Schizophrenia Research 34 (1998) 195–205
Covert visual attention in patients with early-onset schizophrenia M. Øie a, B.R. Rund b,*, K. Sundet c a National Centre for Child and Adolescent Psychiatry, University of Oslo, PO Box 1094, Blindern, N-0317 Oslo, Norway b Institute of Psychology, University of Oslo, PO Box 1094, Blindern, N-0317 Oslo, Norway c Department of Psychosomatic and Behavioral Medicine, The National Hospital, University of Oslo, PO Box 1094, Blindern, N-0317 Oslo, Norway Received 20 February 1998; accepted 22 July 1998
Abstract The aim of the present study is to examine attentional costs (inhibition) in covert visual attention in a group of acutely ill adolescents with schizophrenia without long histories of neuroleptic treatment. Variations in reaction time were analyzed for possible age and sex differences. Adolescents with schizophrenia (n=19) were compared to a group of ADHD subjects (n=20) and a group of normally functioning adolescents (n=30) on a measure of covert visual attention. The results support a hypothesis of abnormally rapid disengagement (reduced costs) in male adolescents with schizophrenia. Such an abnormality has also been found in adults with chronic schizophrenia. Whether this holds true for both sexes of adolescents with schizophrenia or is restricted to male subjects cannot be answered with certainty due to the small number of females with schizophrenia in our sample. Our findings indicate, however, that there are some general sex differences and some specific sex differences related to covert visual attention in adolescents with schizophrenia. © 1998 Elsevier Science B.V. All rights reserved. Keywords: Covert visual attention; Early-onset schizophrenia; Attentional costs
1. Introduction Schizophrenia has long been suggested to be related to an impairment in the regulation of attention. In the present study, adolescents with schizophrenia are compared to adolescents with ADHD and a group of normally functioning adolescents on a measure of covert visual attention developed by Posner (1980) and Posner et al. (1980). In this paradigm, subjects are instructed to respond as quickly as possible to targets in the right or left visual field. Targets are preceded by * Corresponding author.
no cue, or by cues that either correctly signal the location of the impending target (valid cue), or misdirect attention to the opposite visual field (invalid cue). On 80% of the cued trials, the cue is valid. The time between the preceding cue and the target (SOA) is either short (100 ms) or long (800 ms). Responses in the short interval are automatic and occur without volitional control. In contrast, the long interval produces a faster reaction time and allows a greater voluntary control, presumably in part because of a greater attentional facilitation of response processes echoing caudal to rostral processing of attentional cues (Eimer, 1993). Reaction times are compared with baseline
0920-9964/98/$ – see front matter © 1998 Elsevier Science B.V. All rights reserved. PII: S0 9 2 0 -9 9 6 4 ( 9 8 ) 0 0 09 2 - 9
196
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
trials in which the target is preceded by no cue. Such a comparison can give a cost–benefit analysis of performance. Studies using this procedure have consistently demonstrated a faster performance for validly cued trials (benefit) and a slower performance for invalidly cued trials (cost) (Posner et al., 1980; Jonides and Mack, 1984). Through studies of both normal subjects and patients with discrete lesions, Posner et al. (1987) have proposed that the shifting of covert attention to a new location in space can be divided into three separate mental operations that have distinct neuroanatomic substrates. These are: disengaging attention from a target of interest, which is associated with the posterior parietal region; movement of attention from the current stimulus to a new stimulus, which is linked to the midbrain near the superior colliculis; and reengagement of attention to the new target, which is a function of the thalamus or pulvinar. Thus, this widely used experimental paradigm has produced data on the underlying neural structures of visual selective attention. In a spatial attention task, two separate forms of visual–spatial orienting have been demonstrated (Carter et al., 1994; Posner and Cohen, 1984; Muller and Rabbit, 1989; Rafal et al., 1989). In one form, the procedures utilize peripheral cues that occur at the probable location of a subsequent target. The cues automatically summon attention to the target location, regardless of whether the cue has any inherent validity. This automatic facilitation of target detection occurs in the first 300 ms following appearance of the cue, and is followed by an inhibition of return. Inhibition of return is indicated by longer detection times for targets in the cued location than for targets occurring in locations opposite the cue (Posner and Cohen, 1984; Carter et al., 1992). This is considered to be a mechanism favouring the processing of novel stimuli during visual scanning by inhibiting the return of attention to a previously examined location in the visual field (Posner and Cohen, 1984; Rafal et al., 1989; Carter et al., 1994). In the second form of visual–spatial attention, a central cue having a strong predictive value for the location of the target is presented at the centre of the visual field; this cue is typically an arrow pointing toward the probable location of the
