Year : 2000 | Volume
: 48 | Issue : 1 | Page : 15--9
Eye tracking disturbances in Schizophrenia
P Sharma, BS Aslam, S Saxena
Centre for Ophthalmic Sciences, All Institute of Medical Sciences, Ansari Nagar, New Delhi-110 029, India
Centre for Ophthalmic Sciences, All Institute of Medical Sciences, Ansari Nagar, New Delhi-110 029
Purpose: To study the frequency of different types of eye tracking disturbances in schizophrenia.
Materials and Methods: Smooth pursuit eye movements were studied by electro-oculography (EOG) in 22 schizophrenic patients (ICD-10 criteria) and 15 age and sex-matched controls. The studied parameters included average pursuit gain, number of saccades, the frequency of different types of saccades (catch-up, back-up, anticipatory saccades), and disturbances during fixation. The results were analysed statistically.
Results: The average pursuit gain was significantly affected in patients for target velocity of 30°/sec (p=0.007). The catch-up and back-up saccades were more common in cases than controls but the difference was not significant (p=0.39 and 0.36 respectively). The anticipatory saccades were significantly more frequent in cases than controls (p<0.0001) for both 15°/sec and 30°/sec target velocities. This was also correlated with the duration of illness.
Conclusion: Anticipatory saccades are significantly more frequent during eye tracking in schizophrenia and appear to be an objective marker for the disease.
|How to cite this article:|
Sharma P, Aslam B S, Saxena S. Eye tracking disturbances in Schizophrenia.Indian J Ophthalmol 2000;48:15-9
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Sharma P, Aslam B S, Saxena S. Eye tracking disturbances in Schizophrenia. Indian J Ophthalmol [serial online] 2000 [cited 2022 Aug 17 ];48:15-9
Available from: https://www.ijo.in/text.asp?2000/48/1/15/14861
Schizophrenia is a common psychiatric disorder affecting almost 1% of the general population. Its diagnosis and aetiology has puzzled and fascinated psychiatrists and despite consistent study, the condition remains an enigma. Psychophysiological functions have been studied for genetic marking and one of the most objective tests is eye tracking disturbances (ETD) or smooth pursuit eye movement (SPEM) abnormalities.[1-3] The presence of ETD in biological relatives of schizophrenics has been reported several times, as also similarity of ETD in twins of schizophrenia. This has lead to the hypothesis of a latent trait of schizophrenia.[5,6] The different ETDs studied have been: gain of pursuit movements, frequency of catch-up and back-up saccades, anticipatory saccades and square wave jerks, as also log stimulus-noise ratio, and time-off the target per cycle, with different studies giving discordant views. In this study on ETD in schizophrenics compared with age-sex matched controls by electro-oculography, we compared the relative importance of different types of saccades in pursuit movements to highlight the role of intrusive saccades such as anticipatory saccades in schizophrenia.
Materials and Methods
Twenty-two patients with schizophrenia ranging from 21 to 43 years (Mean age = 29.1, ±5.9 years S.D.) were selected based on diagnostic criteria listed in the International Classification of Diseases (ICD-10, WHO, Geneva, 1993). The mean duration of the illness was 6.3 ± 6.2 years. All the patients were on anti-psychotic drugs, the mean chlorpromazine-equivalent dose being 538 ± 357mg. Patients on drugs like barbiturates, lithium and benzodiazepines were excluded. Other exclusion criteria were: presence of tardive dyskinesia, central nervous system disorder, significant eye diseases of motility like strabismus or nystagmus and gross visual impairment, hearing impairment and alcohol and/or tobacco dependence. Sociodemographic information was collected using a questionnaire structured specifically for this study. Detailed clinical work-up included present and past psychiatric symptoms, personal and family history, medical history of premorbid personality, systemic physical examination, and mental state examination. The scales for assessment of negative and positive symptoms were completed for each patient.
