Schizophrenia Research, 7 (I 992) 159-l 68 159

0 1992 Elsevier Science Publishers B.V. All rights reserved 0920-9964/92/$05.00

SCHIZO 00230

Scanning eye movements in schizophrenic patients

Relationship to clinical symptoms and regional cerebral blood flow using
1231-IMP SPECT

Masahiko Tsunoda, Masayoshi Kurachi, Satoru Yuasa, Youichi Kadono, Miye Matsui and
Akinori Shimizu
Depurtmenr qf Neuropsychiulry, Faculi_y of Medicine, Tqvama Medical and Pharmaceutical Univrrsity, To~amu, Japan

(Received 19 March 1991; revision received and accepted IO February 1992)

Eye movements during the Benton Visual Retention Test were examined using an eye-mark recorder in 32
schizophrenic patients and 32 normal controls. The patients had significantly fewer eye fixations, longer
mean duration of fixation and shorter length of mean scan path than the controls. In the patients, these
eye movement parameters were significantly correlated with the negative symptom score but not with the
positive symptom score on the Positive and Negative Syndrome Scale. These parameters had a significant
correlation with the composite score on the Scale for the Assessment of Negative Symptoms (SANS). In
particular, they were highly correlated with avolition-apathy and affective flattening or blunting scores on
SANS subscales. Thus, examination of scanning eye movements seemed to be a good objective index of
negative symptoms. Secondly, regional cerebral blood flow (rCBF) was examined using N-isopropyl-p-
[‘231]iodoamphetamine (123I-IMP) and single photon emission computer tomography in 17 of 32 patients.
With regard to the relationship between the eye movement parameters and rCBF, the mean duration of
fixation was negatively correlated with lz31-IMP uptake in the left superior frontal area and left basal
ganglia. The mean length of the scan path was correlated with uptake in the left superior frontal area.
These findings suggest that the characteristic eye movements of schizophrenic patients are likely to be
related with dysfunction of the frontal-basal ganglia neural circuit.

Key word.s: Eye movement: Single photon emission computer tomography; (Schizophrenia)

INTRODUCTION open. With regard to the former, Shimazono et al.

(1965) using an electrooculogram (EOG) with
subjects at rest, found that chronic schizophrenic
The examination of eye movements has been used patients showed small rapid eye movements more
as a psychophysiological method of investigating frequently than normal controls. Studies with the
the pathophysiology of schizophrenia. Eye move- eyes open are further classified into two types: the
ments seem to reflect various functions such as study of tracking eye movements when subjects
level of consciousness, attention and cognitive are pursuing a visual target and the study of
behavior. There are at least two conditions for the scanning eye movements when subjects are viewing
study of eye movements: eyes closed and eyes a figure or picture. Studies of tracking eye move-
ments in schizophrenic patients have shown disor-
Correspondence to: M. Tsunoda, Department of NeuropSy-
ders of smooth pursuit eye movement, that is,
chiatry, Faculty of Medicine, Toyama Medical and Pharma- occasional saccadic intrusions and saccadic smooth
ceutical University, 2630 Sugitani, Toyama-shi, Toyama pursuit tracking (Holzman et al., 1973; Shagass
930-01, Japan. et al., 1974; Levin et al., 1982). In addition, several
160

