ and 5’ of visual angle for schizophrenic patients had reliabilities > 0.60, while the saccades of 6’ to 10’ of visual angle each had reliabilities < 0.35. For this reason, when change in saccade frequency over time was examined, smaller (3’ to

5 o of visual angle) and larger (> 5 “) saccades were considered separately. The distribution of the larger saccades was skewed and, therefore, was transformed logarithmically before statistical analyses.

Results Pursuit accuracy of the schizophrenic patients was more deviant than that of the normal controls at the time of admission (t = 2.82, df = 15, p < 0.02) and at week 4 (t= 3.5 1, df= 15,p< 0.01). While schizophrenic patients at admission had 67% more small and 68% more large saccades during pursuit tracking than normals, the differences between the patients and the normal controls were not significant. In contrast, at week 4, schizophrenic patients had significantly more saccades than controls (t = 2.26, df = 15, p < 0.05), but the differences between schizophrenic patients and normal controls were significant for small (t = 2.52, df = 15,~ < 0.03) but not large (t = 0.34, df = 15,~ < 0.74) saccades. The schizophrenic patients demonstrated a 57% increase in small saccades and a 77% decrease in large saccades during the 4-week study period (see Fig. 2), while pursuit accuracy ratings remained stable. An example of tracking perforFig. 2. Frequency of large and small saccades during 30 set of pursuit tracking over a 4-week period (Greater

than 0

0

5 degrees

(3-5

of visual angle)

degrees

of visual angle)

- schizophrenics (n-9)

l - normal controls (n-8) mean +/-

SEM

8

15..

w z

4

1 WeeZk

in .St’ody

E fn

1

*

10

I I

57 1

We’&

3

in Study

4

. (p from

C.05)

controls

mance of one patient that depicts the change over time in saccade size is depicted in Fig. 3. On admission, that patient exhibited a high prevalence of large saccades, while on day 14 the patient had few large saccades, but a greater number of smaller saccades. Test-retest reliabilities for pursuit accuracy and for small and large saccades during pursuit were computed between initial and week 4 testing to determine the stability of performance over time. As Table 1 indicates, the reliability of saccade frequencies during pursuit tended to be lower for the schizophrenic subjects than the normal

35 Fig. 3. Examples of eye tracking performance admission and on day 14 of hospitalization

of a schizophrenic

patient on

PERFORMANCE ON A!JHISSION SHOWNGFREQUENT LNwE SAccADES BPRS SCORE - 62) (CPZ DoSE =o,

PERFORNANCE ON DAY 14 SHOWINGINCREASEDF&Q,!JENCYOF SNALL SACCAD& 6PRS SCORE= 47) (CPZ DOSE- 1400; CPZ = chlorpromazine.

BPRS = Brief Psychiatric

Rating Scale

controls. The reliability for small saccades was significantly lower for the schizophrenic patients. In contrast, pursuit accuracy ratings were relatively stable over time for the schizophrenic patients, though ratings were somewhat less stable for schizophrenic patients than normal controls. When one patient whose tracking accuracy improved dramatically during hospitalization was excluded, the test-retest correlation for pursuit accuracy in the schizophrenic group rose from 0.57 to 0.66. Reliability ratings for saccades during tracking were unchanged or decreased when this subject was excluded. To evaluate variability in tracking performance over time and its relationship to changes in clinical state and neuroleptic dose, the slopes were calculated of each patient’s pursuit accuracy; large, small, and average saccade frequency; clinical state (BPRS score); and neuroleptic dose over time. The slope of large saccades was significantly related to the rate of increase in neuroleptic dose (r = -0.77, df 7, p < q

Table 1. Test-retest reliabilities between initial and 4-week retesting for eye movement measures during 30 set of pursuit tracking in 9 schizophrenic patients and 8 normal controls Normals Schizophrenics Pursuit

accuracy ratings

0.57

0.88

of small saccades (3-5 degrees of visual angle)

-0.051

0.91

Frequency of large saccades (> 5 degrees of visual angle)

-0.36

0.24

Total saccade freouencv

-0.072

0.80

Frequency

1. Significantly 2. Significantly

less than normal controls, less than normal controls,

p c 0.01, P-tailed. p c 0.06. P-tailed.