Fifteen matched controls of the same age group (Mean age 29.4 ± 5.6 years, range 23-42 years) were selected after excluding past or present history of psychiatric illness, psychiatric illness in first-degree relatives, presence of paranoid or schizoid personality disorder, schizotypal disorder and any significant anxiety problem. Other exclusion criteria were: presence of motility, and visual impairment, hearing impairment and alcohol and / or tobacco dependence. An additional 50% cases were enrolled compared to the controls to check the variance in the study group, as the control group was more harmonious.
Informed consent was obtained from all participants. They were requested to abstain from alcohol for three days and smoking for at least 24 hours prior to eye tracking. Compliance with this request was confirmed with reports from nursing staff and/or family members. The eye tracking was done in the electrophysiology laboratory of Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, on Amplaid MK-15 (Amplaid, spa, 20139 Milano, Italy) electrodiagnostic system. Silver-silver chloride electrodes were placed at the nasal and temporal canthi of each eye (four-electrodes). After the forehead of the patient was thoroughly cleaned with spirit and ether to reduce the skin impedance, the fifth neutral electrode was placed on it. The patient was seated at a fixed distance (130 cm) from the oculomotor stimulator OM 15 (Amplaid, Italy). The OM 15 has an array of multiple light-emission diodes which generate smooth target movements without any moving part. The target amplitude was 30° at 130 cm with two speeds, 0.25 cycles per second (cps), and 0.5 cps. Sinusoidal tracking was used as it is more suitable for studying SPEM abnormalities in schizophrenics. Calibration was done before and after each eye-track recording. Fixation was also recorded for 12 seconds.
The observations were made on: (1) the average gain of pursuit movement, (2) the frequency of all saccades (compensatory or intrusive), and (3) for the frequency of each type of saccade: catch-up saccade, break-up saccade, anticipatory saccade and square wave jerks, as per the standard description.[2,7]
The data were analysed using the chi-square test for gender and t-test for comparing age and average pursuit gain. Rank-sum two sample (Mann-Whitney) test was used to compare the frequency of saccades and fixation deviation.
The average pursuit gain [Table:1] was found to be less in schizophrenics compared to controls at both target velocities, 0.25 cps and 0.50 cps. The difference at 0.25 cps was not significant (p=0.054) but it was statistically significant at 0.5 cps (p=0.007) by t-test.
[Table:2] shows the frequency of saccades of both compensatory and intrusive types (all types of saccades). The frequency at 0.25 cps was 3.85 ± 2.0 for schizophrenics compared to 0.60 ± 0.60 normals and at 0.5 cps 4.04 ± 1.20 for schizophrenics and 0.40 ± 1.12 for the normals. The t values by the Mann-Whitney test, were 4.4 and 4.7 respectively, suggesting a p-value of 0.000 (p< 0.001), indicating a significant difference.
[Table:3] shows the frequency of the different types of saccades ([Figure:1] and [Figure:2]). The catch-up saccades and back-up saccades which are compensatory saccades, were found to be marginally more than the controls but the difference was statistically not significant. However, the anticipatory saccades showed a clearly different presentation in schizophrenics compared to normals. Among schizophrenics the mean frequency was 2.79 ± 1.88 saccades per cycle at 0.25 cps and 3.29 ± 1.41 saccades per cycle at 0.5 cps, compared to none of the normals showing anticipatory saccades. Mann-Whitney tests indicate t-values of 4.6 and 4.8 with a probability value of 0.000 for both the target velocities. The square wave jerks were also seen in a few schizophrenic patients at 0.5 cps but were not seen in controls, but the difference was not statistically significant.
[Table:4] shows the deviation during steady fixation. A deviation of more than 1 degree on either side of the baseline was considered significant. Based on the criteria, the mean frequency of deviation was 4.27 ± 2.51 in patients compared to 2.0 ± 2.0 in controls (t: 2.58 and p: 0.005). Further, we studied the correlation coefficient of various parameters and anticipatory saccades with the duration of illness, which may be indicative of chronicity and an indirect evidence of severity. [Table:5] shows the average gain frequency of all saccades and frequency of anticipatory saccades. The frequency of anticipatory saccades showed a good correlation at 0.25 cps as well as 0.5 cps target movement. The frequency of all saccades also showed a good correlation for 0.25 cps target velocity.