studies have indicated possible disturbance of sac- subjects of our study. Single photon emission
cadic eye movements (Schmid-Burgk et al., 1982). computed tomography (SPECT) is now one of the
With respect to scanning eye movements, Moriya most useful methods for studying the functions of
(1979) first reported the impairment of eye move- the living human brain. In order to understand
ments in schizophrenic patients using an eye-mark the neural mechanism of eye movement distur-
recorder. He observed that chronic schizophrenics bances in schizophrenic patients, we investigated
and their relatives had less frequent eye movements the relationships between eye movements and
and a more limited area of inspection than normal rCBF using SPECT and N-isopropyl-p-[‘231]iodo-
controls when viewing an S-shaped geometric amphetamine (‘231-IMP).
figure. Thereafter, Kojima et al. (1986, 1989, 1990)
found that the ‘Responsive Search Score’, which
is the total number of sections on which the METHODS
subjects’ eyes fixed in response to the confirmative
question, was significantly lower in schizophrenics Subjects
than in normals. Gaebel et al. (1986, 1987, 1989) Thirty-two patients with schizophrenia (16 males
also investigated the relationships between visual and 16 females, 28.4 f 5.2 years) diagnosed accord-
search behavior, EEG and psychopathology in ing to DSM-IIIR (American Psychiatric Associa-
patients admitted with schizophrenia. tion, 1987) and 32 normal controls (16 males and
Eye movements with the eyes closed seem to be 16 females, 26.4& 3.8 years), who gave informed
related to the arousal level or habituation, while consent, were examined. The schizophrenic
tracking eye movements are related to attentional patients were in- or outpatients of Toyama Medical
performance. Scanning or searching eye move- and Pharmaceutical University Hospital. The
ments are considered to be related to active atten- mean duration of illness was 5.2 f4.6 years.
tion or the higher cognitive functions. Therefore, Patients with alcohol or drug dependency, visual
assessments of scanning or searching behavior in disturbance, or neurological dysfunction were
a spontaneous looking situation seem to be a excluded from the study. All schizophrenic patients
useful method of recording and analyzing objec- were on neuroleptic medication (mean daily dosage
tively the cognitive dysfunctions underlying schizo- 485 & 353 mg CPZ). The normal controls consisted
phrenic symptoms. Moriya (1979) reported that of medical students, nurses and staff members of
the reproduction of an S-shaped figure was poor the hospital. Educational level was higher for
in schizophrenic patients. This finding led us to controls (15.0 f 3.8 years) than for schizophrenic
use the Benton Visual Retention Test, which is patients (12.9f 1.8 years). All subjects had at least
widely used in the field of neuropsychology. We 0.5-0.5 eye sight by naked or corrected vision.
investigated eye movements in schizophrenic
patients during the Benton Visual Retention Test Procedure
using an eye-mark recorder. To elucidate what sort The subject sat on a chair 1.2 m in front of a
of clinical symptoms eye movement parameters translucent screen and was given Administration A
reflect, we examined relationships between eye of the Benton Visual Retention Test (Form 1)
movement parameters and clinical symptoms. In (Benton, 1963); ten test figures were rear-projected
recent years, a classification of schizophrenic symp- on the screen for 10 s by means of a Kodak
toms into positive and negative has been proposed. projector. The width of the figure was 32” horizon-
This has heuristic value for the study of pathophys- tally and 10” vertically. Figure 8 was reversed in
iology in schizophrenia. Considering this, we inves- order to equalize the number of peripheral figures.
tigated the relationships between eye movements The subject was asked to study the figures shown
and clinical symptoms using the Positive and Nega- on a screen for 10 s and immediately thereafter to
tive Syndrome Scale (PANSS) (Kay et al., 1986) recall the figure by drawing it. The drawings were
and the Scale for the Assessment of Negative assessed by the examiner afterward. While the
Symptoms (SANS) (Andreasen, 1981). patients were viewing the 5th to 10th figures, the
Regional cerebral blood flow was measured at eye movements were recorded with an eye-mark
rest in 17 schizophrenic patients who were the recorder (Nat V type). The eye-mark recorder
consists of a helmet which is equipped with very The psychopathological status of the schizophre-
small video cameras attached to the left and right nic patients was assessed by two doctors with the
sides and the top of the helmet. The side cameras Scale for the Assessment of Negative Symptoms
record the infrared lights reflected on the eyeballs. (SANS) (Andreasen, 1981) and the Positive and
The camera on the top of the helmet records Negative Syndrome Scale (PANSS) (Kay et al.,
figures on the screen. These recordings are stored 1987). In 26 of the 32 schizophrenic patients
in a video tape recording system. This technique Wechsler Adult Intelligence Scale (WAIS) tests
enables us to see the eye-fixation points and eye (Wechsler, 1955) were performed.
movements on the figure simultaneously. The data On another day, regional cerebra1 blood flow
of 6 figures recorded with the eye-mark recorder was studied using ‘231-IMP SPECT in 17 of the
were analyzed by a computer. A fixation point 32 schizophrenic patients and 5 of the controls.
was defined as a gaze held for more than 200 ms. The relationships between the eye movements and
The following parameters were extracted: mean the SPECT images were examined. The subjects
number of fixation points per test figure (MNF), remained quiet and cooperative during this scan
mean duration (s) of a single fixation (MDF) and procedure. Three mCi of ‘231-IMP was injected
mean scan path (degree) (MSP). MSP is the dis- into an antecubital vein while the subjects were in
tance between two successive eye fixations. the supine position with their eyes closed. The