36 0.0 l), as was the change in the average size of saccades during tracking (r -0.75, df = 7, p < 0.02). Similarly, a significant correlation (r = 0.69, df = 7,p < 0.04) between raw change scores (values at admission minus values at week 4 of hospitalization) in the frequency of large saccades and neuroleptic dose was found. Of note, correlations between neuroleptic dose at week 4 and small saccades (r= -0.29, df = 7,p < 0.45) large saccades (r = -0.09, df = 7, p < 0.8 l), and total saccade frequency (r = -0.27, df 7, p < 0.47) were all nonsignificant, indicating no association between neuroleptic dose and saccade size during periods of greater clinical stabilization. These findings indicate that increases in neuroleptic dose in acutely ill patients were associated with a decline in the size of saccades. The slopes representing changes in other eye movement parameters were not associated with changes in neuroleptic dose, and no eye movement measures were significantly associated with changes in clinical state. q

q

Discussion The two most important findings of this study are the difference in stability over time of tracking accuracy and saccade frequency, and the significant relationship between neuroleptic dose and saccade size. We found that pursuit accuracy of schizophrenic patients remained moderately stable during hospitalization for an acute episode even in the context of improvement in clinical state and increased neuroleptic dose. In contrast, the test-retest reliabilities for saccades during pursuit were consistently lower for schizophrenic patients than for normal controls. During the course of clinical recovery, we observed an increase in small saccades and a decrease in large saccades in the schizophrenic patients. Spohn et al. (1988) also reported the occurrence of large saccades in schizophrenic patients which they interpreted as reflecting a difficulty directing attention to the tracking task. Our interpretation is consistent with this view. It seems most parsimonious to attribute the change in occurrence of saccades of different sizes observed in the present study to normalization of attentional processes. Acute psychosis typically involves marked difficulties in attention and planning, which probably render the schizophrenic patient less able to detect and correct for dynamically changingdisparities between visual focus and target location. A reduced ability to detect and adjust for tracking error may lead to fewer but more gross corrective saccades during periods of acute psychosis, which would account for the increase in saccade size and decrease in saccade frequency observed at the time of hospitalization. With neuroleptic treatment and clinical recovery, there may be improved attention and planning, and in turn a more rapid correction for pursuit error represented by a greater number of saccades that are typically smaller in size. A similar relationship between oculomotor performance and stage of clinical illness has been reported in the literature on Alzheimer’s disease. In patients whoare mildly demented, there appears to be an increase in small corrective saccades, but in more demented patients, there is a reduction in saccade frequency accompanied by greater tracking error and more frequent large corrective saccades (Hutton, 1985). The similarity of the relationship between clinical state and tracking performance in our schizophrenic patients and in Alzheimer’s disease suggests that more severe deficits in mental status are associated with a reduction in small saccades and an increased number of large corrective saccades required to realign gaze on the moving stimulus.

