Abnormal processing of irrelevant information in chronic schizophrenia: Selective enhancement of stroop facilitation

Psychiatry Research, 4 I : I 37- I46 Elsevier

137

Abnormal Processing of Irrelevant Information in Chronic Schizophrenia: Selective Enhancement of Stroop Facilitation Cameron

S. Carter, Lynn C. Robertson,

Received September January 19, 1992.

23. 1991; revised

and Thomas E. Nordahl

version

received

December

16. 1991; accepted

Abstract. Thirteen medication-free chronic schizophrenic patients and 11 normal control subjects were administered a trial by trial version of the Stroop Color Naming Task which evaluated separately the processes of interference and facilitation. There was no difference between the groups in the amount of interference to naming the colors of color-incongruent words. However, patients with schizophrenia showed significantly greater speed in naming the colors of color-congruent words when compared with control subjects. Thus, facilitation on the Stroop Task appears to be selectively enhanced in schizophrenia. Similar findings have been recently observed in patients with Parkinson’s disease. This result may indicate a selective disruption of an automatic inhibitory process in this patient group and is consistent with the hypothesis that a deficit in mesocortical dopamine projections to the frontal cortex underlies some of the cognitive deficits of chronic schizophrenia. Key Words. Attention, lobe.

cognition,

Stroop

Task, information

processing,

frontal

On the basis of their findings in regional cerebral blood flow activation studies using an automated version of the Wisconsin Card Sorting Task, Weinberger et al. (1988) have proposed that reduction in mesolimbic dopamine projections to the dorsolateral prefrontal cortex accounts for many of the cognitive deficits seen in chronic schizophrenia. In a recent review of the role of frontal lobe pathology in schizophrenia, Robbins (1990) stressed the need for further studies in schizophrenia to identify other cognitive tasks associated with the functioning of the frontal lobe which might provide converging evidence for this hypothesis. The Stroop Color Naming Task @troop, 1935) is one of the most thoroughly investigated tasks in cognitive science (see Macleod [ 19911 for an exhaustive review). The traditional version of the task compares the speed of naming the color of ink in which a word with a semantic meaning incongruous to its color is printed (e.g., the word “redl’printed in blue) to the time taken to name colored patches or color words

Cameron S. Carter, M.B.B.S., is Assistant Professor of Psychiatry; Lynn C. Robertson, Ph.D., is Assistant Professor of Psychiatry and Neurology; and Thomas E. Nordahl, M.D., is Assistant Professor of Psychiatry in the School of Medicine, University of California at Davis. (Reprint requests to Dr. C.S. Carter, Dept. of Psychiatry, University of California at Davis Medical Center, 4430 V St., Sacramento, CA 95817, USA.) 0161781/92/$05.00

@ 1992 Elsevier Scientific

Publishers

Ireland

Ltd.

138 printed in black and white. Variations of the task relate the speed of naming the ink color of colored words whose meanings are not color related (e.g., “dog” printed in red). While the precise nature of this task remains the subject of much discussion, its essential feature is that subjects cannot completely suppress the semantic processing of color-incongruent words, with the result that color-naming times are longer for this condition. The slowing of color naming is referred to as Stroop interference. Stroop interference is seen in normal subjects and has been shown to be increased in subjects with lesions in the frontal lobes (Perret, 1974; Golden, 1976). Studies in schizophrenia have shown prolonged color naming of incongruent color word lists (Abramczyk et al., 1983; Wysocki and Sweet, 1985; Everett et al., 1989). It is unclear, however, whether this actually represents increased interference in these patients, since response times for neutral stimuli are also increased, and it is possible that this slowing represents a more general poverty of responding by these patients (Chapman and Chapman, 1978). Everett et al. (1989) have shown that there is less interference in schizophrenic patients for short lists of stimuli than for long lists, suggesting that a vulnerability to fatigue on this demanding cognitive task may account for the greater Stroop interference in these patients. More recent investigations of the Stroop phenomenon have used single word (trial by trial) presentations of stimuli on a visual display unit or tachistoscope, a modification that has increased the sensitivity of the task. This advance also allowed the role of many stimulus parameters to be explored, with the result that variations of the Stroop paradigm have been used to identify and explore a variety of cognitive mechanisms (Logan et al., 1984; La Heij et al., 1985; Neil1 and Westberry, 1987). Studies using this approach have shown that in addition to the robust interference seen with color-incongruent stimuli, a smaller but reliable speeding of color naming is seen for color words presented in their own color (e.g., the word “red” presented in red). This effect is referred to as,facilitation (Macleod, 1991). Stroop effects have been widely viewed as automatic-that is, not subject to strategic control by the subject (Posner and Snyder, 1975). Several recent studies, however, have suggested that this is not always the case. Using a spatial analogue of the Stroop Task, in which response conflict was between word meaning (“above” or “below”) and spatial location of the verbal stimulus, Logan and Zbrodoff (1979; Logan, 1980) showed that the interference and facilitation effects of congruent and incongruent stimuli could be reversed by manipulating expectancies via the proportion of conflicting trials. In a later replication using a color conflict task with vocal responding (instead of a key press as in their earlier experiments), this effect appeared to be predominantly a reduction in interference (Logan et al., 1984). However, since these authors did not use any neutral (noncolor) words, a precise comparison of the impact of greater expectancy on interference and facilitation components cannot be made from their data. More recently, Tzelgov et al. (1990) have shown that while subjects can exercise some cognitive control and reduce Stroop interference under some circumstances, Stroop facilitation proceeds automatically, independent of cognitive control, under the same circumstances. These investigators presented subjects with blocks of color-naming trials in which the proportion of color words (incongruent and congruent) to noncolor words was

