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Schizophrenia Research 133 (2011) 172–181

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Schizophrenia Research
journal homepage: www.elsevier.com/locate/schres

Review

Impaired cognitive inhibition in schizophrenia: A meta-analysis of the Stroop


interference effect
René Westerhausen a, b,⁎, Kristiina Kompus a, Kenneth Hugdahl a, b
a
Department of Biological and Medical Psychology, University of Bergen, Jonas Lies vei 91, N-5009 Bergen, Norway
b
Division of Psychiatry, Haukeland University Hospital, N-5009 Bergen, Norway

a r t i c l e i n f o a b s t r a c t

Article history: Schizophrenia has been consistently shown to be associated with impairment in executive functioning. How-
Received 27 April 2011 ever, although frequently treated as such, the term executive functioning does not refer to a unitary cognitive
Received in revised form 9 August 2011 function; it rather represents a set of basic, lower-level cognitive sub-components, e.g. updating, shifting, and
Accepted 29 August 2011
cognitive inhibition. This specification into sub-components allows for a further differentiation of the execu-
Available online 19 September 2011
tive deficits found in schizophrenia. Focusing on the sub-component of cognitive inhibition, we here present
Keywords:
a meta-analysis of interference effect as assessed with the Stroop Color-Word Interference paradigm. Includ-
Schizophrenia ing the results of 36 studies with 1081 schizophrenia patients and 1026 healthy control subjects, it was
Stroop paradigm shown that schizophrenia patients exhibit an increased Stroop interference effect both in response time
Inhibition (mean effect size: M(g) = 0.43; 95% confidence interval, CI95%: 0.35–0.52) and accuracy (M(g) = 0.62;
Interference CI95%: 0.47–0.77) measures of interference. However, a meta-regression analysis revealed that the size of
Meta-analysis the effect varies depending on the version of the Stroop paradigm used. Regarding the response time mea-
Executive functions sures of interference, studies using the classical card version of the paradigm showed a significantly larger
effect size than studies using a single-trial computerized version of the paradigm (M(g) = 0.60 vs.
M(g) = 0.19). Despite of the dissociation between the two versions of the paradigm, the results of the present
meta-analysis indicate that the reported global deficits in executive functioning found to be associated with
schizophrenia are at least partly due to a reduced ability of cognitive inhibition.
© 2011 Published by Elsevier B.V.

1. Introduction meta-analyses have revealed that executive functions are affected in


schizophrenia (Green et al., 2000; Johnson-Selfridge and Zalewski,
Cognitive impairment can be considered a primary symptom asso- 2001; Fioravanti et al., 2005). However, although frequently treated
ciated with schizophrenia (Kerns et al., 2008; Simpson et al., 2010) as such, the term executive functions does not refer to a unitary cog-
and is likely to constitute the basis for the reduced abilities of schizo- nitive faculty; it rather summarizes a set of basic sub-components
phrenia patients to organize their lives with respect to vocational and which together constitute executive functioning (Miyake et al.,
interpersonal relations, or self-care activities (Aubin et al., 2009). 2000; Jurado and Rosselli, 2007). Thus, also the analysis of the execu-
Furthermore, the level of cognitive functioning has been shown to tive impairments associated with schizophrenia will likely benefit
be an important predictor for the recovery from the illness and the from an analysis on the level of specific subcomponents as opposed
functional outcome (Harvey et al., 1998; Green et al., 2000), underlin- to an approach on the global level of executive functioning (Kerns
ing the importance of achieving a better understanding of the nature et al., 2008).
of cognitive deficits associated with schizophrenia in order to opti- According to an influential model proposed by Miyake et al.
mize rehabilitation and intervention programs. The cognitive func- (2000), a central sub-component of executive functioning is the abil-
tions which enable individuals to interact with their environment in ity to utilize weaker sources of information or select less likely behav-
a purposeful and meaningful way are usually summarized in the ior in the presence of a competing, stronger sources or behavioral
term “executive functions” (Jurado and Rosselli, 2007), and previous tendencies (Miller and Cohen, 2001; Posner and Rothbart, 2007).
Usually referred to as “inhibition” or “cognitive inhibition” (Nigg,
2000; Friedman and Miyake, 2004; MacLeod, 2007) this process has
been defined as “the stopping or overriding of a mental process, in
whole or in part, with or without intention” (see MacLeod, 2007,
⁎ Corresponding author at: Department of Biological and Medical Psychology, University
p.5). A frequently applied paradigm which is considered to assess
of Bergen, Jonas Lies vei 91, N-5009 Bergen, Norway. Tel.: +47 5586640. cognitive inhibition (Miyake et al., 2000; Nigg, 2000) is the Stroop
E-mail address: rene.westerhausen@psybp.uib.no (R. Westerhausen). Color-Word Interference Test or, for short, the Stroop paradigm

0920-9964/$ – see front matter © 2011 Published by Elsevier B.V.


doi:10.1016/j.schres.2011.08.025
R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181 173