37 It is important to note that the change in saccade frequency and size does not simply reflect problems of volitional inattention or noncompliance. Eye tracking requires a continuous rather than a discrete response so that it is possible to observe that the patient is continually attempting to maintain focus on the target. Any brief periods of discontinued tracking were not included in the analysis of performance. Further, since the smooth pursuit eye movement system is not under volitional control except under unusual laboratory conditions, the patients’ continued pursuit eye movements reflect sustained effort and attention to the task. Our finding of a significant relationship between neuroleptic dose increase and reduction in the frequency of large saccades during pursuit tracking is one of the first demonstrations of a significant relationship between neuroleptic treatment and eye tracking performance in schizophrenia. While Holzman et al. (1975) reported a tendency toward decreased tracking accuracy as represented by more frequent velocity arrests when chlorpromazine was administered to normal subjects, our results suggest that neuroleptics may have a beneficial effect on tracking performance in schizophrenic patients, with the normalization of cognitive processes resulting from neuroleptic treatment causing a reduced need for large coarse corrections for pursuit error. Kornetsky and Orzack (1964) also reported a beneficial effect of neuroleptic treatment on attention in their studies with the continuous performance test. While our findings suggest that neuroleptics may improve attention and eye tracking performance, the relationship between clinical state and tracking performance should not be minimized. Improved attention could in fact be seen as the clinical response to neuroleptic treatment most relevant to tracking performance. Our findings may also clarify a discrepancy in previous studies as to whether schizophrenic patients have increased small or large saccades during tracking. Iacono and Koenig (1983) reported smaller saccades in recovered schizophrenic patients, while Mather and Putchat (1982-83) found larger saccades in hospitalized schizophrenic patients. Since our findings indicate that saccade size during tracking varies with clinical state, the different findings in the Iacono and Koenig and the Mather and Putchat studies could be explained by differences in the clinical state of the patients at the time they were studied. The present study suggests that globally deviant tracking accuracy is a relatively stable traitlike characteristic in schizophrenia which remains relatively stable during acute changes in clinical state and neuroleptic treatment. In contrast, more refined indices of tracking saccade frequency may reveal state-dependent components of tracking performance as it varies over the course of acute episodes. This hypothesis is supported in an interesting way by our previous finding that pursuit accuracy, and not frequency or size of saccades, was associated with trait deficit characteristics in schizophrenia, including ventricle-brain ratio on computed tomography, negative symptoms, cognitive deficits, and poor premorbid adjustment (Sweeney et al., 1987). One model which can explain this pattern of results is that there is a trait deficit in smooth pursuit eye movements in schizophrenia which accounts for impaired pursuit accuracy. This deficit might be in the gain control of smooth pursuit eye movements, an impairment that has been reported by Schmid-Burgk et al. (1982) and Yee et al. (1987). The ability to use saccades to correct efficiently for this deficit might vary with clinical state and treatment.

38 Nuechterlein and Dawson’s (1984) distinction between types of vulnerability indicators for schizophrenia can be applied to the present findings. Pursuit accuracy is close to what they describe as a stable vulnerability indicator for schizophrenia as it is traitlike, consistently deviant from normal levels, and relatively independent from acute symptom changes. In contrast, saccade frequency is more likely a mediating vulnerability factor as it varies with symptomatology, but is deviant from normal levels during symptomatic and asymptomatic episodes. However, somewhat paradoxically, the abnormality of high saccade frequency is most prevalent during periods of recovery rather than during periods of severe acute psychosis. The findings of this study have important implications for future studies of eye tracking impairments in schizophrenia. The results highlight the value of examining components of eye tracking deviance to differentiate parameters of the dysfunction which may be traitlike and specific to schizophrenia, and which might reveal underlying central nervous system origins of the deficit. The ultimate utility of commonly used global quantitative and qualitative ratings of eye tracking abnormality is likely to be limited as they do not include a differentiated analysis of the components of the abnormality. Studies of the sensitivity and specificity of tracking impairments to schizophrenia, and their role as a familial marker in schizophrenia, should include separate analyses of the pursuit and saccadic eye movement systems. Further, the poor test-retest reliability of the saccadic frequency and the somewhat lowered reliability for the tracking accuracy suggests that studies of eye tracking as a trait marker in schizophrenia should not be conducted during the acute phase of the illness when state-dependent disturbances in tracking are most pronounced. Acknowledgments. This project was supported in part bygrantsfrom the National Institutes of Health (BRSG SO7 RR-05396 and USPHS MH-14854) and grants from the Scottish Rite Schizophrenia Research Program, Northern Masonic Jurisdiction, USA, to Dr. Sweeney and Dr. Solomon and by the Stephen Levy Foundation to Dr. Frances.

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