Fig. 1. Regions of interest (ROIs). Fs, superior frontal gyrus; Fm, middle frontal gyrus; BG, basal ganglia; Fsp, superior frontal
gyrus; C, precentral gyrus; L, limbic lobe; P. inferior parietal lobe; T, superior temporal gyrus; Fl, F2, F3. frontal gyrus;
F4, precentral gyrus: PI, inferior parietal lobe; 01, occipital gyrus; Ce, cerebellum.
 162

subject’s heads were fixed with a molded plastic RESULTS

headholder as the transverse slices were taken
parallel to orbito-mental (OM) line. About 15 min
after injection three-dimensional data sets were Fig. 2 presents the sequence of eye movements of
reconstructed with a slice thickness of 6 mm. For a schizophrenic patient and a normal control. The
quantitative analysis, 30 regions of interest (ROIs) eyes moved less frequently and the scanning range
were designated in 3 coronal and 2 sagittal slices of the fixations was much more limited in the
(Fig. 1) (Yuasa et al., 1990). The 3 coronal slices schizophrenic patient.
were vertical to the OM line and 39%, 46%,
54% from the frontal pole. The 2 sagittal slices Elementary components of eye movements
were 40% lateral from midline. The coordinates The elementary components of eye movements
of the ROIs were obtained from an atlas (Matsui consist of MNF, MDF and MSP. Fig. 3 shows
and Hirano, 1977). Each ROI was square with distributions of the elementary components.
an area of 20.25 pixel units (each unit = Table 1 presents a comparison between schizophre-
6mm x6 mm x6mm). Slice 1 presents the ROIs nic patients and controls of eye movement parame-
of the superior frontal gyrus, middle frontal gyrus ters. Unpaired t-tests indicated that the MNF of
and basal ganglia of both sides. The ROIs of the patients was less than that of normal controls
superior frontal gyrus contain the supplementary (t=2.52, df=62, ~~0.05). The MDF of the
motor areas and those of basal ganglia contain patients was longer than that of normal controls
part of the caudate nucleus, putamen and globus (t=4.48, df=62, p<O.Ol). The patients had
pallidus. We calculated the ratio to the cerebellum shorter MSP than normal controls (t = 6.45, df =
by dividing the value of each ROI by that of the 62, p<O.Ol). The number of correct scores on the
cerebellum. We also calculated the ratio to the Benton Visual Retention Test for the patients was
whole brain by dividing the count of each ROI fewer than the normal controls (t= 6.63, df= 62,
by the average count of all ROTS. SPECT imaging p<O.Ol). The error scores of the patients were
was performed on a General Electric Maxi Cam- higher than those of the controls (t= 5.83, df= 62,
era 400/AT and Maxi Star with middle-energy ~~0.01). When the error scores of the right and
collimeter. left periphery were analyzed by paired t-tests,

*. 743
Schizophrenic patient
\m Normal control
A

Fig. 2. (A) Sequence of eye movements of a schizophrenic patient and a control. A circle indicates a single fixation and the size of
circle indicates a duration of a fixation. (B) Immediate recall after a 10-s exposure.
 163

Hcan scan path (deg) Hcan duration of a

LL
- 0.5-

singic
O.G-

flxatlon
0 l-

(see)

Fig. 3. Distributions of eye movement parameters.