(Stroop, 1935; MacLeod, 1991). In this paradigm cognitive inhibition paradigm had to be described in enough detail to be able to extract all
is tested by asking the participants to name the ink color in which a information necessary to perform the analysis; (e) the results had to
series of color words is printed, whereas the ink color does not corre- be independent, i.e. had not been (in total or partly) published in anoth-
spond to the semantic meaning of the color word (e.g., the word er included report; and (f) the language of the publication was
“blue” printed in the color red). Confronted with such stimuli the English, French, or German.
dominant process is to read the word (i.e., answering with “blue”) The application of the above criteria reduced the number of stud-
and in order to successfully follow the requirements of the task, the ies to 36, published between 1984 and 2011. Of these, 23 used the
reading process has to be inhibited in favor of the naming of the ink DSM-IV, 7 the DSM-III-R, and 3 the ICD-10 to diagnose the patients.
color (here: “red”; c.f. Cohen et al., 1990; Friedman and Miyake, For the remaining three of the studies the diagnosis criteria were
2004). Although frequently applied and interpreted alone, this so- not explicitly stated. An overview of the included studies can be
called incongruent condition has to be related to a “neutral”, color found in Table 1 and Appendix A.
naming condition in order to quantify the extent to which the incon-
gruency interferes with the color naming performance (MacLeod, 2.2. Variables of interest
1991). An appropriate neutral condition contains stimuli, such as
“X's” or colored patches, of which the ink color has to be determined The INT in the Stroop paradigm is usually defined as the perfor-
by the participant. The response time or accuracy difference between mance in a neutral, color naming condition (NEU) subtracted from the
incongruent and neutral condition provides an interference (INT) performance in the incongruent (INC) condition (MacLeod, 1991). The
score and can be seen as an inverse indicator of inhibition subcompo- performance can be measured as time to perform the task or the num-
nent of executive functioning. Thus, deficits in inhibition should re- ber of errors committed while performing the task. Hence, INT as an in-
sult in an increased INT. crease in the response time (INT_T) or an increase in the number of
The use of the Stroop paradigm has a long tradition in schizophrenia errors (INT_E) served as dependant variables in the present meta-
research and dates back to a study by Wapner and Krus published in, analysis. Regarding the INT_T parameter, the included studies reported
1960 (Wapner and Krus, 1960), who were the first to show that pa- the response time in three different ways: (a) as the mean single-trial
tients with schizophrenia needed over-proportionally more time in response time differences per stimulus; (b) the time to name the colors
the interference condition than controls. Since these early studies, the of the stimuli present on each card, or (c) the number of stimuli correct-
Stroop paradigm has been frequently applied providing largely incon- ly identified in a given time period. However, all three measures could
sistent results (for review see Henik and Salo, 2004) and preventing a be expressed as items processed per time unit and are thus treated as
general conclusion about the cognitive inhibition abilities associated equivalent in the present analysis. Furthermore, three of the studies in-
with schizophrenia. Thus, the aim of the present meta-analysis was to cluded in the meta-analysis (cf. Table 1) used a method suggested by
systematically analyze and statistically summarize the studies available. Golden (1978) to determine INT instead of a simple difference score.
Since the inconsistency has been attributed to the large variety of para- This method utilizes a combination of a neutral color naming and a
digm versions that have been employed (Hepp et al., 1996; Perlstein et word reading condition (reading color words written in black ink) to
al., 1998; Henik and Salo, 2004), the present meta-analysis focuses on predict the time for the INC condition. The predicted time subtracted
the methodological aspects of the paradigm. More specifically, we from the observed time is considered a measure of INT. In order to
focus on the distinction between card and computerized versions of make use of as much data as possible in our meta-analysis, these
the Stroop paradigm, which – although both are supposed to assess three studies were included. However, a separate analysis removing
the same cognitive processes – show substantial methodological differ- these studies did not substantially change the results or their
ences that might especially interfere with the performance of schizo- interpretation.
phrenia patients. The traditional card versions of the paradigm usually
consists of a series of multiple-stimuli cards, with each card represent- 2.3. Calculation of study effect size
ing only one condition (e.g., one card for the neutral and one for the in-
congruent condition). In contrast, in the computerized version the The aim of the analysis was the difference between healthy con-
participant is presented with one stimulus at a time and stimuli of dif- trols and schizophrenia patients in the dependant variables INT_T
ferent conditions are usually intermixed. and INT_E, whereby the difference was expressed as the effect size
Hedges' g serving as an unbiased estimate of the population effect.
2. Material and methods Hedges' g represents the standardized mean difference (also known
as Cohen's d) corrected for the sample bias (Hedges and Olkin, 1985).
2.1. Study characteristics and selection In the attempt to calculate the effect sizes for the included studies,
three different situations were encountered. First, both mean and
The studies were selected using Pubmed (ncbi.nlm.nih.gov/ standard deviation for the respective INT parameter were available
pubmed), ISI Web of Knowledge (apps.isiknowledge.com), and PsycInfo so that g could be directly computed. Second, only the test statistics
(apa.org/pubs/databases/psycinfo) databases using combined search (F-/t-values) for the group comparison were reported in the original
terms related to the Stroop paradigm (Stroop, color-word test, interfer- study and the effect size had to be calculated using formulas convert-
ence) and to schizophrenia (schizophrenia, psychosis). Furthermore, the ing these test-statistics to effect size measures (Cohen, 1988). Third,
reference lists of published articles were used to locate additional stud- only the raw mean and standard deviations of the experimental con-
ies. The search was performed in the end of December 2010 and the ditions (incongruent, neutral) were reported. In this case, following
meta-analysis thus covers all studies published or published online the approach taken by van Mourik et al. (2005), mean and standard
ahead of print at this time point. After screening the abstracts of the ini- deviation of the INT score were calculated for each group before the
tial search results for relevance, 141 studies were identified. These stud- effect size measures were determined. To achieve this, however,
ies were analyzed deeper and the following inclusion criteria were also the standard deviation of the interference score has to be esti-
applied: (a) inclusion of a healthy, non-clinical control group in addition mated which is only possible knowing the intercorrelation of the per-
to the schizophrenia group; (b) application of a standard version of the formance in the NEU and the INC conditions. As suggested by van
paradigm, i.e. excluding emotional, lateralized, or phonemic variants of Mourik et al. (2005), this correlation was set to r = 0.70 what closely
the Stroop paradigm; (c) calculation of effect size measure for a group matches the correlation reported by other studies (Abramczyk et al.,
comparison regarding INT possible, i.e. studies not including a neutral 1983). In two studies (Boucart et al., 1999; Chen et al., 2001) the
“color-naming” condition were excluded (see below); (d) the Stroop raw RT or error means (and SD) were only available in graphs, and
174 R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181

Table 1
Characteristics of studies included in meta-analysis.

StudyID Schizophrenia patients Controls Stroop paradigm Comment on data usage

n m/all age Diagnosis n m/all Age Version Interference Stimulus Response


criterium calculation presentation modality

Barch 1999a 40 0.50 39.4 DSM-IV 20 0.45 36.1 CPT Difference Intermixed Verbal Effect is mean of two conditions
using color patches and animal
names, respectively, as neutral
stimuli
Barch 1999b 56 0.57 28.3 DSM-IV 25 0.52 35.2 CPT Difference Intermixed Verbal
Barch 2004 29 0.55 35.4 DSM-IV 29 0.62 36.2 CPT Difference Intermixed Verbal
Barch 2005 10 0.67 40.3 DSM-IV 22 0.55 36.6 CPT Difference Intermixed Verbal Data from placebo condition
Barr 2008 28 0.57 47.0 DSM-IV 32 0.53 40.0 Card Golden Blocked Verbal Data as average of pre-nicotine
and pre-placebo condition
Boucart 1999 12 0.75 30.9 n.a. 12 0.75 n.a. CPT Difference Both Verbal Average of block and intermixed
task version
Brebion 1996 32 0.66 35.6 DSM-IV 32 0.69 37.1 Card Difference Blocked Verbal
Breton 2011 52 0.69 32.7 DSM-IV 53 0.36 43.8 Card Difference Blocked Verbal
Buchanan 1994 39 n.a. n.a. DSM-III-R 30 0.67 34.2 Card Golden Blocked Verbal Patient data as average of both
groups
Carter 1993 23 0.83 32.1 DSM-III-R 14 0.71 31.3 CPT Difference Intermixed Verbal Patient data pooled over both
patient groups; Sample is
extension of Carter et al. (1992)
Carter 1997 14 0.57 35.7 DSM-IV 15 0.47 34.3 CPT Difference Intermixed Verbal
Chen 2001 56 0.45 32.8 DSM-IV 64 0.41 34.4 CPT Difference Intermixed Manual Patient data as average of both
measuring points
Dollfus 2002 17 0.70 29.8 DSM-IV 17 0.70 28.1 Card Difference Blocked Verbal
George 2002 25 n.a. n.a. DSM-IV 35 n.a. n.a. CPT Difference Intermixed Manual Mean of smoker and non-
smokers at baseline
Golden 1976 35 n.a. n.a. n.a. 37 n.a. n.a. Card Difference Blocked Verbal
Haker 2009 43 0.74 34 ICD-10 45 0.73 35 Card Difference Blocked Verbal Original study used quotient
to express INT_T; difference
values kindly provided by
authors
Henik 2002 11 0.82 32.1 DSM-III-R 16 0.81 31.7 CPT Difference Intermixed Verbal Data as average of the three
employed experimental
conditions
Hepp 1996 44 0.55 36.0 ICD-10 50 0.58 36.9 CPT Difference Intermixed Verbal Also provides Card data for
subsample of 9 patients and
31 controls.
Jaquet 1997 42 0.60 37.7 DSM-IV 19 n.a. n.a. Card Difference Blocked Verbal
Killian 1984 34 0.50 24.3 Others 26 0.50 28.8 Card Difference Blocked Verbal Patient data as average of both
measuring points
Markela-Lerenc 2009 15 0.60 27.4 DSM-IV 15 0.47 27.7 CPT Difference Intermixed Manual
Matsuzawa 2008 20 0.60 30.7 DSM-IV 16 0.75 30.0 Card Difference Blocked Verbal
McGowan 2004 16 n.a. 37.4 DSM-IV 12 n.a. 38.3 Card Difference Blocked Verbal
McNeely 2003 13 0.62 31.6 DSM-IV 13 0.54 28.7 CPT Difference Intermixed Manual
Moritz 2002 25 0.56 34.7 DSM-IV 70 1.33 33.1 Card Difference Blocked N.a.
Mulet 2007 46 0.70 31.5 DSM-IV 39 0.21 21.6 Card Golden Blocked Verbal
Nordahl 2001 9 0.78 37.6 DSM-III-R 10 0.80 32.3 CPT Difference Intermixed Verbal
Perlstein 1998 55 0.54 38.5 DSM-IV 24 0.56 35.5 Both Difference Both Verbal Average of CPT and card version
for main analysis
Rizzo 1996 33 0.64 32.8 DSM-III-R 33 0.64 31.3 Card Difference Blocked Verbal
Sacco 2006 14 0.43 41.9 DSM-IV 15 0.67 38.3 CPT Difference N.a. N.a.
Salo 1997 24 n.a. n.a. DSM-III-R 16 0.56 40.8 CPT Difference Intermixed Verbal Patient data as average of both
groups
Salo 2002 23 n.a. n.a. DSM-IV 16 0.63 36.4 CPT Difference Intermixed Verbal Patient data as average of both
groups;
Scholes 2010 49 0.88 37.8 ICD-10 35 0.77 34.2 Card Difference Blocked Verbal Data of non-cannabis groups
Szoke 2009 54 0.72 33.8 DSM-IV 42 0.52 41.5 Card Difference Blocked Verbal
Takei 2009 31 0.39 33.8 DSM-IV 65 0.37 34.7 CPT Difference Intermixed Verbal
Taylor 1996 12 0.67 39.2 DSM-III-R 12 0.67 37.9 CPT Difference Intermixed Verbal