target. Central cues initiate only the controlled orienting mechanism. The controlled mechanism requires development of a spatial expectancy on the basis of the probabilistic information provided by the cue. The findings of cost and benefit hold whether the cue is peripheral or central (Posner, 1980). It has been suggested that controlled selective visual attention is mediated by networks that include the posterior parietal cortex and frontal lobes, whereas automatic selective visual attention is mediated by subcortical structures (Posner et al., 1984, 1988; Robertson et al., 1988; Carter et al., 1992). Posner et al. (1988) were the first to use this paradigm to study selective attention in schizophrenia. They demonstrated that acutely psychotic, mostly medicated inpatients with schizophrenia were slow in disengaging their attention from an invalid cue (increased costs) in the left visual field to a target in the right visual field in the 100-ms interval. This finding was interpreted as indicating a left hemisphere deficit in schizophrenia, similar to that seen in patients with left parietal lesions (Posner et al., 1984). Posner et al. (1988) employed peripheral cues in combination with a probability manipulation. Peripheral cues were presented with an 80% probability that the target would appear in the cued location. As such, Posner et al.’s findings are based on a task that does not discriminate between the automatic and controlled forms of spatial orienting. However, the controlled form of attention usually occurs at long intervals (see above). Subsequent studies of covert attention in patients with schizophrenia have yielded conflicting findings, possibly due to clinical heterogeneity, varied clinical status, or methodological differences. Potkin et al. (1989) replicated the findings of Posner et al. (1988) in chronic and nevermedicated patients with schizophrenia. Others have found no asymmetry in medicated chronic inpatients (Strauss et al., 1991; Gold et al., 1992; Moran et al., 1992; Liotti et al., 1993; Sereno and Holzman, 1996). Maruff et al. (1995) proposed that first-episode, unmedicated and medicated patients with schizophrenia have disadvantages in invalidly cued targets in the right visual field. This
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
is not the case for chronic, medicated patients who show no such visual field differences. Strauss et al. (1992) reported decreased costs for invalidly cued targets appearing in the right visual field in a group of moderately psychotic chronic patients with mostly negative symptoms. This pattern was also found by Nestor et al. (1992) in medicated chronic inpatients, and by Carter et al. (1992, 1994) in unmedicated, moderately symptomatic outpatients with chronic schizophrenia. Carter et al. (1994) reported findings suggestive of reduced costs during controlled orienting in the right visual field in a subgroup of stable unmedicated patients with chronic undifferentiated schizophrenia. More recently, Bustillo et al. (1997) reported a right visual field disadvantage in non-deficit patients with schizophrenia but not in subgroups of clinically stable, medicated patients with schizophrenia. Thus, the research in this field suggests that increased costs for invalidly cued targets appearing in the right visual field are evident in acutely ill patients with schizophrenia, in subgroups of patients with undifferentiated schizophrenia, and in non-deficit patients with schizophrenia. Decreased costs for invalidly cued targets in the right visual field seem to be evident in chronic, unremitted patients with a high level of negative symptoms. In the present study, a neuropsychiatric comparison group was included, in addition to a comparison group of normally functioning adolescents, to control for the effect of motivation, medical settings, and the generalized effect of having a psychiatric diagnosis. Patients with affective disorders and patients with Attention-Deficit Hyperactivity Disorder (ADHD) clearly manifest attentional disturbances. Due to the fact that there are few young subjects with affective disorders, adolescents with ADHD were included as a comparable neuropsychiatric group. This group of patients has also been examined with the Covert Visual Attention task. Swanson et al. (1990, 1991), using a version of the task which mixed automatic and controlled attention, reported an asymmetrical pattern of performance in ADHD patients in which the costs associated with invalidly cued left field targets were reduced or absent. Carter et al. (1995) showed the same pattern as shown by Swanson et al. (1990,
197
1991) in a version of the task selectively measuring controlled attention. This deficit was related to diminished right hemispherical frontal–striatal catecholamine activity. However, the ADHD subjects in Swanson et al.’s and Carter et al.’s studies were children with a mean age of 9 years (Swanson et al.) and 10.5 years old (Carter et al.). Sex differences have been largely ignored in the study of covert visual attention in schizophrenia, even though there is a considerable amount of literature suggesting that male patients with schizophrenia have a worse premorbid history, an earlier age at onset, larger ventricle brain ratios, and a more chronic course than female patients ( Watt, 1978; Lewine et al., 1981; McGlashan and Bardenstein, 1990). There is little consensus regarding sex differences in neuropsychological functioning in patients with schizophrenia (Lewine et al., 1996). Some investigators have found sex differences to vary by neuropsychological tasks ( Hoff et al., 1992). Lewine et al. (1996) showed that female patients with schizophrenia had greater difficulty than male patients on various visual processing tasks. Normal females have also been shown to have slower RTs than males (Coles et al., 1975). Due to the variability of results using covert visual attention tasks, the primary aim of the present study was to examine attentional costs (inhibition) in covert visual attention in a group of adolescents with schizophrenia without long histories of neuroleptic treatment. The hypothesis was that they would demonstrate an increased cost to invalidly cued targets appearing in the right visual field in the short interval, similar to the acutely ill patients in the studies of Posner et al. (1988) and Maruff et al. (1995) studies. Secondly, we wished to examine any possible sex differences in covert visual attention.