139 varied. In doing so, they manipulated the likely expectancy that subjects would have for neutral, congruent, and incongruent stimuli. These investigators found that interference effects (color-naming times for incongruent stimuli) were greatest in blocks of trials in which the proportion of color words (and hence expectancy for these stimuli) was low. However, varying the proportion of color words had no effect on facilitation (color-naming times for congruent vs. neutral stimuli). This suggests that in the Color Conflict Stroop Task interference and facilitation are distinct, dissociable operations and that the interference effect is subject to a significant degree of cognitive control, whereas facilitation may reflect a more automatic process. In view of the strong association between the Stroop Task and frontal lobe functioning and because previous reports using traditional versions of this task in schizophrenia have failed to distinguish between general slowing and increased interference effects, we sought to investigate frontally mediated cognition in patients with chronic schizophrenia using a more rigorous trial by trial version of the task. By using a trial by trial version of the Color Conflict Stroop Task, we could also assess both facilitation and interference, Since previous studies have suggested a loss of cognitive control in schizophrenia (Callaway and Naghdi, 1982), we hypothesized that the interference parameter would be abnormal in these patients. The demonstration of a dissociation between the interference and facilitation measures would argue against the explanation that the findings of earlier studies reflected a general slowness of processing in schizophrenic patients and suggest instead a discrete cognitive abnormality associated with frontal lobe pathology. Such a finding would also be further evidence that interference and facilitation are distinct cognitive operations and would suggest that they are served by separate neural systems.

Methods Subjects. The schizophrenic group consisted of 13 outpatient participants in an investigational drug study in the Department of Psychiatry at the University of California at Davis Medical Center. All met DSM-III-R criteria for chronic schizophrenia (American Psychiatric Association, 1987) on the Structured Clinical Interview for DSM-III-R (Spitzer and Williams, 1987). All had been withdrawn from antipsychotic medication for at least 2 weeks before testing. Two patients had been treated previously with haloperidol decanoate and had received their last injections 9 and 10 weeks before testing. Some patients had continued to use anticholinergic medications until 4 days before testing, and six patients had used short-acting benzodiazepines, chloral hydrate, or diphenhydramine intermittently during their neuroleptic-free washout period. These subjects took no medications for 24 hours before testing. Only patients with negative urine drug screens were used as subjects in the study. All patients were chronic and had been ill for a mean period of 10.07 (SD = 6.13) years. They scored in the mild to moderate range on core symptoms of the Brief Psychiatric Rating Scale (Kane et al., 1988). Control subjects were recruited by advertisement and had no lifetime history of mental disorder and no first degree family history of psychotic disorder. Eleven control subjects were matched with patients for age (schizophrenic patients: mean = 32.5 years, SD = 4.3 years; control subjects: mean = 31 years, SD = 6.1 years; t = 0.72, d’= 22, p = 0.48), gender (schizophrenic patients: IO males, 3 females; control subjects: 9 males, 2 females; x2 = 0.087, df = 1, p = 0.77) and years of parent’s education (to match approximately for socioeconomic status; patients: mean = 13.4, SD = 2.0; control subjects: mean = 14.5, SD = 2.1; t = -1.27, df = 22, p = 0.21). There was one left-handed subject in

140 each of the two groups. All subjects had normal or near normal vision by Snellon the day of testing. Both patients and controls were paid for their participation.