Notes: The StudyID (first column) refers to the list provided in Appendix A; n = number of subjects; m/all = proportion of males in the respective sample; CPT = computerized
version of the Stroop paradigm; Card = card version of the Stroop paradigm; n.a. = respective information not available.

thus were read out using a ruler. This procedure was conducted twice effect. The effect size obtained for INT_T and INT_E, respectively,
and the average of both read-outs was taken to calculate the INT served as dependant variables. Regarding the analysis of INT_T, first
scores. Finally, whenever more than one effect size estimate was an “analytic” meta-analysis was performed using a fixed-effects
available for a study the average of the different effects was taken model to estimate the weighted mean effect (M(g)) over all studies
(for details see Table 1). and test whether it deviates from zero. A fixed-effect approach was
a priori chosen with the assumption that all included studies measure
2.4. Statistical analysis the same population effect.
Since the first analysis step indicated significant inhomogeneity in
A meta-analysis was conducted testing for differences between the INT_T effect sizes, a second, explorative meta-analysis step was
patients with schizophrenia and healthy controls in the interference conducted aiming to identify reasons for this variance. Following
R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181 175

the procedure described by Hedges and Olkin (1985), the meta- inhomogeneity remained with I2 =78.4% high for the card version, but
regression analysis was performed using a weighted-least square ap- was low (I2 =33.8%) in the computerized version.
proach with the inverse of each study's weight (i.e., one divided by
the estimated variance of g) employed as weights. Suggested to be 3.2. Interference as increase in errors
an important influencing factor (Hepp et al., 1996; Perlstein et al.,
1998; Henik and Salo, 2004) the meta-regression analysis was The meta-analysis of the INT_E consisted of k = 12 studies including
applied contrasting the results of studies which used a card version 424 patients and 343 control subjects (cf. Fig. 3). The fixed effect estima-
of the paradigm with the results of those studies that used single- tion revealed a significant weighted mean effect size of M(g) = 0.62
trial computerized version. (CI95%: 0.47–0.77; Z = 8.22; p b 0.0001) indicating a stronger interfer-
The threshold of statistical significance for the mean effect size ence effect in the patient group. A significant intercept of the Egger's re-
analysis as well as for the meta-regression were set to α = 0.05. The gression analysis (a= 3.21; t(11) = −2.46; p = 0.034) can be taken to
significant threshold for inhomogeneity testing was set to α = 0.10 indicate a significant report bias in the data, which might lead to an
to increase statistical power (Deeks et al., 2008) and the inhomogene- overestimation of the population effect size. However, an Nfs = 196 in-
ity was expressed using the I 2 index, which quantifies the percentage dicates that the number of unpublished studies (showing no effect)
of the variability in the effect size estimates due to inhomogeneity of would have to be rather large to nullify the present effect in the pub-
the studies. The presence of a publication bias was assessed using fun- lished studies. Homogeneity of the included study effects can be as-
nel plots and Egger's regression procedure (Egger et al., 1997), and for sumed (Q(11)= 16.07, p = .139; I2 = 31.6%).
significant effects Rosenberg's fail safe N was calculated to estimate
the number of unpublished studies (showing no effect) which 4. Discussion
would nullify a present effect in the published studies (Rosenberg,
2005). Power analyses were conducted using GPower 3.0 software The present meta-analysis indicates that patients with schizo-
(http://www.psycho.uni-duesseldorf.de/abteilungen/aap/gpower3/). phrenia show a significant increased interference effect when com-
pared with healthy controls. The interference effect was present
3. Results both regarding the response time (INT_T) and the errors (INT_E) in
the Stroop paradigm. Patients with schizophrenia not only appear to
3.1. Interference as increase in response time be over-proportionally slower than controls, but also produce rela-
tively more errors in a task in which inhibitory control processes
The analytic meta-analysis included k = 36 studies summarizing are required. Thus, the present analysis supports the notion that
the data of 1081 schizophrenia patients and 1026 healthy schizophrenia is associated with a reduction in the ability of cognitive
control subjects. The analysis revealed a mean weighted effect size inhibition. Beyond this overall effect, the present data also confirms a
of M(g) = 0.43 (95% confidence interval, CI95%: 0.35–0.52), signifi- dissociation between the INT_T results obtained with the card and
cantly deviating from zero (Z = 9.62, p b 0.0001), and indicating that computerized version of the Stroop paradigm, i.e. although both ver-
the patients with schizophrenia show a pronounced INT_T. The Fail sions are supposed to measure the same cognitive construct, the two
Safe N was high (Nfs = 828) and a non-significant intercept in the versions provide inconsistent results when applied in schizophrenia
Egger's regression analysis (a = −1.35; t(35) = −0.98; p = 0.33) research. The level of performance in the two test versions seems to
indicates that a report bias is unlikely. However, a significant test be influenced not only by the ability of cognitive inhibition, but also
for inhomogeneity (Q(35) = 118.47, p b 0.0001) together with an by additional aspects of the testing procedure. Apparently, these as-
I 2 = 70.5% indicated a substantial inter-study variability in the latent pects differentially affect schizophrenia patients and controls so that
population effect sizes (Deeks et al., 2008). a closer examination of possible reasons for this dissociation is likely
To further explore reasons for the inhomogeneity we conducted a to shed additional light on the cognitive impairments associated with
meta-regression analysis contrasting the results of studies which schizophrenia. In the following sections, we thus examine in more de-
used a card or computerized version of the test. One study (Perlstein tail the methodological differences between the card and the comput-
et al., 1998), providing data for both test versions, was excluded from erized version which might have contributed to the differences in the
the regression analysis in order to guarantee independence of the group comparison effect size revealed for the two test versions.
data points included for both test versions. The analysis revealed a
significant prediction of the study effect size by test version (b =
−0.44; t(32) = − 2.88, p = 0.007, see Fig. 1) indicating a significantly
larger effect in the card as compared to the computerized version of
the Stroop paradigm. The weighted mean effect size of the 16 includ-
ed studies (including 565 patients and 538 controls) using the card
version was M(g) = 0.68 (CI95%: 0.55–0.80). The weighted mean ef-
fect of the 19 studies (461 patients, 464 controls) using the comput-
erized version was M(g) = 0.22 (CI95%: 0.09–0.35). Although
different in magnitude, the mean effects of both versions also deviat-
ed significantly from zero (card version: Z = 10.71, p b 0.0001,
Nfs = 459; computerized version: Z = 3.26; p = 0.001; Nfs = 31).
Adding the data from Perlstein et al.(1998), as well as the results of
the card version provided by Hepp et al.(1996), the weighted mean effect
size of the card version increased slightly to M(g)=0.60 (CI95%: 0.48–
0.71; 18 studies; 629 patients, 593 controls; see Fig. 2a) and remained sig-
nificant (Z=9.90; pb 0.0001; Nfs=438). Adding the results of Perlstein Fig. 1. Meta-regression analysis indicating a significant difference (b = − 0.44; t(32) =
et al. (1998) to the analysis of computerized version slightly reduced − 2.88, p = 0.007) between the results obtained in the card and computerized version
the mean effect size to M(g)=0.19 (CI95%: 0.06–0.32; 20 studies; 516 of the Stroop paradigm. Each circle represents the effect size of a single study. The size
of the circle codes the weight with which of each effect size was entered in the meta-
patients, 488 controls; Z=2.97; p=0.003; Nfs=23; see Fig. 2b). Inter- regression analysis (weighted-least square approach). The solid horizontal lines indi-
estingly, although significant for both the card (Q(17)=78.85, cate the mean effect for both test versions, and the gray area marks the 95%-confidence
pb 0.0001) and the computerized version (Q(19)=28.70, p=0.07), the interval of the mean effects.
176 R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181