2. Subjects and methods 2.1. Subjects The schizophrenia group consisted of 19 subjects (mean age=16.2 years, s.d.=1.1; five females and 14 males) who met the criteria of a schizophrenic
198
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
disorder according to the revised third edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-III-R; American Psychiatric Association, 1987). The diagnoses were based on clinical interviews by senior clinicians and the patients’ case records. The specific diagnoses according to DSM-III-R were as follows: schizophrenia disorganized (n=11), schizophrenia paranoid (n=4), schizophrenia undifferentiated (n= 1), schizophreniform disorder (n=1), schizoaffective disorder (n=1), and delusional disorder (n= 1). A subsample of 13 patients with schizophrenia was diagnosed by two senior psychologists. They agreed on the specific schizophrenia diagnosis in 12 (92%) of the cases. The patients were followed up 6 months after discharge from hospital, and 1 year thereafter to confirm the initial diagnoses, which were unchanged. The mean duration of hospitalization at the time of testing was 11.7 weeks (s.d.=15.6). Eighteen subjects were right-handed, and one was left-handed. Eleven of the patients had not yet started neuroleptic treatment at the time of testing, whereas three of the patients were drug-free during testing and for a period of at least 5 days before testing. Five were receiving standard neuroleptic medication (perphenazin, 3; thioridazin, 1; zuclopenthixoli, 1). Eleven of the patients were assessed on the Brief Psychiatric Rating Scale (BPRS; Lukoff et al., 1986) within 1 week of testing. [For more detailed information, see Rund et al. (1996).] The mean total BPRS score was 61.1 (s.d.=19.3). The interrater-reliability (ICC 1,2) for the BPRS total score was 0.99. A ‘positive symptoms’ score based on the factor analysis conducted by Ventura et al. (1995) was extracted from the BPRS. This score consists of seven items. The mean positive symptoms score was 21.2 (s.d.=7.5). Both of these scores indicate that the patients were characterized by psychotic positive symptoms at the time of testing. The patients’ psychosocial functioning was assessed with the Global Assessment Scale (GAS; Endicott et al., 1976). The mean score was 41.7 (s.d.=12.0). The mean total raw score on the Child Behavior Checklist (CBCL; Achenbach, 1991) was 61.8 (s.d.=32.8). The estimated average IQ, as determined by the Similarities, Block
Design, Digit Symbol and Digit Span subtests from the Wechsler Intelligence Scale for Children— Revised ( WISC-R; Wechsler, 1974), was 98.2 (s.d.=11.4) in the schizophrenia group. The ADHD group consisted of 20 male adolescents (mean age=14.1 years, s.d.=1.5) who met the criteria from the DSM-III-R for ADHD. The skewed sex distribution reflects the fact that ADHD is much more common in boys than girls. They were significantly ( p<0.05) younger than the subjects in the two other groups. The ADHD diagnoses were based on information obtained from semi-structured interviews with the patients’ parents. The adolescents fulfilled at least eight of the DSM-III-R criteria for the condition. Attention problems were marked both at home and at school. In addition, all had exhibited significant hyperactivity, impulsivity and inattention between ages 6 and 10 as assessed by the Parent’s Rating Scale ( Wender et al., 1985). All were outpatients. None of the subjects had any history of psychosis. Seventeen subjects were right-handed, and three were left-handed. Twelve of the subjects received stimulant medication (methylphenidate, 11; dextroamphetamine, 1). The medication was discontinued for at least 24 h before testing. One patient received a small dose of haloperidol (1 mg day−1) because of tics. The mean total raw CBCL score was 60.3 (s.d.=17.7). The mean GAS score was 50.8 (s.d.=7.5). The group of patients with schizophrenia scored significantly lower on the GAS than the group of patients with ADHD (F=8.1, df=1,36, p=0.007). The mean estimated IQ was 98.6 (s.d.=11.2) in the ADHD group. The scores on the CBCL showed that the level of psychopathology in the patient groups was significantly above that of the normal comparison group: F(2,62)=70.02, p<0.001. Thirty healthy adolescent volunteers (mean age=15.7 years, s.d.=1.6; 14 females and 16 males) were included as a normal comparison group. The subjects attended regular school classes at normal grade level. Screening included the CBCL. Individuals with a total raw score higher than 45 were excluded. The estimated mean IQ was 110.5 (s.d.=9.5). Twenty-nine subjects were right-handed, and one was left-handed. The sub-
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
jects received a small compensation to cover their travelling costs. 2.2. Apparatus and procedure The Covert Visual Attention task was presented on an IBM PS/2 computer that controlled the stimulus displays and recorded the responses. MEL software (Psychological Software Tools, 1990) was used to administer the test. Stimuli were presented on a 14-inch Sony Trinitron monitor. Each candidate for the study was screened for head injury and neurological disorders including seizures. They were screened for mental retardation with the results of the Similarities and Block Design subtests of the WISC-R ( Wechsler, 1974). After the subjects had been informed with a complete description of the study, their written consent was obtained, as well as consent from one parent. The subjects were tested with a broad neuropsychological test battery. The Covert Visual Attention test was given at the start of the test battery. All subjects were tested individually in a darkened room and seated 70 cm from the monitor. They were instructed to keep their eyes fixed at a cross in the middle of the screen, and to press the space bar with the index finger of the dominant hand as quickly as possible whenever they detected a target in either of two peripheral squares positioned 10 cm from central fixation on either side. Five blocks of 48 trials were presented, for a total of 240 trials. On 83% of the trials, a visual cue was provided by brightening one of the two target locations either 100 or 800 ms before the target appeared. On 80% of the cued trials, the cue was valid, correctly indicating the location of the target; on 20% of the cued trials, the cue was invalid, the target appearing in the opposite location. On 17% of the trials, no cue was provided before the target appeared. The subjects were informed about the different cue types but not informed about their probability. The importance of maintaining central fixation was emphasized. RT was measured from the onset of the target to the onset of the key press. For each subject, the median RT for each condition was computed. RTs beyond 1500 ms (which was assumed to be an omission error) and
199
less than 100 ms (which was assumed to be an anticipation error or false alarm) were excluded. After the response, the target disappeared from the screen, and the two boxes remained on the screen for a 1000-ms intertrial interval. Short breaks between each block were provided. There was no monitoring of eye movements during the test session, but the test–retest reliability of this task was relatively high: 0.90 in the valid condition, 0.75 for the invalid condition and 0.55 for the no-cue condition (Posner et al., 1988). When significant interactions between visual field and condition were found in the analysis, specific measures of attentional benefit and cost were computed to examine the source of the interaction. Benefits were calculated by comparing RT for valid and uncued targets for the left and right visual fields. Costs were calculated by comparing the RT for uncued and invalidly cued targets for both visual fields. Because cost and benefit were measured in relation to a baseline uncued condition, relative measures of benefit [(uncued RT−valid cue RT )/uncued RT ] and cost [(uncued RT−invalid cue RT )/uncued RT ] were computed to control for the group differences in RT baseline. Further, a validity effect was calculated by comparing valid to invalid cue conditions. The measures of cost and validity effects are minimally influenced by age on RT since subjects serve as their own controls.