TABLE 1 movement parameters and dosage (MNF: r=

Comparison between schizophrenics and controls ofeye movement -0.27, n.s.; MDF: r=0.22, ns.; MSP: r= -0.12,
parameters during the Benton Visual Retention Test ns.). We examined the eye movement measure-
ments twice in 6 schizophrenic patients and 5
Schizophrenics Controls t-Test
normal controls. In the normal controls, the results
(n = 321 (n = 32)
of the two measurements were almost identical
MNF 18.9k3.4 20.7 +2.5 2.52* (MNF: 20.6 vs. 20.5; MDF: 0.36 vs. 0.37; MSP:
MDF (s) 0.45*0.11 0.35 kO.05 4.4s** 6.9 vs. 6.7). In the schizophrenic patients, both
MSP (deg) 4.9* I.0 6.8? 1.2 6.45** were also similar in case of the same clinical states.
NCS 6.1 _t2.2 8.9kO.9 6.63*+ WAIS was performed in 26 of 32 schizophrenic
NES 5.523.7 1.4+ 1.3 5.83**
patients. There was a positive correlation between
*p < 0.05, **pi 0.01 (unpaired t-Test). Verbal IQ (r = 0.64, p < 0.01) or Full Scale IQ (r =
MNF, mean number of fixation points for a figure of the test; 0.53, ~~0.01) of WAIS and correct scores of
MDF, mean duration of a single fixation; MSP, mean scan Benton Visual Retention Test. There was no sig-
path: NCS, number of correct scores on the test; NES, number nificant relation between IQ of WAIS and eye
of error scores on the test.
movement parameters (MNF, MDF, MSP). These
results suggest that the level of intelligence influ-
errors on the right side were found to be more ences the scores of Benton’s test, but not eye
frequent than those on the left in the patients (t= movements. In the present study, educational level
3.15, df=31, ~~0.01) but not in the controls (t= was significantly higher for controls than for schiz-
1.53, df= 31, n.s.) (Table 2). ophrenic patients, but eye movement parameters
None of the relationships between eye movement seemed not to be influenced by the difference of
parameters and performance on the Benton Reten- educational level.
tion Test were significant in terms of correct scores
(MNF: r=0.26, n.s.; MDF: r= -0.17, n.s.; MSP: Relation between eye movement parameters and
r-0.14, n.s.) or error scores (MNF: Y= -0.27, clinical symptoms
n.s.; MDF: r=0.23, n.s.; MSP: r=-0.13, n.s.). The eye movement parameters were correlated
There was no significant relation between eye with the negative symptom scores on the PANSS
164

TABLE 2

Comparison between schizophrenics and controls of errs scores on the Benton Visual Retenrlon Tesl

Left hdf RighI half f-Test L<ft peripheral Right peripheral i- Te.sr

Schizophrenics 2.3 i 2.0 3.Oi2.3 1.73 1.0+1.4 1.8& 1.2 3.15**

Controls 0.5 * 0.8 0.8+0.8 1.60 0.3 + 0.5 OSkO.6 1.53

**p < 0.01 (paired f-test).

(MNF: Y= -0.47. ~~0.01; MDF: r-0.38, flattening or blunting (r = ~ 0.52, p < 0.01; r = 0.42,
~~0.05; MSP: r= - 0.41, ~~0.05) but did not p < 0.05; r = - 0.42, p < 0.05; respectively) but not
with the positive symptom scores (Y= 0.02, n.s.; with attention (r = - 0.25, n.s.; r= 0.14, n.s.; r=
Y= 0.01, ns.; r= - 0.32, n.s.; respectively) in schiz- - 0.28, n.s.; respectively). There was no significant
ophrenic patients (Table 3). relation between performance on the Benton
The relationships between eye movement param- Visual Retention Test and clinical symptoms. In
eters and the scores on SANS are given in Table 4. the present study, Pearson’s product moment cor-
There was a positive correlation between MDF relations between the scores obtained by two raters
and the composite SANS scores (r = 0.43, p < 0.05). were as follows: PANSS (positive subscale), r=
In the same way, there was a negative correlation 0.91; PANSS (negative subscale), r = 0.88; SANS
between MNF (v= -0.53, ~~0.01) or MSP (v= (composite score), r = 0.89; SANS (affective flatten-
- 0.42, p< 0.05) and the composite scores. Con- ing or blunting), r = 0.92; SANS (alogia), r = 0.88;
cerning the subscales of SANS, the parameters SANS (avolition-apathy) r = 0.83; SANS (anhedn-
were highly correlated with avolition-apathy ia-asociality), r = 0.94; SANS (attention), r = 0.89.
(MNF: r= -0.58, p<O.Ol; MDF: r=0.60,
~~0.01; MSP: r= -0.41, ~~0.05) and affective Relation between eye movement parameters and
rCBF using
lz31-IMP SPECT
TABLE 3 Regional cerebral blood flow was measured using
Correlation coejicien, between eye movement parameter.7 and
lz31-IMP SPECT in 17 of the 32 patients and 5
scores on PANSS of the 32 controls. In the patients Spearman’s rank
test indicated that MDF was negatively correlated
PANSS MNF MDF MSP with ‘231-IMP uptake using the ratio to cerebellum
in the left superior frontal area (rs= -0.57,
Negative symptoms - 0.47** 0.38* -0.41*
Positive symptoms 0.02 0.01 -0.32 p< 0.05) and left basal ganglia (r, = - 0.46,
~~0.05). MSP was also correlated to uptake in
*p<O.O5, **p<O.Ol (Pearson). the left superior frontal area (r,=0.62, ~~0.01)
For abbreviations see Table 1. (Fig. 4, Table 5). In the same way, there was a