Fig. 2. Forest plot of the study effect size (squares) and 95%-confidence interval (horizontal line) of the difference between schizophrenia patients and controls in the Stroop inter-
ference effect measured as increase in response time (INT_T): (a) and (b) summarize the studies utilizing the card and the computerized version, respectively. The size of the square
indicates the weight of the study in the calculation of the mean effect over all studies (bottom row; gray diamond). Open squares indicate those studies which were not part of the
meta-regression analysis (for details see Result section). The numbers at the right margin represent the individual study effect size; the numbers in parentheses give the lower and
upper boundaries of its confidence interval.
R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181 177

Fig. 3. Forest plot of the study effect size (squares) and 95%-confidence interval (horizontal line) of the difference between schizophrenia patients and controls in the Stroop inter-
ference effect measured as increase in response errors (INT_E). The size of the square indicates the weight of the study. The open squares represent studies which used the card
version of the paradigm, while the black squares are studies using a computerized version. Like in Fig. 2, numbers at the right margin represent the individual study effect size
and the boundaries of the confidence interval.

4.1. Dissociation between card and computerized Stroop version presentation, (c) the response modality, and (d) the way errors are
accounted in the data analysis (Henik and Salo, 2004). Regarding
The Stroop paradigm versions which have been used to study the context of stimulus presentation, the computerized version pre-
schizophrenia patients can be grouped in two major categories sents only one stimulus at a time (the target stimulus), while the
(Henik and Salo, 2004): traditional multiple-stimuli card versions card version additionally confronts the subjects – depending on the
and single-trial computerized versions. The card version consists of position of the target stimulus on the card – with two or more flank-
a series of cards – one for each condition – on which multiple stimuli ing stimuli which can be present below, above, and to either side of
are presented, and the total time to name the color of all items of a the target stimulus. Thus, the card version might be seen as a “dual
card (or number of correctly named stimuli in a given time) is task”, which not only requires inhibiting the prepotent process of
taken as measure of performance. In the computerized version one reading in favor of the color naming (Cohen et al., 1990), but also de-
stimulus is presented at a time, whereby stimuli of different condi- mands resistance to interference from adjacent non-target stimuli
tions are usually intermixed. Regarding the response time derived (Friedman and Miyake, 2004). As a result, the card version might be
measures (INT_R), the present meta-analysis indicates that the tradi- experienced as more demanding than the computerized version,
tional multiple-stimuli card versions yielded, with M(g) = 0.60 to what especially would affect the performance of schizophrenia pa-
0.68, a mean effect size which can be classified to be moderate to tients. In accordance with this notion, Boucart et al. (1999) report
large (Cohen, 1988). On the other hand, studies using the computer- an increase in the interference effect in schizophrenia patients in a
ized version yielded only a small mean effect size (M(g) = 0.19 to computerized Stroop version with additionally presented flanking
0.22). This dissociation fits well to the observation presented in a color words relative to the performance in the regular single-item
review by Henik and Salo (2004), that only the use of the card version version of the task. Furthermore, only in the task with flanking non-
consistently reveals a difference between schizophrenia patients and target words, the interference effect was stronger in schizophrenia
controls. The here indicated smaller population effect size of the patients than in healthy controls, who in general appear to be little af-
computerized version requires a substantially larger sample size to fected by the presence of distractor stimuli (MacLeod and Hodder,
guarantee sufficiently high statistical power (see Supplementary 1998; MacLeod and Bors, 2002). Although these findings indicate a
Table 1). Thus, assuming comparable sample sizes, studies using the higher susceptibility to distracting stimuli in patients, evidence from
card version should more frequently and consistently yield significant studies directly assessing the patients' resistance to interference, e.g.
group comparisons than studies using the computerized version. The by using various versions of the Flanker task (Friedman and Miyake,
claim of a dissociation between the two versions of the paradigm is 2004), appears to be inconsistent. While some studies find an in-
further supported by the studies on healthy subjects, reporting no creased distractor interference in schizophrenia (Wang et al., 2005;
or only moderate correlations of INT assessed with the computerized Urbanek et al., 2009; Breton et al., 2011) others do not find any signif-
and the card version (Hepp et al., 1996; Kindt et al., 1996; Perlstein et icant differences to control groups (Kopp et al., 1994; Nestor et al.,
al., 1998). 2007). However, assuming that the presence of flanking stimuli
Possible reasons for this dissociation might be found in (a) the would indeed be the basis for the dissociation between card and com-
context of stimulus presentation, (b) the mode of stimulus puterized version, it is not clear if this is due to the presence of non-
178 R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181