2.3. Data analysis Statistical analyses were performed using the SPSS for Windows, Release 6.1. (SPSS Inc., 1989–1994). Data were examined with a multivariate approach by an analysis of variance (ANOVA) for repeated measures with group (schizophrenia, ADHD, normal ) as the between-subject factor, and interval (800 ms, 100 ms), cue (valid, invalid, uncued ), and visual field ( left, right) as the withinsubject factors. To examine group differences between patients with schizophrenia and the comparison groups, follow-up ANOVAs with and without age as covariate were performed. Separate one-way ANOVAs were used to analyze the cost measures in males separately. Pearson correlations
200
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
were computed between the GAS score and measures from the test.
Table 2 Multivariate analysis of variance for group, visual field, cue and interval interactions (all right-handed, n=64) Effect
df
F
p
Group (corrected for age) Visual field Cue Interval Cue×interval Visual field×cue Visual field×interval Visual field×cue×interval Group×visual field Group×cue Group×interval Group×cue×interval Group×visual field×interval Group×visual field×cue Group×visual field×cue×interval
2, 60 1, 61 2, 122 1, 61 2, 122 2, 122 1, 61 2, 122 2, 61 4, 122 2, 61 4, 122 2, 61 4, 122 4, 122
0.36 4.37 54.32 136.25 16.27 1.86 0.56 0.25 1.26 0.37 0.84 2.25 0.11 0.54 1.26
0.698 0.041 0.001 0.001 0.001 0.161 0.457 0.779 0.292 0.828 0.437 0.068 0.895 0.708 0.289
3. Results The results are shown in Table 1. The data for left-handed subjects are excluded. However, when data from the left-handed subjects were included in the analysis, the results did not change significantly. The initial analysis showed a main effect of group [F[2,61]=3.10, p<0.05), reflecting that subjects in the ADHD group had overall slower RTs compared to subjects in the other groups. Since the subjects with ADHD were significantly younger than the subjects in the other groups, and because increasing age has been associated with an overall slowing of RTs on a visual–spatial processing task (Robinson and Kertzman, 1990), an analysis of covariance with age as the covariate was performed. The effect of group was not significant when correcting for age differences in this manner ( Table 2). The following main effects were significant: cue, with fastest RTs for validly cued targets compared to the invalidly and uncued targets; interval, with faster RTs in the 800-ms interval; visual field, with faster RTs for right visual field targets. Further, there was a significant interaction with cue×interval, with faster RTs in
the 800-ms interval for the validly cued targets in the 100 ms interval compared to invalidly cued targets, t(63)=2.75, p<0.008, for validly cued targets compared to invalidly cued targets, t(63)= 11.21, p<0.001, and for validly cued targets in the 100 ms interval compared to no-cue targets, t(63)=8.70, p<0.001, when collapsing the data across visual field. There were no significant interactions between the groups and any of the repeated measures of interval, cue or visual field. However, there was
Table 1 Reaction time for the experimental conditions in Covert Visual Attention task for patients with schizophrenia, Attention-Deficit Hyperactivity Disorder and normal adolescents (all right-handed ) Condition
Schizophrenia (n=18)
ADHD (n=17)
Normal (n=29)
Delay (ms)
Cue
Visual field
Trials
Mean
s.d.
Mean
s.d.
Mean
s.d.