testing on

Stroop Task. Stimuli were presented on an Everex color monitor with the presentation of stimuli controlled by an Everex 386si microcomputer. Response timing was to I-msec resolution and was controlled by the 8253 chip. Stimulus timing was tied to the vertical sync pulse. Stimuli were presented in one of four colors: red, blue, green, or purple. The incongruent stimuli consisted of each of the four color names presented printed in one of the three remaining colors. The congruent stimuli consisted of one of the four color names presented in its own color. Neutral stimuli consisted of one of four color unrelated words (dog, bear, tiger, or monkey) printed in one of the four colors. Neutral words were selected to match the four color words in length and frequency. They were chosen from a single semantic category to eliminate semantic confounds. Subjects’ heads were immobilized in a chin-rest 540 mm from the monitor screen through-

out the procedure. Their verbal response latencies were measured with a Gerbrand’s voiceoperated relay interfaced with the computer and monitored through the game port. Subjects were given standardized instructions to ignore the meaning of each word and to name its color as quickly and accurately

as possible

as each stimulus

was presented

on the visual display unit. in the center of the screen. The subject’s response was registered via a switch triggered by the voice-operated relay (and recorded by the computer in msec) and terminated the presentation of the stimulus. This was followed by the experimenter response which keyed in the first letter of the subject’s response, providing a record of the accuracy of each response. This experimenter response initiated the subsequent trial. After 24 practice trials, subjects were presented with a block of 96 experimental trials in which 24 trials (25%) were incongruent, 24 trials (25%) were congruent, and 48 (507)o were neutral. Incongruent, congruent, and neutral stimuli were distributed randomly throughout the block of trials.

Each trial began with a blank screen for 500 msec after which the stimulus was presented

Analysis. Median reaction times for correct responses for each task condition were subjected to an analysis of variance for mixed design, with one between-subjects factor (schizophrenia vs. control) and one within-subjects factor (word type: congruent, incongruent, or neutral). The possibility of a speed-accuracy tradeoff’s biasing the results was evaluated by performing a correlation analysis between subject’s mean reaction times and the number of errors made by each subject.

Results Patients made errors on 7.7% of trials, while controls made errors on 3.OYo of trials. There was no evidence of a speed-accuracy tradeoff. In fact, there was a strong positive correlation between reaction times and errors (r = 0.615, p < 0.0001). Subjects with faster reaction times made fewer errors than those with longer reaction times. Table 1 displays the median reaction times of each group for each word type. The analysis revealed that schizophrenic patients’ responses were slower than controls’ (F= 5.97; df= 1, 22; p < 0.02), word type influenced response time (F= 88.6; df’= 2, 44; p < O.OOOl), and the influence of word type was different in schizophrenic patients than in controls, as reflected in a significant word type X group interaction (F = 4.55; c#‘= 2, 44; p < 0.02). Planned comparisons to evaluate interference effects compared schizophrenic patients with control subjects for incongruent and neutral words only. Interference was 229 msec on average for schizophrenic patients and 188 msec for controls, and

141

Table 1. Mean reaction times (msec) for color naming by word type: Schizophrenic patients vs. controls Schizophrenics (n = 13) Mean

Word type Neutral

incongruent

Congruent

Controls (n= 11)

SD

Mean

SD

890

260.7

692.7

83.3

1119.3

281.2

880

139.6

740.8

158.8

643

78.7

there was no group X word type interaction (F = 1.11; df = 1, 22; NS). The facilitation effect was evaluated by a planned comparison comparing schizophrenic patients with controls for congruent and neutral words only. Facilitation was 150 msec on average for schizophrenic patients and 49 msec for controls, as reflected in an overall group X word type interaction (F= 4.35; df = 1,22;p < 0.05). As shown in Fig. 1, patients with schizophrenia showed more facilitation than controls but equal amounts of interference. The overall increase in reaction time for schizophrenic patients could have produced the appearance of increased facilitation (i.e., the small amount of facilitation in normal subjects may have been a floor effect). However, note that the overall increase in reaction time for schizophrenic subjects did not change the amount of interference when compared with that observed in the controls, and therefore the rate of processing did not change. To test more rigorously the contribution of longer reaction time, we selected schizophrenic subjects and controls (n = 7 in each group) who had reaction times for neutral stimuli in the same range (schizophrenic patients: mean = 717 msec, SD = 50 msec; controls: mean = 726

Fig. 1. Comparison of schizophrenic patients and normal controls on interference and facilitation scores 240 220 200

0

Control

n= 11

180 4

160

g

140

$

120

2

100

y

a0 60 40 20 0 Interference l

p<

Facilitation

.05

Scores of interference = mean reaction time for incongruent stimuli minus mean reaction time for neutral stimuli. Scores of facilitation = mean reaction time for congruent stimuli minus mean reaction time for neutral stimuli.