target stimuli per se or to the fact that the dual-task situation over- subjects have shown that the Stroop interference effect is reduced
strains the patients' limited cognitive resources. In any case, it when the response modality is switched from oral to manual re-
would appear that as long as the patients are confronted with only sponse (Redding and Gerjets, 1977; Ikeda et al., 2010). This effect
one stimulus or task at a time, their performance is little affected. was explained referring to stimulus–response compatibility, i.e. in
With increasing cognitive load, however, the deficits become more the oral response modality the pre-dominant, but incorrect response
obvious. of reading the word maps onto the same (oral) response modality as
A second methodological difference between the two Stroop par- the required response to name the color. In the manual response mo-
adigm versions can be found in the mode of stimulus presentation, dality, however, the correct and incorrect answer map on to different
i.e. whether the different conditions (neutral, incongruent, etc.) are responses, apparently reducing the interference effect (MacLeod,
presented in separate blocks or in an intermixed, randomized fashion. 1991). Applied on the present case, the use of the manual response
The mode of presentation is tightly linked to the Stroop version: all modality in some of the computerized studies should result in a smal-
studies included in the present meta-analysis which used the card ler average (across studies) interference effect compared with card
version also used a blocked presentation with the stimulus cards con- versions of the paradigm. However, it should only have an effect on
taining stimuli of only one condition. Of the 20 studies using comput- the observed difference regarding the group effect sizes, if it would
erized version, all but one study used intermixed presentation only, be assumed that the manual response reduces the interference effect
whereas the exception, Boucart et al. (1999), additionally used a stronger in schizophrenia patients than controls. Recalculating the
blocked version of the single-trial version. However, basic experi- meta-analysis of the computerized studies after removing the five
mental research on the Stroop interference effect in healthy subjects single-trial studies which did not employ verbal responses, the
has repeatedly shown that intermixing incongruent trials with neu- mean effect dropped from the original M(g) = 0.19 with 20 studies
tral or congruent trial increases the response time to the incongruent to M(g) = 0.13 (CI95%: −0.02–0.27; Z = 1.66; p = 0.096). Thus, rath-
trials and, in turn, also the interference effect (Lowe and Mitterer, er than bringing the effect size of computerized and card version clos-
1982; Tzelgov et al., 1992). This effect appears to be linear, i.e. the in- er together it increased the distance between them, so that it seems
terference effect gets stronger the less frequent the incongruent trials unlikely that the response modality can explain the effect size differ-
are (Tzelgov et al., 1992). Interestingly, however, a study by Henik et ences found between both versions of the test.
al. (2002) showed that the interference effect is less affected by the Fourth, the difference in effect sizes might be due to the different
intermixing of congruent and neutral trials in schizophrenia patients ways in which the two test versions deal with errors committed dur-
than in control subjects. Manipulating the proportion of incongruent ing testing. Regarding the computerized version, error trials are usu-
stimuli in three steps (37.5%, 25%, and 12.5%) did not significantly ally removed from the analysis and the mean reaction time is
alter the interference effect in the schizophrenia group, but stepwise calculated considering only the correct color naming responses
increased the interference effect in the control group (Henik et al., (Carter et al., 1992; Chen et al., 2001; Takei et al., 2009). However,
2002). As a result the group difference, expressed as effect size, chan- in the majority of studies using the card version it is not explicitly
ged from g = 0.62, i.e. lower interference in controls, to g = − 0.39 stated how errors were treated. Perlstein et al. (1998) explicitly re-
and −0.55, respectively, indicating lower interference in patient port that erroneous responses were pointed out to the subjects with
group. Interpolating from these findings it could be predicted that a the instruction to correct the response (see also Stroop's original pro-
blocked presentation mode, like the card version (with blocks of cedure; Stroop, 1935). However, even when not pointed out by the
100% incongruent trials), would show the largest differences between examiner, participants might notice their errors and spontaneously
the two groups. On the other hand, standard intermixed presentation correct themselves (van der Elst et al., 2006). Thus, the mean time
modes, employing between 25 and 50% incongruent stimuli (cf. measured in the incongruent but also in the neutral condition of the
Carter et al., 1992; Takei et al., 2009), should produce smaller effect card version, not only summarizes correct responses (like in the
sizes. These predictions would well fit to the results of the present single-trial version) but also includes the time for erroneous
meta-analysis showing that the difference between schizophrenia pa- responses and their corrections. Furthermore, the present meta-
tients and controls in INT_T is smaller in the intermixed computer- analysis showed a significant higher INT_E in schizophrenia patients
ized than in the blocked card version. However, the only study (M(g) = 0.62–0.64) as compared to controls, also indicating an
comparing blocked and intermixed presentation mode in the same over-proportionally increased number of errors in the incongruent
subjects by Boucart et al. (1999) did not reveal any significant effect condition in schizophrenia patients. Consequently, the inclusion of in-
on the group difference in INT_T. Regarding the cognitive processes correct and corrected answers in the time measures obtained for the
that might underlie the described phenomenon, it has been argued card version substantially biases the time measures of the card ver-
that a blocked presentation (or high proportion of incongruent stim- sion in disfavor of the patients, resulting in an accentuation of the in-
uli) allows healthy subjects to establish a task set or cognitive task terference effect (when expressed as INT_T). The increased effect size
representation which leaves the subject prepared to inhibit the of the INT_T found in the card as opposed to the computerized ver-
word reading (Tzelgov et al., 1992). The task set is, however, weaker sion might thus at least partly reflect the inclusion of errors than indi-
when only a low proportion of incongruent stimuli is presented mak- cate the involvement of divergent cognitive processes in the two test
ing it more difficult for the subject to exert inhibitory processes, and versions.
increasing the response times. In schizophrenia patients the task set
might be in general be weaker than in healthy controls, and changes 4.2. Limitations and perspective
in the proportions of incongruent stimuli might less affect the quality
of the already weak task set, so that the response time stay on stable, The present meta-analysis focused on the methodological aspects
low level. of the Stroop paradigm and how these aspects influence the perfor-
Third, it has been suggested that differences in the response mo- mance of schizophrenia patients relative to healthy controls. An alter-
dality might also contribute to the differences between the card and native approach would be to focus on patient variables, i.e. how
computerized version (Henik and Salo, 2004). In the present meta- different symptoms or subgroups affect the performance. Indeed,
analysis, all studies based on the card version used an oral response, some studies have addressed the questions how patients with posi-
while this was only the case in 15 out of the 20 studies using a com- tive vs. negative symptoms (e.g., Buchanan et al., 1994), or first-
puterized version. Four of the remaining five studies used a manual episode patients initially vs. after stabilization (e.g., Chen et al.,
response, i.e. a keypress, as response mode and in one study the rele- 2001) perform in the Stroop paradigm. Other studies were interested
vant information was not reported. Previous studies on healthy in the effects medication has on the performance (e.g., Killian et al.,
R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181 179