The interest in eye movement abnormalities in schizophrenics started when Diefendorf and Dodge described these and coined the term "praecox pursuit". These abnormalities were subsequently confirmed by Couch and Fox, and White. Subsequently, both qualitative ratings and global quantitative scores have been shown to have a consistently higher rate of eye-tracking disturbances (ETD) in schizophrenia patients compared to normals.[11-13]
Additional support for specificity came from studies showing higher rates of ETD in schizophrenics compared to those of affective disorders[11,14] and non-psychotic disorders.[15,16] On the other hand, bipolar and unipolar patients have performed normally[15,16] as also patients with schizophreniform disorders. Further, first- and second-degree biological relatives of schizophrenia patients including both clinically discordant co-twins and other family members unaffected with schizophrenia usually have a higher rate of ETD),[12,13,18-20] whereas relatives of patients with affective disorders and non-psychotic patients do not show ETD rates different from that of the normal population. ETD abnormalities include reduced gain of pursuit movement with increased frequency of corrective catch-up saccades and back-up saccades, and also abnormal intrusive saccades disturbing a smooth pursuit eye movement. In the latter the observation of square-wave jerks and anticipatory saccades is noteworthy.
In this study, to compare eye tracking disturbances between schizophrenic patients and normal controls, four variables in eye movement were studied to select the most sensitive one. The four variables are: pursuit gain, frequency of all saccades, frequency of different types of saccades and the deviation during fixation. All the four variables have been shown to differ in the two groups, corroborating previous studies.
The mean pursuit gain at lower target velocity (0-25 cps) was lower in patients compared to controls, but the difference was only marginally significant (p=0.54). However, at 0.5 cps, the difference was more marked and was statistically significant (p=0.007, see [Table:1]). This would suggest that a 0.5 cps target velocity pursuit should be chosen to distinguish ETD in schizophrenia. This also clarifies the variable observations of some authors' inability to show difference in pursuit gain in schizophrenics.[2,21,22]
The frequency of all saccades irrespective of type showed a significant difference between the schizophrenic patients and normals [Table:2]. This was true for both target velocities of 0.25 cps and 0.50 cps. The statistical significance of p< 0.001 suggests a high degree of confidence. This corroborates the results of other workers.
Observing the frequency of specific types of saccades, it was observed that the catch-up saccades and back-up saccades that have received attention for some time, do not show a statistically significant difference. This was also reported by Abel et al. On the other hand, the anticipatory saccades (AS) differ strikingly in their frequency in schizophrenia and normal controls [Table:3]. Patients made a mean 2.79 AS per cycle (which lasts 2 seconds for 0.50 cps) for the two target velocities. The controls did not make any AS at either target velocity tracking. This has also been observed by others.[25,26] It has been observed by Levy and Holzman that the cycles of eye tracking consisting of AS are not samples of smooth pursuit and do not accurately reflect the functional integrity of the smooth pursuit system. According to them these are eliminated by instructions. But it has been observed by Stark that they are not simply due to general failure of attention as they occur in successful pursuit. They may be considered to be due to failure of involuntary attention. We also observed that the frequency of anticipatory saccades is correlated with the duration of illness of schizophrenia, unlike some other variables [Table:5]. This would further emphasise the significance of anticipatory saccades that may provide an insight into the aetiology of schizophrenia.
Finally, with regard to the fourth variable of deviation of eyes during fixation of more than one degree in amplitude over a period of 12 seconds [Table:4]. This was also significantly different in the two groups (p=0.005). This type of measure has not been reported in the literature earlier, though saccades during fixation of a stationary target have been reported by Schmid-Burgk et al.
To conclude, an electro-oculographic recording of eye movements tracking a sinusoidal target can be helpful in the diagnosis of schizophrenia. Particularly, a simple assessment of the frequency of anticipatory saccades per cycle can be further studied as a possible biological diagnostic test for schizophrenia. The high frequency of anticipatory saccades also needs study from the point of view of aetiopathogenesis of this disease.
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