142 msec; SD = 70 msec). Statistical power was low for this comparison, and significant differences were not found. However, facilitation still tended to be longer for schizophrenic subjects than for controls (F= 2.50; df= 1, 12; p = 0.13). Whereas the facilitation effect for these seven controls was 57 msec, it was 93 msec for the seven patients with schizophrenia. Interference showed little change: 222 msec for controls and 213 msec for schizophrenic patients. To evaluate further the possibility of a floor effect that limited facilitation in normal subjects, we performed a correlational analysis between the amount of facilitation (congruent minus neutral reaction times) and the overall reaction time for each subject (r = 0.08, df= 9, NS). The range of reaction times for the normal subjects was 610 to 897 msec, and the range of facilitation scores was -14 to 139 msec. These analyses demonstrate that there was an almost zero correlation between overall reaction time and the amount of facilitation, a finding inconsistent with the concept of a floor effect limiting facilitation in normal subjects.

Discussion Although the schizophrenic group was generally slower than the control group, the dissociation of performance on the facilitation and interference components of the Stroop Task argues for the presence of a specific cognitive abnormality being measured by this task. Furthermore, this abnormality is in the more automatic facilitation process and does not affect the more controlled interference effect, which appears intact. Patients with chronic schizophrenia show an enhanced facilitation of color naming of color-congruent words. An alternative to this conclusion is that the difference between the groups reflects a floor effect in the control group’s facilitation performance instead of an increase in facilitation in the generally slower schizophrenic group. However, in the current study, the subgroup of schizophrenic patients with faster reaction times still showed a trend toward greater facilitation than control subjects. Furthermore, no correlation was found between the facilitation scores and overall reaction times in our normal subjects, again making a floor effect limiting facilitation in this group unlikely. Although we cannot rule out entirely the possibility that a floor effect accounted for the group differences in facilitation in the present study, consideration of the findings of Tzelgov et al. (1990) also suggests that facilitation in normal subjects is not subject to a floor effect. The amount of interference seen in our control subjects was similar to that found by Tzelgov et al. (1990) in normal subjects (49 msec in the present study and 59 msec in the latter study for the 50% neutral condition). For Tzelgov et al., this value did not change whether the probability of a neutral word was 7570, 507& or 25$?&while the interference effects varied systematically. The 75yC neutral condition produced more interference, while the 25% condition produced less interference than the 50% condition. In other words, subjects adopted the strictest criterion in the 25% neutral condition because there was a greater probability that an incongruent stimulus would appear and that inhibition of word reading would be needed. If facilitation were affected by control, this inhibition should also decrease the advantages that congruent stimuli have. However. Tzeglov et al. found

143 no difference over probability schedules on facilitation. If a floor effect had been operating in these normal subjects, the facilitation would have been expected to be the same for the 75% neutral condition or even for the 50% neutral condition, but by the 25% neutral condition we would have expected some reduction in facilitation. It could be argued that only a very small proportion of neutral stimuli need be presented before facilitation is diminished, but this explanation seems implausible. A replication of the study of Tzeglov et al. in which the proportion of neutral stimuli was varied in 10% increments would shed further light on this question. However, the findings of their study would also argue against a floor effect limiting Stroop facilitation in normal subjects. Our finding of a normal amount of Stroop interference in our group of patients with chronic schizophrenia suggests that the increased interference effect seen in the studies of Abramczyk et al. (1983) Wysocki and Sweet (1985), and Everett et al. (1989) may have been due to a more general processing deficit rather than an increased level of interference, per se. This effect could either be a general slowing (our schizophrenic patients were slower overall than controls) or reflect a vulnerability of control processes relevant to the interference effect to fatigue. Everett et al. (1989) showed that patients with schizophrenia showed less interference with a short list of incongruent stimuli than with a long one and suggested that findings of increased interference in patients with schizophrenia might reflect increased fatigability of control processes in these patients. A crucial difference between the current study and those above is the trial by trial design and the fact that only 25% of the stimuli were conflict stimuli, whereas earlier studies used cards with lists of color words on which 100% of the stimuli were color-incongruent. As discussed above, Tzeglov et al. (1990) have shown that with increasing frequency of incongruent stimuli normal subjects are able, presumably on the basis of expectancy, to reduce the interference effect. Experiments in which 100% of a block of stimuli were incongruent would constitute an optimal condition for reducing interference by exercising cognitive control. The current study, with the trial by trial design and relatively small percentage of incongruent stimuli, would not tap these control processes to the same degree. The possibility that Stroop interference might be increased in schizophrenia under conditions that demand sustained cognitive control could be evaluated by presenting different blocks of color-naming trials to schizophrenic subjects and normal subjects in which the percentage of incongruent stimuli varied from block to block. Henik et al. (1992) recently observed a selective increase in facilitation in patients with Parkinson’s disease on a version of the Stroop Task that used the same parameters and stimuli as in the current study. The findings presented here, together with those of Henik et al., provide further support for the hypothesis of Weinberger et al. (1988) that cognitive deficits in schizophrenia are the consequence of diminished dopamine activity in the mesocortical projections of the ventral striatum. Weinberger et al. (1988) have reported a negative correlation between the number of perseverative errors made by subjects during the Wisconsin Card Sorting Task and the increase in regional cerebral blood flow in the dorsolateral prefrontal cortex during the performance of the task in patients with schizophrenia and in Parkinson’s