1984). It appears likely that these and other patient variables have Barch 1999a: Barch, D. M., Carter, C. S., Hachten, P. C., Usher, M.,
substantial impact on the level of performance. Thus, a systematic Cohen, J. D., 1999. The “benefits” of distractability: mechanisms
analysis of the effect of these variables would provide valuable infor- underlying increased Stroop effects in schizophrenia. Schizophr. Bul.
mation about how much the here revealed impairment in cognitive 25(4) 749–762.
inhibition can be considered a primary symptoms of schizophrenia
or is just secondary to medication or other symptoms. However, at Barch 1999b: Barch, D. M., Carter, C. S., Perlstein, W., Baird, J.,
the present time point the few available studies examining the effect Cohen, J. D., Schooler, N., 1999. Increased Stroop facilitation
of these specific patient variables do not allow a meta-analytic effects in schizophrenia are not due to increased automatic spreading
summary. activation. Schizophr. Res. 39(1) 51–64.
The separate analyses of studies using the computerized and the
card versions of the Stroop paradigm did not only reveal difference Barr 2008: Barr, R. S., Culhane, M. A., Jubelt, L. E., Mufti, R. S., Dyer,
in effect size, but also indicated difference in the homogeneity of M. A., Weiss, A. P., et al., 2008. The effects of transdermal nicotine on
the individual study results: the effect sizes from studies using the cognition in nonsmokers with schizophrenia and nonpsychiatric
computerized version were homogenous, while those of the card ver- controls. Neuropsychopharmacology 33(3) 480–490.
sion still showed considerable inhomogeneity. Thus, other – here not
considered patient or methodological variables – might substantially Boucart 1999: Boucart, M., Mobarek, N., Cuervo, C., Danion, J. M.,
influence the performance in the card version of the paradigm, and 1999. What is the nature of increased Stroop interference in schizo-
increase the variance of the results. The nature of these factors re- phrenia? Acta Psychol., 101(1). 3–25.
mains to be determined.
Brebion 1996: Brebion, G., Smith, M. J., Gorman, J. M., Amador, X.,
4.3. Conclusion 1996. Reality monitoring failure in schizophrenia: the role of selective
attention. Schizophr. Res. 22(2) 173–180.
The present meta-analysis indicates that schizophrenia patients
show an increased Stroop interference effect which is present both Breton 2011: Breton, F., Plante, A., Legauffre, C., Morel, N., Ades, J.,
in time and accuracy measures of interference. This finding supports Gorwood, P., et al., 2011. The executive control of attention differen-
the notion that the reported deficits in global executive functioning tiates patients with schizophrenia, their first-degree relatives and
(Green et al., 2000; Fioravanti et al., 2005) are at least partly attribut- healthy controls. Neuropsychologia 49 203–208.
able to an impairment in the sub-component of cognitive inhibition.
It remains to be analyzed if these deficits can also be measured in Buchanan 1994: Buchanan, R. W., Strauss, M. E., Kirkpatrick, B.,
other paradigms, e.g. Stop signal paradigms, which are also assumed Holstein, C., Breier, A., Carpenter, W. T., Jr., 1994. Neuropsychological
to measure cognitive inhibition (Friedman and Miyake, 2004). Since impairments in deficit vs nondeficit forms of schizophrenia. Arch
cognitive inhibition only represents one of several sub-components Gen Psychiatry 51(10) 804–811.
of executive functions (Miyake et al., 2000; Kerns et al., 2008), it
also remains to be systematically analyzed if and to what degree Carter 1997: Carter, C. S., Mintun, M., Nichols, T., Cohen, J. D., 1997.
other sub-components, like shifting or updating (Miyake et al., Anterior cingulate gyrus dysfunction and selective attention deficits
2000), are affected. Such necessary extensions would ultimately in schizophrenia: O-15 H2O PET study during single-trial Stroop
lead to a profile of executive deficits in schizophrenia, which might task performance. Am. J. Psychiatry. 154 1670–1675.
prove helpful to evaluate treatment effects, support remediation or
training approaches, and guide future research. Carter 1993: Carter, C. S., Robertson, L. C., Nordahl, T. E., O'Shora-
Supplementary materials related to this article can be found on- Celaya, L. J., Chaderjian, M. C., 1993. Abnormal processing of irrelevant
line at doi:10.1016/j.schres.2011.08.025. information in schizophrenia: the role of illness subtype. Psychiatry
Res. 48 17–26.
Role of funding source
Funding for this study was provided by European Research Council (ERC, Advanced Chen 2001: Chen, E. Y. H., Wong, A. W. S., Chen, R. Y. L., Au, J. W. Y.,
Grant to Kenneth Hugdahl); the ERC had no further role in study design; in the collec-
2001. Stroop interference and facilitation effects in first-episode
tion, analysis and interpretation of data; in the writing of the report; and in the deci-
sion to submit the paper for publication. schizophrenic patients. Schizophr. Res. 48(1) 29–44.

Contributors Dollfus 2002: Dollfus, S., Lombardo, C., Benali, K., Halbecq, I.,
RW designed the study, managed the literature search and statistical analyses. RW, Abadie, P., Marie, R. M., et al., 2002. Executive/attentional cognitive
KK, and KH wrote the manuscript. All authors contributed to and have approved the functions in schizophrenic patients and their parents: a preliminary
final manuscript.
study. Schizophr. Res. 53 93–99.
Conflict of interest
None. George 2002: George, T. P., Vessicchio, J. C., Termine, A., Sahady,
D. M., Head, C. A., Pepper, W. T., et al., 2002. Effects of smoking
Acknowledgment abstinence on visuospatial working memory function in schizophre-
None. nia. Neuropsychopharmacology 26(1) 75–85.

Appendix A. Study ID and studies included in the meta-analysis Golden 1976: Golden, C. J., 1976. Identification of brain disorders
by the Stroop Color and Word Test. J. Clin. Psychol. 32(3) 654–658.
Barch 2005: Barch, D. M., Carter, C. S., 2005. Amphetamine
improves cognitive function in medicated individuals with schizo- Haker 2009: Haker, H., Rossler, W., 2009. Empathy in schizophrenia:
phrenia and in healthy volunteers. Schizophr. Res. 77(1) 43–58. impaired resonance. Eur. Arch. Psychiatry Clin. Neurosci. 259(6) 352–361.

Barch 2004: Barch, D. M., Carter, C. S., Cohen, J. D., 2004. Factors Henik 2002: Henik, A., Carter, C. S., Salo, R., Chaderjian, M., Kraft, L.,
influencing Stroop performance in schizophrenia. Neuropsychology Nordahl, T. E., et al., 2002. Attentional control and word inhibition in
18(3) 477–484. schizophrenia. Psychiatry Res. 110(2) 137–149.
180 R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181