TABLE 4
TABLE 5
Correlation coeffcienr between eye movement parameters and
SANS subscales Rank correlation coeficienl (r,) between eye movement parame-
ters and ‘231-IMP uptake using the ratio to the c~erehrllum in=
SANS subscales MNF MDF MSP 17J

1. Affective flattening or blunting - 0.52** 0.42* - 0.42* Superior frontal area Basal ganglia
2. Alogia - 0.45* 0.32 - 0.36*
3. Avolition-apathy - 0.58** 0.60** L 0.41* L<fi Right Left Right
4. Anhedonia-asociality - 0.39* 0.30 - 0.22
5. Attention ~ 0.25 0.14 -0.28 MDF ~ 0.57* ~ 0.28 - 0.46* 0.17
Composite score - 0.53** 0.43* ~ 0.42* MSP 0.62** 0.37 0.38 0.25

*piO.O5. **p<O.Ol (Pearson). *pi 0.05, **p < 0.01 (Spearman).

For abbreviations see Table 1. For abbreviations see Table I.
 165

Left basal ganglia Left superior frontal area

.
.
l l Schizophrenic
lOI n . A Control
&A l

I
’ : .
IC .*
. l* . .

.
00 . .
.

10

c
0:3 0’1 0:5 3 1 5 6 1

Mean duration (secl Mean scan path (de91

Fig. 4. Correlation between eye movement parameters and lz31-IMP uptake using the ratio to the cerebellum

negative correlation between MDF and IMP contact’ and ‘motionlessness’, but not with ‘halluci-
uptake using the ratio to whole brain in the left nation and delusion’ or ‘disturbance of self’ as
superior frontal area (r, = - 0.59, p < 0.05) or left determined by the rating scale of Kyushu Univer-
basal ganglia (Ye= - 0.53, ~~0.05). MSP was sity. Gaebel (1989) stated that minimal scanning
correlated to the uptake in the left superior frontal was related to negative symptoms, especially emo-
area (v,=O.51, pCO.05). tional withdrawal (Brief Psychiatric Rating Scale)
and restricted affect (SANS). In our study as well,
eye movement parameters were significantly corre-
DISCUSSION lated with negative symptoms, especially avolition-
apathy and affective flattening or blunting. These
results suggest that examination of scanning eye
In the present study, schizophrenic patients had movements would be a good objective index of
significantly less MNF, longer MDF and shorter negative symptoms.
MSP on the Benton Visual Retention Test than Attentional deficits are frequently found in schiz-
normal controls. These results correspond with ophrenic patients. In the present study, however,
Moriya’s (1979) and Kojima’s (1986, 1989, 1990) the eye movement parameters were not correlated
reports using an S-shaped figure and a picture. with attention on the SANS subscales. We cannot
Gaebel (1989) divided scanning eye movements of conclude that eye movement parameters are not
schizophrenic patients in a free-looking situation related with attention, since SANS assesses only
into two types: ‘minimal scanning’ and ‘extensive one aspect of attentional performance. However,
scanning’. The former was characterized by longer narrow scanning was related to avolition or affec-
MDF and shorter MSP, and was related to poor tive blunting, and it seems difficult to attribute
search performance, while the latter differed these symptoms to attentional disturbance. Scan-
slightly from the scanning of normal controls. The ning eye movements are considered to represent
‘minimal scanning’ type coincided with our results, higher cognitive behavior, including active
but we were not able to observe the other viewing attention.
style during Benton’s test (Fig. 3). In the present study, correct scores on the Ben-
In regard to the relation between eye movements ton Visual Retention Test were significantly lower
and clinical symptoms, Moriya (1979) reported for the schizophrenics than for the normal controls.
that inadequate eye movement (narrow scanning) The error scores of the patients were significantly
was associated with ‘bizarre postures’, ‘lack of higher than those of the controls. Contrary to our
166