100 100 100 100 100 100 800 800 800 800 800 800
Valid Valid Invalid Invalid No cue No cue Valid Valid Invalid Invalid No Cue No Cue
Left Right Left Right Left Right Left Right Left Right Left Right
40 40 10 10 10 10 40 40 10 10 10 10
355.14 358.19 408.37 411.74 400.77 403.81 325.00 321.50 347.60 344.45 338.40 338.62
50.7 72.5 115.8 82.5 90.4 88.6 66.1 72.5 79.7 93.9 57.5 40.3
407.11 404.53 493.47 460.64 430.00 441.61 360.70 356.62 385.70 370.02 401.88 383.26
77.8 93.9 123.3 98.3 70.2 106.4 61.4 50.7 74.5 63.5 69.1 55.1
366.79 362.40 426.52 417.16 397.15 390.19 334.70 326.90 350.90 333.64 359.89 362.26
53.3 53.7 73.3 64.4 58.5 66.7 50.8 52.1 68.2 55.9 56.9 51.6
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
a trend for group×cue×interval interaction: F(4,122)=2.25, p=0.068. In a follow-up exploratory ANOVA, collapsing the data across visual field, the schizophrenia group had significantly (Duncan’s post-hoc test, p<0.05) less costs in the 100-ms interval (mean=−15.52, s.d.=116.9) as compared to the ADHD group (mean=−82.55, s.d.=95.38). The results for the normal group were intermediate, between the results of two other groups (mean=−56.32, s.d.=58.9) ( Fig. 1). The results were the same when analyzing relative measures of cost and benefit. No significant differences were found in the 800-ms condition. As shown in Fig. 1, the effect of inhibition of return seen at the 800-ms interval is striking for all groups. Although the pattern is not the same as true inhibition of return (in which RTs for valid cues are slower than for invalid), there are generally no costs, and appreciably reduced validity effects compared to the 100-ms interval data. A significant correlation between GAS and cost in the right visual field, 100-ms interval (r=0.53, p<0.028) reflects the fact that in the schizophrenia group, the patients with highest GAS score had significantly more cost. When analyzing the cost measure for males only, a significant group effect was found (Fig. 2) [F[2,42]=3.61, p<0.035] due to male subjects with schizophrenia having less cost (mean=2.79, s.d.=65.93) for invalidly cued right visual field targets in the 100-ms interval, as compared to males with ADHD (mean=−63.52, s.d.=86.71) and normal males (mean=−18.10, s.d.=47.61). No significant differences were found
201
Fig. 2. RTs in the Covert Visual Attention task as a function of cue condition, interval and visual field for right-handed male subjects with schizophrenia, ADHD and normal subjects. No: no cue; Va: valid cue; In: invalid cue; L100: left visual field 100-ms interval; R100: right visual field 100-ms interval; L800: left visual field 800-ms interval; R800: right visual field 800-ms interval.
in the left visual field conditions. The results also showed a pattern of reduced cost for invalidly cued left visual targets in the 800 ms interval for ADHD subjects (mean=13.23, s.d.=47.63) compared to the male subjects with schizophrenia (mean=−3.07, s.d.=86.30). The difference was not significant, however. The normals show evidence of an almost ‘true’ inhibition of return in this condition. There was no significant difference between subjects with schizophrenia and normal comparison subjects on the cost measures when analyzing the results for females separately. When including sex as a between-group factor, females had overall slower RTs compared to male subjects [F[1,43]= 4.07, p<0.05]. The ADHD subjects were excluded from this analysis because all were male. There were no significant differences between male and female subjects within each group on any demographic data or clinical ratings.
4. Discussion
Fig. 1. RTs in the Covert Visual Attention task for right handed subjects with schizophrenia, ADHD and normal subjects as a function of cue and interval. 100: 100-ms interval; 800: 800-ms interval. No: no cue; Va: valid cue; In: invalid cue.
The results of the present study do not confirm the hypothesis that young patients with early-onset schizophrenia demonstrate increased costs to invalidly cued targets appearing in the right visual field in the short interval, similar to the acutely ill patients in Posner et al.’s and Maruff et al.’s studies (Posner et al., 1988; Maruff et al., 1995).
202
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
The lack of lateralized slow RT for invalid cues characterizing the young, mostly unmedicated, patients in our sample is similar to the findings for samples of older, medicated chronically ill patients and remitted patients (Carter et al., 1992, 1994; Gold et al., 1992; Moran et al., 1992; Nestor et al., 1992; Strauss et al., 1991, 1992; Liotti et al., 1993). The inconsistencies between studies on this point do not, therefore, seem to be due to chronicity or use of medication, as proposed by Maruff et al. (1995). A statistical trend indicated reduced costs for invalid cues in the short interval in patients with schizophrenia. This supports previous findings (Nestor et al., 1992; Carter et al., 1992, 1994) of reduced costs for invalid cues, particularly for those presented to the right visual field. In the absence of a significant interaction of group×cue×visual field×interval, these differences can only be considered as post hoc in nature. A similar reduction of costs of invalid cueing has been reported in studies of covert visual attention using central directional cues, in patients with Parkinson’s disease ( Wright et al., 1990) and normal subjects given both dopaminergic and noradrenergic antagonists (Clark et al., 1988). It has been proposed that the reduction of costs in all theses cases, as well as in patients with chronic schizophrenia, may depend on the reduction of monoaminergic neurotransmitters involved in the inhibition of unattended spatial locations. Carter et al. (1992) point out that the variability in dopamine activity during the course of the illness, with variation in clinical state or associated with the effects of treatment, may account for the reversed asymmetry in costs, which contrasts the findings of Posner et al. Further, rapid disengagement may be interpreted as a faulty inhibitory processes of activated, but not relevant, associations, perhaps underlying the associative disturbance in schizophrenia (Maher, 1983; Laberge and Brown, 1989; Nestor et al., 1992). The findings in the present study are based on a task that does not discriminate perfectly between automatic and controlled forms of covert visual attention. Nestor et al. (1992) and Carter et al. (1992, 1994) used versions of the task that tap each aspect of covert visual attention separately. They showed reduced costs in right visual field in both versions of the