Hepp 1996: Hepp, H. H., Maier, S., Hermle, L., Spitzer, M., 1996. The Scholes 2010: Scholes, K. E., Martin-Iverson, M. T., 2010. Cannabis
Stroop effect in schizophrenic patients. Schizophr. Res. 22(3) 187–195. use and neuropsychological performance in healthy individuals and
patients with schizophrenia. Psychol. Med. 40(10) 1635–1646.
Jaquet 1997: Jaquet, I., Lancon, C., Auquier, P., Bougerol, T., Scotto,
J. C., 1997. Frontal neuropsychological impairments in 42 schizophrenic Szoke 2009: Szöke, Andrei, Meary, Alexandre, Ferchiou, Aziz,
patients. Encephale 23(1) 34–41. Trandafir, Anca, Leboyer, Marion, Schuerhoff, Franck, 2009. Correla-
tions between cognitive performances and psychotic or schizotypal
Killian 1984: Killian, G. A., Holzman, P. S., Davis, J. M., Gibbons, dimensions. Eur Psychiatry 24(4) 244–250.
R. D., 1984. Effects of psychotropic medication on selected cognitive
and perceptual measures. J. Abnorm. Psychol. 93(1). 58–70. Takei 2009: Takei, K., Yamasue, H., Abe, O., Yamada, H., Inoue, H.,
Suga, M., et al., 2009. Structural disruption of the dorsal cingulum
Markela-Lerenc 2009: Markela-Lerenc, J., Schmidt-Kraepelin, C., bundle is associated with impaired Stroop performance in patients
Roesch-Ely, D., Mundt, C., Weisbrod, M., Kaiser, S., 2009. Stroop inter- with schizophrenia. Schizophr. Res. 114(1–3) 119–127.
ference effect in schizophrenic patients: an electrophysiological
approach. Int. J. Psychophysiol. 71(3). 248–257. Taylor 1996: Taylor, S. F., Kornblum, S., Tandon, R., 1996. Facilita-
tion and interference of selective attention in schizophrenia. J. Psy-
Matsuzawa 2008: Matsuzawa, D., Obata, T., Shirayama, Y., Nonaka, chiatr. Res. 30(4). 251–259.
H., Kanazawa, Y., Yoshitome, E., et al., 2008. Negative correlation
between brain glutathione level and negative symptoms in schizo-
References
phrenia: a 3 T 1H-MRS study. PLoS One 3(4) e1944.
Abramczyk, R.R., Jordan, D.E., Hegel, M., 1983. “Reverse” Stroop effect in the perfor-
McGowan 2004: McGowan, S., Lawrence, A. D., Sales, T., Quested, mance of schizophrenics. Percept. Mot. Skills 56, 99–106.
Aubin, G., Stip, E., Gelinas, I., Rainville, C., Chapparo, C., 2009. Daily activities, cognition and
D., Grasby, P., 2004. Presynaptic dopaminergic dysfunction in schizo- community functioning in persons with schizophrenia. Schizophr. Res. 107 (2–3),
phrenia - A positron emission tomographic F-18 fluorodopa study. 313–318.
Arch. Gen. Psychiatry 61(2) 134–142. Boucart, M., Mobarek, N., Cuervo, C., Danion, J.M., 1999. What is the nature of increased
Stroop interference in schizophrenia? Acta Psychol. 101, 3–25.
Breton, F., Plante, A., Legauffre, C., Morel, N., Ades, J., Gorwood, P., Ramoz, N., Dubertret, C.,
McNeely 2003: McNeely, H. E., West, R., Christensen, B. K., Alain, C., 2011. The executive control of attention differentiates patients with schizophrenia,
2003. Neurophysiological evidence for disturbances of conflict proces- their first-degree relatives and healthy controls. Neuropsychologia 49, 203–208.
Buchanan, R.W., Strauss, M.E., Kirkpatrick, B., Holstein, C., Breier, A., Carpenter Jr., W.T.,
sing in patients with schizophrenia. J. Abnorm. Psychol. 112(4) 679–688.
1994. Neuropsychological impairments in deficit vs nondeficit forms of schizo-
phrenia. Arch. Gen. Psychiatry 51, 804–811.
Moritz 2002: Moritz, S., Birkner, C., Kloss, M., Jahn, H., Hand, I., Carter, C.S., Robertson, L.C., Nordahl, T.E., 1992. Abnormal processing of irrelevant in-
Haasen, C., et al., 2002. Executive functioning in obsessive- formation in chronic schizophrenia: selective enhancement of Stroop facilitation.
Psychiatry Res. 41 (2), 137–146.
compulsive disorder, unipolar depression, and schizophrenia. Arch. Chen, E.Y.H., Wong, A.W.S., Chen, R.Y.L., Au, J.W.Y., 2001. Stroop interference and
Clin. Neuropsychol. 17(5) 477–483. facilitation effects in first-episode schizophrenic patients. Schizophr. Res. 48 (1),
29–44.
Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences. Lawrence Erl-
Mulet 2007: Mulet, B., Valero, J., Gutierrez-Zotes, A., Montserrat, C., baum, Hillsdale, NJ.
Cortes, M. J., Jariod, M., et al., 2007. Sustained and selective attention Cohen, J.D., Dunbar, K., McClelland, J.L., 1990. On the control of automatic processes: a
deficits as vulnerability markers to psychosis. Eur. Psychiatry 22(3) parallel distributed processing account of the Stroop effect. Psychol. Rev. 97,
332–361.
171–176. Deeks, J.J., Higgins, J.P.T., Altman, D.G., 2008. Analysing data and undertaking meta-
analyses. In: Higgins, J.P.T., Green, S. (Eds.), Cochrane Handbook for Systematic
Nordahl, 2001: Nordahl, T. E., Carter, C. S., Salo, R. E., Kraft, L., Reviews of Interventions (Version 5.0.1). The Cochrane Collaboration www.
cochrane-handbook.org.
Baldo, J., Salamat, S., et al., 2001. Anterior cingulate metabolism
Egger, M., Davey Smith, G., Schneider, M., Minder, C., 1997. Bias in meta-analysis
correlates with stroop errors in paranoid schizophrenia patients. Neu- detected by a simple, graphical test. BMJ 315 (7109), 629–634.
ropsychopharmacology 25(1) 139–148. Fioravanti, M., Carlone, O., Vitale, B., Cinti, M.E., Clare, L., 2005. A meta-analysis of
cognitive deficits in adults with a diagnosis of schizophrenia. Neuropsychol. Rev.
15 (2), 73–95.
Perlstein 1998: Perlstein, W. M., Carter, C. S., Barch, D. M., Baird, Friedman, N.P., Miyake, A., 2004. The relations among inhibition and interference con-
J. W., 1998. The stroop task and attention deficits in schizophrenia: trol functions: a latent-variable analysis. J. Exp. Psychol. Gen. 133 (1), 101–135.
a critical evaluation of card and single-trial stroop methodologies. Golden, C.J., 1978. The Stroop Color Word Test. Stoelting Company, Chicago, IL.
Green, M.F., Kern, R.S., Braff, D.L., Mintz, J., 2000. Neurocognitive deficits and functional
Neuropsychology 12(3) 414–425. outcome in schizophrenia: are we measuring the “right stuff”? Schizophr. Bull.
26 (1), 119–136.
Rizzo 1996: Rizzo, L., Danion, J. M., VanderLinden, M., Grange, D., Harvey, P.D., Howanitz, E., Parrella, M., White, L., Davidson, M., Mohs, R.C., Hoblyn, J.,
Davis, K.L., 1998. Symptoms, cognitive functioning, and adaptive skills in geriatric
Rohmer, J. G., 1996. Impairment of memory for spatial context in patients with lifelong schizophrenia: a comparison across treatment sites. Am.
schizophrenia. Neuropsychology 10 376–384. J. Psychiatry 155 (8), 1080–1086.
Hedges, L.V., Olkin, I., 1985. Statistical Methods for Meta-analysis. Academic Press, New York.
Henik, A., Salo, R., 2004. Schizophrenia and the Stroop effect. Behav. Cogn. Neurosci.
Sacco 2006: Sacco, K. A., Termine, A., Dudas, M. M., Seyal, A. A., Rev. 3 (1), 42–59.
Allen, T. M., Vessicchio, J. C., et al., 2006. Neuropsychological deficits Henik, A., Carter, C.S., Salo, R., Chaderjian, M., Kraft, L., Nordahl, T.E., Robertson, L.C.,
in nonsmokers with schizophrenia: effects of a nicotinic antagonist. 2002. Attentional control and word inhibition in schizophrenia. Psychiatry Res.
110 (2), 137–149.
Schizophr. Res. 85(1–3) 213–221.
Hepp, H.H., Maier, S., Hermle, L., Spitzer, M., 1996. The Stroop effect in schizophrenic
patients. Schizophr. Res. 22 (3), 187–195.
Salo 2002: Salo, R., Henik, A., Nordahl, T. E., Robertson, L. C., 2002. Ikeda, Y., Hirata, S., Okuzumi, H., Kokubun, M., 2010. Features of Stroop and reverse-
Stroop interference: analysis by response modality and evaluation. Percept. Mot.
Immediate versus sustained processing in schizophrenia. J. Int.
Skills 110 (2), 654–660.
Neuropsychol Soc. 8(6) 794–803. Johnson-Selfridge, M., Zalewski, C., 2001. Moderator variables of executive functioning
in schizophrenia: meta-analytic findings. Schizophr. Bull. 27 (2), 305–316.
Salo 1997: Salo, R., Robertson, L. C., Nordahl, T. E., Kraft, L. W., Jurado, M.B., Rosselli, M., 2007. The elusive nature of executive functions: a review of
our current understanding. Neuropsychol. Rev. 17 (3), 213–233.
1997. The effects of antipsychotic medication on sequential inhibitory Kerns, J.G., Nuechterlein, K.H., Braver, T.S., Barch, D.M., 2008. Executive functioning
processes. J. Abnorm. Psychol. 106(4) 639–643. component mechanisms and schizophrenia. Biol. Psychiatry 64 (1), 26–33.
R. Westerhausen et al. / Schizophrenia Research 133 (2011) 172–181 181