expectation, neither correct nor error scores were movement disturbances in schizophrenic patients
significantly correlated with eye movement param- is a dysfunction of the internal information circuit
eters. Correct performance on the Benton Visual through the left basal ganglia. There could be two
Retention Test requires complex information pro- reasons why dysfunction of the circuit pars basal
cessing: external information accessing by eye ganglia occurs in schizophrenics. One is the effect
movements, and the next internal information of medication. The present tests were performed
processing. Both may be required in reproducing in patients who were under treatment with various
Benton’s figures. The internal information process- drugs; therefore the effect of medication on ocular
ing might also be disturbed in schizophrenic movements cannot be excluded. But we found no
patients. significant correlation between eye movement
Schizophrenic patients showed significantly parameters and dosage. Moriya (I 979) also found
more errors for right peripheral figures than the no relation between the two. Therefore. the effect
controls. and the errors for right peripheral figures of medication on eye movements seems to be
were more frequent than those for left peripheral slight, if any. In order to exclude the effect of
figures in the patients. Our results were in accor- medication, drug-free patients need to be examined
dance with those of Kawazoe et al. (1987). This in the future. The other reason is the pathophysiol-
finding in schizophrenia is possibly caused by left ogy of schizophrenia. Several researchers (Ingvar
hemispheric dysfunction, since the right visual field and Franzen, 1974; Kurachi et al., 1985, 1987;
is connected with the left hemisphere. Another Weinberger et al., 1986) have reported frontal lobe
reason why errors for the right periphery were dysfunction in schizophrenic patients, while others
higher than those for the left may be the eye (Bogaerts et al., 1985; Stevens, 1986; Buchsbaum
movements themselves in schizophrenic patients. et al., 1987) have indicated basal ganglia dysfunc-
We did not analyze the laterality of the eye move- tion. In recent years, some investigators (Wolfson
ments directly, but Kawazoe et al. (1987) indicated et al., 1985) have observed the dysfunction of the
that there was a tendency for schizophrenics to frontal lobe and basal ganglia in parkinsonian
look less frequently at the right hemifield compared patients. Therefore, to understand the mechanism
to controls during the Benton Retention Test. of eye movement disturbances in schizophrenia, it
Gaebel (1989) also showed that minimal scanners would be informative to compare the eye move-
were characterized by a left-sided deviation of their ments of schizophrenic patients with those of
gaze focus with respect to gaze direction during a parkinsonian patients.
search task. These findings support the relative Roland et al. (1982) measured rCBF of the
hypofunction of the left hemisphere in schizophre- cortex and basal ganglia during voluntary move-
nic patients. ment of the fingers in normal volunteers. They
In recent years, the neural mechanism of eye reported that rCBF increased bilaterally in the
movements has become clearer. Based on studies supplementary motor areas (30%), head of the
of saccadic eye movements, Hikosaka (1983, 1989) caudate nucleus (I l-l 5%) and putamen (15%)
considered that there were internal information and they noted a strong contralateral increase
circuits passing through the prefrontal cortex and (30%) and a weaker ipsilateral increase (14%) in
basal ganglia, and external information circuits the globus pallidus. The findings of these regions
mainly passing through the parietal cortex and correspond with those of the regions to which eye
frontal eye field. He explained that the substantia movement parameters were related in our study.
nigra was the origin of GABAergic tonic inhibition Guenther et al. (1986) measured rCBF in schizo-
and that the caudate nucleus controlled the inhibi- phrenic patients who were given the task of squeez-
tion of saccadic eye movement by changing the ing a handle. They observed a widespread
level of nigro-collicullar inhibition. In the present nonreactivity of rCBF and no flow increase in the
study we used ‘231-IMP SPECT and found a contralateral primary motor area in schizophrenics
correlation (Table 5) between eye movement with marked negative symptoms (Type II) (Crow
parameters and the ‘231-IMP uptake in left supe- et al., 1980). These findings suggest that the eye
rior frontal area and basal ganglia. These results movement dysfunctions that we obtained in the
suggest that the underlying mechanism of eye patients represent a partial phenomenon of a more
 167

generalized movement dysfunction. Goldberg functions of monkey substantia nigra pars reticulata. 3.
Memory-contingent visual and saccade responses.
(1985) proposed two motor systems for voluntary
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