task. Therefore, our results combined with those of Nestor et al. (1992) and Carter et al. (1992, 1994) point to a genuine reduction of costs of invalid cueing in patients with schizophrenia. This seems to be evident in both chronic adult patients and in adolescence with first-episode schizophrenia. At the long interval, there are generally less costs to invalidily cued targets and appreciably reduced validity effects as compared to the data in the short interval. This suggests that inhibition of return is ‘washing out’ what would be expected to be a large cueing effect from controlled orienting at this long interval. Nestor et al. (1992) and Carter et al. (1992, 1994) showed reduced costs in the right visual field in versions of the task that selectively evaluated controlled shifts of attention. This tendency was observed most clearly for normal comparison subjects in our study. Patients with schizophrenia in the present study did not differ from the normal comparison group on overall RT. This is in contrast to a generally slow RT that has been found to characterize patients with schizophrenia (Nuechterlein, 1977). The subjects with schizophrenia in the present study were significantly younger than those in other studies of covert visual attention in schizophrenia, and most of the patients were neuroleptic-naı¨ve. This may indicate that impairments in overall RT in covert visual attention are not present in the very early phase of a schizophrenic illness, but are secondary to neuroleptic medication, hospitalization or the disease process itself. Our RT findings are also consistent with the results from Potkin et al.’s study (Potkin et al., 1989) in which first-episode patients did not differ from normal controls in RTs on the Covert Visual Attention task. Further, Potkin et al. (1989) found that patients with chronic schizophrenia had a significantly slower RT on the Covert Visual Attention task than firstepisode patients, consistent with a progressive deterioration of the non-lateralized component of RT during the course of schizophrenia. In addition, RT on a visual–spatial processing increases with age (Robinson and Kertzman, 1990). The adolescents in the present study were tested within a multitask neuropsychological battery, and the results showed that they did not differ significantly in RT on a span of apprehension task (Rund
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
et al., 1998). However, they responded significantly more slowly compared to normals on tests of psychomotor tempo. Thus, it is possible that when more complex levels of reaction-time tasks are introduced, adolescents with schizophrenia will respond significantly more slowly than normals. Another possible reason for our results of no significant differences between groups on overall RT is that the high variability in RT in the schizophrenia group might have obscured a difference in RT between the groups. However, using the median value in the analyses of overall RT and excluding outliers in both groups did not change the results in any substantial way. It can be argued that it is not correct to speculate about group differences in overall RT for a task that is not developed to measure overall RT per se. Males with schizophrenia showed lower costs in the right visual field in comparison with normal males. The findings partially support the formulation of Posner et al. (1988) that right visual field cues less efficiently summon attention as compared to left visual field cues in patients with schizophrenia. This is also consistent with a left hemisphere dysfunction. Males with ADHD showed the opposite pattern of laterality to that found for the males with schizophrenia: they showed no decreased costs for invalidly cued right-field targets in the short interval, but decreased costs for invalidly cued left-field targets in the long interval. This pattern of performance is consistent with the results of both Swanson et al. (1990, 1991) and Carter et al. (1995). Further, this suggest some specificity for the schizophrenia finding, as well as reliability for the Posner task. Data from other neuropsychological tests used in the broader multitask battery showed that patients with schizophrenia performed poorly on measures of executive functions, verbal and visual memory and early information processing (Rund et al., 1996; Øie and Rund, 1998). However, adolescents with schizophrenia did not perform poorly on a degraded stimulus continuous performance test, supposed to measure sustained attention. Further, they did not show any impairments in performance on a dichotic listening test designed to measure auditory selective attention and laterality (Øie et al., 1998; Rund et al., 1998). These
203
results indicate that the patients with schizophrenia were characterized by severe cognitive impairments, but that the dysfunction in covert visual attention does not represent a generalized attentional dysfunction as performances on tests of selective and sustained attention were not impaired. The influence of sex on measures of RT is unclear. Females have generally slower RTs than males (Coles et al., 1975), but this is shown to be restricted to movement times and not to decision times (Lynn and Ja-Song, 1993). In our study, female subjects had generally slower RTs than male subjects, but the covert attention task is not designed to dissociate the two components of RT. There is a growing set of data indicating that sex hormones influence the level of arousal and thus measures of RT (Broverman et al., 1964) and the development of cerebral lateralization of function (Grimshaw et al., 1995), with greater hemispherical specialization in males (Hiscock et al., 1994; Mead and Hampson, 1996). The female subjects in our study were not asked to report their menstrual phases, and we cannot correlate field differences with hormonal status. However, our findings of significant differences in cost between the male groups, but not between female groups, underline that the sex of a subject may be a confounding factor in RT studies. In summary, our results do not support the hypothesis of a left hemisphere lateralized slow RT in disengagement in covert visual attention in young patients with schizophrenia. In contrast, the results support a hypothesis of abnormally rapid disengagement in male adolescents with schizophrenia. Such an abnormality has also been found in adults with chronic schizophrenia. Whether this holds true for both sexes of adolescents with schizophrenia or is restricted to male subjects cannot be answered with certainty due to the small number of females with schizophrenia in our sample. Our findings indicate, however, that there are some general sex differences and some specific sex differences related to covert visual attention in adolescents with schizophrenia. Acknowledgment This study was supported by grants from the Norwegian Research Council (No. 377.94/013)
204
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205
and from Haldis and Josef Andresen’s Foundation. The authors would like to thank Michael Posner, PhD, for valuable comments on a previous version of this manuscript.