Killian, G.A., Holzman, P.S., Davis, J.M., Gibbons, R.D., 1984. Effects of psychotropic Posner, M.I., Rothbart, M.K., 2007. Research on attention networks as a model for the
medication on selected cognitive and perceptual measures. J. Abnorm. Psychol. integration of psychological science. Annu. Rev. Psychol. 58, 1–23.
93 (1), 58–70. Redding, G.M., Gerjets, D.A., 1977. Stroop effect — interference and facilitation with
Kindt, M., Bierman, D., Brosschot, J.F., 1996. Stroop versus Stroop: comparison of a card verbal and manual responses. Percept. Mot. Skills 45 (1), 11–17.
format and a single-trial format of the standard color-word Stroop task and the Rosenberg, M.S., 2005. The file-drawer problem revisited: a general weighted method
emotional Stroop task. Pers. Individ. Differ. 21 (5), 653–661. for calculating fail-safe numbers in meta-analysis. Evolution 59 (2), 464–468.
Kopp, B., Mattler, U., Rist, F., 1994. Selective attention and response competition in Simpson, E.H., Kellendonk, C., Kandel, E., 2010. A possible role for the striatum in
schizophrenic-patients. Psychiatry Res. 53 (2), 129–139. the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 65 (5),
Lowe, D.G., Mitterer, J.O., 1982. Selective and divided attention in a Stroop task. Can. 585–596.
J. Psychol. 36 (4), 684–700. Stroop, J.R., 1935. Studies of interference in serial verbal reactions. J. Exp. Psychol. 18, 38–48.
MacLeod, C.M., 1991. Half a century of research on the Stroop effect: an integrative re- Takei, K., Yamasue, H., Abe, O., Yamada, H., Inoue, H., Suga, M., Muroi, M., Sasaki, H.,
view. Psychol. Bull. 109 (2), 163–203. Aoki, S., Kasai, K., 2009. Structural disruption of the dorsal cingulum bundle is as-
MacLeod, C.M., 2007. The concept of inhibition in cognition. In: Gorfein, D.S., MacLeod, sociated with impaired Stroop performance in patients with schizophrenia. Schi-
C.M. (Eds.), Inhibition in Cognition. American Psychological Association, Washing- zophr. Res. 114 (1–3), 119–127.
ton, DC, pp. 3–23. Tzelgov, J., Henik, A., Berger, J., 1992. Controlling Stroop effects by manipulating expec-
MacLeod, C.M., Bors, D.A., 2002. Presenting two color words on a single Stroop trial: ev- tations for color words. Mem. Cogn. 20 (6), 727–735.
idence for joint influence, not capture. Mem. Cogn. 30 (5), 789–797. Urbanek, C., Neuhaus, A.H.M., Opgen-Rhein, C., Strathmann, S., Wieseke, N., Schaub,
MacLeod, C.M., Hodder, S.L., 1998. Presenting two incongruent color words on a single R., Hahn, E., Dettling, M., 2009. Attention network test (ANT) reveals gender-
trial does not alter Stroop interference. Mem. Cogn. 26 (2), 212–219. specific alterations of executive function in schizophrenia. Psychiatry Res. 168,
Miller, E.K., Cohen, J.D., 2001. An integrative theory of prefrontal cortex function. Annu. 102–109.
Rev. Neurosci. 24, 167–202. van der Elst, W., van Boxtel, M.P., van Breukelen, G.J., Jolles, J., 2006. The Stroop color-
Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A., Wager, T.D., 2000. word test: influence of age, sex, and education; and normative data for a large
The unity and diversity of executive functions and their contributions to complex sample across the adult age range. Assessment 13 (1), 62–79.
“frontal lobe” tasks: a latent variable analysis. Cogn. Psychol. 41 (1), 49–100. van Mourik, R., Oosterlaan, J., Sergeant, J.A., 2005. The Stroop revisited: a meta-analysis
Nestor, P.G., Kubicki, M., Spencer, K.M., Niznikiewicz, M., McCarley, R.W., Shenton, M.E., of interference control in AD/HD. J. Child Psychol. Psychiatry 46 (2), 150–165.
2007. Attentional networks and cingulum bundle in chronic schizophrenia. Wang, K., Fan, J., Dong, Y., Wang, C.Q., Lee, T.M.C., Posner, M.I., 2005. Selective impair-
Schizophr. Res. 90 (1–3), 308–315. ment of attentional networks of orienting and executive control in schizophrenia.
Nigg, J.T., 2000. On inhibition/disinhibition in developmental psychopathology: views Schizophr. Res. 78 (2–3), 235–241.
from cognitive and personality psychology and a working inhibition taxonomy. Wapner, S., Krus, D.M., 1960. Effects of lysergic acid diethylamide, and differences be-
Psychol. Bull. 126 (2), 220–246. tween normals and schizophrenics on the Stroop Color-Word Test. J. Neuropsychi-
Perlstein, W.M., Carter, C.S., Barch, D.M., Baird, J.W., 1998. The Stroop task and attention atry 2, 76–81.
deficits in schizophrenia: a critical evaluation of card and single-trial Stroop meth-
odologies. Neuropsychology 12 (3), 414–425.

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