144 disease, but not in normal control subjects. Weinberger et al. have argued that this reflects a relative deafferentation of mesocortical dopamine projections to the dorsolateral prefrontal cortex in both illnesses. Perret (1974) has shown a strong association between lesions in the frontal lobe (particularly the left frontal lobe) and disruption of performance on the classical Stroop Task. Little is known about the localization of the facilitation and interference components. In a recent study of patients with obsessive-compulsive disorder (Martinot et al., 1990) however, the metabolic rate of the lateral prefrontal cortex correlated negatively with performance on the classical version of the Stroop Task. Using a subtraction approach in an activation study in which subjects first completed congruent trials followed by incongruent trials, Pardo et al. (1990) found the anterior cingulate area to be the most robustly responsive brain region identified by positron emission tomography. Their finding suggests that the anterior cingulate is active during interference trials, but not during facilitation trials. Posner et al. (19886) have hypothesized the existence of an anterior attentional system closely tied to systems involved in the processing of language. The lateral frontal cortex is proposed to serve the more automatic process of activation of semantic networks while parts of the cingulate cortex are thought to be involved in the controlled selection of relevant responses. The findings of Pardo et al. (1990) are quite consistent with this hypothesis. Posner and colleagues have also proposed that a paucity of dopaminergic afferent input affecting the anterior attentional system underlies abnormal performance on the covert orienting of visual spatial attention that they reported to be present in a group of patients with schizophrenia (Posner et al., 1988~; Early et al., 1989). Manschreck et al. (1988) and Kwapil et al. (1990) have reported that some patients with schizophrenia have increased priming of word recognition when the priming stimulus is semantically related to the target. It has been suggested that this represents a loss of inhibitory activity within the semantic network (Kwapil et al., 1990). The increased facilitation effect seen in the current study may represent an analogous finding to the increased semantic priming effect reported above. Other authors have attempted to relate priming phenomena to Stroop phenomena (Logan 1980; La Heij et al., 1985). La Heij et al. (1985) were able to show that conflicting stimuli could under some conditions produce Stroop-like interference and under other situations produce priming-like speeded responding. In the study of La Heij et al., however, conflict was purely semantic; no color conflict was involved and relevance to the classical color-conflict Stroop Task as used in the current study is unclear. A possible relationship between priming effects in the lexical decision task and facilitation by congruent stimuli in the Stroop Task is suggested by the findings that both of these measures appear to be abnormal in schizophrenia. Conclusions about the specificity of such a relationship must await the results of further studies of semantic priming and Stroop phenomena in schizophrenic patients. Such a relationship is, however, in line with the theoretical model of Posner and his colleagues outlined above. Finally, if, as Posner et al. (1988h) have proposed, semantic activation occurs in the lateral prefrontal cortex, then loss of dopaminergic afferents to this region, as has been proposed by Weinberger et al. (1988) to occur in schizophrenia, could accoum fo: this effec’.

145 In summary, the results of this study suggest that the performance of medicationfree patients with chronic schizophrenia on the Stroop Task is characterized by a general slowing of responses and a specific enhancement of the facilitation of color naming by color-congruent stimuli. This finding supports a converging body of evidence from neuropsychological, cognitive, and imaging studies that schizophrenic patients show pathology in the frontal lobe. In association with the recent observation of increased Stroop facilitation using the same task parameters in Parkinson’s disease, our finding is consistent with the hypothesis that deafferentation of mesocortical dopamine projections to the frontal cortex may underlie some of the cognitive abnormalities in patients with chronic schizophrenia. Acknowledgments. We are grateful to Marc R. Chaderjian, Linda J. Celaya, and Anne Cummings for assistance in collecting the data presented in this article. We also thank an anonymous reviewer, who suggested the last analysis presented in the results section. Our study was supported in part by VA Medical Research Council award AA06637 to Lynn C. Robertson and N.I.H. Grant MH-46990 to Thomas E. Nordahl.

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