References Achenbach, T.M., 1991. Manual for the Child Behavior Checklist/4-18 and 1991 Profile. University of Vermont, Burlington, VT. American Psychiatric Association, 1987. Diagnostic and Statistical Manual of Mental Disorders, 3rd ed., revised. American Psychiatric Association, Washington, DC. Broverman, D.M., Broverman, I.K., Vogel, W., Palmer, R., Klaiber, E.L., 1964. Cognitive style and physical development. Child Dev. 35, 1343–1359. Bustillo, J.R., Thaker, G., Buchanan, R.W., Moran, M., Kirkpatrick, B., Carpenter, W.T., 1997. Visual informationprocessing impairments in deficit and nondeficit schizophrenia. Am. J. Psychiatry 154, 647–654. Carter, C.S., Robertson, L.C., Chaderjian, M.R., Celaya, L.J., Nordahl, T.E., 1992. Attentional asymmetry in schizophrenia: Controlled and automatic processes. Biol. Psychiatry 31, 909–918. Carter, C.S., Robertson, L.C., Chaderjian, M.R., O’ShoraCelaya, L., Nordahl, T.E., 1994. Attentional asymmetry in schizophrenia: The role of illness subtype and symptomatology. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 18, 661–683. Carter, C.S., Krener, P., Chaderjian, M., Northcutt, C., Wolfe, V., 1995. Asymmetrical visual–spatial attentional performance in ADHD: Evidence for a right hemispheric deficit. Biol. Psychiatry 37, 789–797. Clark, C.R., Geffen, G.M., Geffen, L.B., 1988. Catecholamines and the covert orienting of attention in humans. Neuropsychologia 27, 1331–1339. Coles, M.H., Porges, S.W., Duncan-Johnson, C.C., 1975. Sex differences in performance and associated cardiac activity during a reaction time task. Physiol. Psychol. 3, 141–143. Eimer, M., 1993. Spatial cueing, sensory gating and selective response preparation: An ERP study on visuo-spatial orienting. Electroencephalogr. Clin. Neurophysiol. 88, 408–420. Endicott, J., Spitzer, R.L., Fleiss, J., Cohen, J., 1976. The Global Assessment Scale: A procedure for measuring overall severity of psychiatric disturbance. Arch. Gen. Psychiatry 33, 766–771. Gold, J.M., Randolph, C., Coppola, R., Carpenter, J.C., Goldberg, T.E., Weinberger, D.R., 1992. Visual orienting in schizophrenia. Schizophr. Res. 7, 203–209. Grimshaw, G.M., Bryden, M.P., Finegan, J.K., 1995. Relations between prenatal testosterone and cerebral lateralization in children. Neuropsychology 9, 68–79. Hiscock, M., Inch, R., Jacek, C., Hiscock-Kalil, C., Kalil, K.M., 1994. Is there a sex difference in human laterality? I.
An exhaustive survey of auditory laterality studies from six neuropsychology journals. J. Clin. Exp. Neuropsychol. 16, 423–435. Hoff, A.L., Riordan, H., O’Donell, D.W., Morris, L., DeLisi, L., 1992. Neuropsychological functioning of first-episode schizophreniform patients. Am. J. Psychiatry 149, 898–903. Jonides, J., Mack, R., 1984. On the cost and benefit of cost and benefit. Psychol. Bull. 1, 29–44. Laberge, D.L., Brown, V., 1989. Theory of attentional operations in shape identification. Psychol. Rev. 96, 101–124. Lewine, R., Straus, J., Gift, E., 1981. Sex differences in age at first hospital admission for schizophrenia: fact or artifact. Am. J. Psychiatry 138, 440–444. Lewine, R.R.J., Walker, E.F., Shurett, R., Caudle, J., Haden, C., 1996. Sex differences in neuropsychological functioning among schizophrenic patients. Am. J. Psychiatry 153, 1178–1184. Liotti, M., Dazzi, S., Umlita, C., 1993. Deficits of the automatic orienting of attention in psychiatric patients. J. Psychiatr. Res. 27, 119–130. Lukoff, D., Nuechterlein, K.H., Ventura, J., 1986. Appendix A: Manual for Expanded Brief Psychiatric Rating Scale (BPRS ). Schizophr. Bull. 12, 594–602. Lynn, R., Ja-Song, M., 1993. Sex differences in reaction times, decision times, and movement times in British and Korean children. J. Gen. Psychol. 154, 209–2130. Maher, B.A., 1983. A tentative theory of schizophrenic utterance. In: Maher, B.A., Maher, W.B. (Eds.), Progress in Experimental Personality Research. Psychopathology Academic Press, New York, pp. 1–52. Maruff, P., Hay, D., Malone, V., Currie, J., 1995. Asymmetries in the covert orienting of visual spatial attention in schizophrenia. Neuropsychologia 33, 1205–1223. McGlashan, T., Bardenstein, K., 1990. Gender difference in affective, schizoaffective, and schizophrenia disorder. Schizophr. Bull. 16, 319–330. Mead, L.A., Hampson, E., 1996. Asymmetric effects of ovarian hormones on hemispheric activity: Evidence from dichotic and tachistoscopic tests. Neuropsychology 10, 578–587. Moran, M.J., Thaker, G.K., Smith, D., Cassady, S., LayneGedge, J., 1992. Shifts in covert visual attention in schizophrenic patients and normal controls. Biol. Psychiatry 32, 617–620. Muller, H.J., Rabbit, P., 1989. Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J. Exp. Psychol. Hum. Percept. Perform. 15, 315–330. Nestor, P.G., Faux, S.F., McCarley, R.W., Penhune, V., Shenton, M., Pollak, S., 1992. Attentional cues in chronic schizophrenia: Abnormal disengagement of attention. J. Abnorm. Psychol. 4, 682–689. Nuechterlein, K.H., 1977. Reaction time and attention in schizophrenia: A critical evaluation of the data and the theories. Schizophr. Bull. 3, 373–428. Posner, M.I., 1980. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25. Posner, M.I., Snyder, C.R.R., Davidson, B.J., 1980. Attention
M. Øie et al. / Schizophrenia Research 34 (1998) 195–205 and the detection of signals. J. Exp. Psychol.: Gen. 109, 160–174. Posner, M.I., Cohen, Y., 1984. Components of visual orienting. In: Bouma, H., Bouwhuis, D.G. ( Eds.), Attention and Performance. Erlbaum, Hillsdale, NJ, pp. 531–556. Posner, M.I., Walker, J.A., Friedrich, F.J., Rafal, R.D., 1984. Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863–1874. Posner, M.I., Inhoff, A.W., Friedrich, J.F., Cohen, A., 1987. Isolating attention systems: A cognitive–anatomical analysis. Psychobiology 15, 107–121. Posner, M.I., Early, T.S., Reiman, E.M., Pardo, P.J., Dhawan, M., 1988. Asymmetries in hemispheric control of attention in schizophrenia. Arch. Gen. Psychiatry 45, 814–821. Potkin, S.G., Swanson, J.M., Urbanchek, M., Carreon, D., Bravo, G., 1989. Lateralized deficits in covert shifts of visual attention in chronic and never-medicated schizophrenics compared to normal controls. Schizophr. Res. 2, 95 Rafal, R.D., Calabresi, P.A., Brennan, C.W., Sciolto, T.K., 1989. Saccade preparation inhibits reorienting to recently attended locations. J. Exp. Psychol. 15, 673–685. Robertson, L.C., Lamb, M.R., Knight, R.T., 1988. Effects of lesions of temporo-parietal junction on perceptual and attentional processing in humans. J. Neurosci. 10, 3757–3769. Robinson, D.L., Kertzman, C., 1990. Visuospatial attention: effects of age, gender, and spatial reference. Neuropsychologia 28, 291–301. Rund, R., Øie, M., Sundet, K., 1996. Backward-masking in adolescents with schizophrenic disorders or Attention Deficit Hyperactivity Disorder. Am. J. Psychiatry 153, 1154–1157. Rund, R., Øie, M., Zeiner., P., Sundet, K., 1998. Span of apprehension in adolescents with schizophrenia or ADHD. Submitted. Sereno, A.B., Holzman, P.S., 1996. Spatial selective attention in schizophrenic, affective disorder, and normal subjects. Schizophr. Res. 20, 33–50. Strauss, M.E., Novakovic, T., Tien, A.Y., Bylsma, F., Pearlson,
205
G.D., 1991. Disengagement of attention in schizophrenia. Psychiatry Res. 37, 139–146. Strauss, M.E., Alphs, L., Boekamp, J., 1992. Disengagement of attention in chronic schizophrenia. Psychiatry Res. 43, 87–92. Swanson, J.M., Shea, C., McBurnett, K., Potkin, S.G., Fiore, C., Crinella, F., 1990. Attention and hyperactivity. In: Enns, J.T. ( Ed.), The Development of Attention: Research and Theory. Elsevier Science, Amsterdam, pp. 383–403. Swanson, J.M., Posner, M.I., Potkin, S., Bonforte, S., Youpa, D., Fiore, C., Cantwell, M.D., Crinella, F., 1991. Activating tasks for the study of visual–spatial attention in ADHD children: a cognitive anatomic approach. J. Child. Neurol. Suppl. 6, 119–127. Ventura, A.J., Nuechterlein, K.H., Subotnik, K., 1995. Symptom dimension in recent-oncet schizophrenia: The 24-item BPRS. Paper presented at the Fifth Bi-Annual International Congress on Schizophrenia Research, Warm Springs, VA, 8–12 April. Watt, N.F., 1978. Patterns of childhood social development in adult schizophrenia. Arch. Gen. Psychiatry 35, 160–165. Wechsler, D., 1974. The Wechsler Intelligence Scale for Children—Revised. The Psychological Corporation, New York. Wender, P.H., Wood, D.R., Reimherr, F.W., 1985. Pharmacological treatment of Attention Deficit Disorder, Residual Type (ADD, RT, ‘Minimal Brain Dysfunction’, ‘Hyperactivity’) in adults. Psychopharmacol. Bull. 21, 222–231. Wright, M.J., Burns, R.J., Geffen, G.M., Geffen, L.B., 1990. Covert orienting of visual attention in Parkinson’s disease: an impairment in the maintenance of attention. Neuropsychologia 28, 151–159. Øie, M., Rund, B.R., 1998. Neuropsychological deficits in adolescent-onset schizophrenia. Submitted. Øie, M., Rund, B.R., Sundet, K., Bryhn, G., 1998. Auditory laterality and selective attention: normal performance in patients with early-onset schizophrenia. Schizophr. Bull., in press.