Psychiatry Research: 181 (2010) 24–29

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Psychiatry Research: Neuroimaging

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Color Stroop and negative in : An fMRI study

Lida Ungara, Paul G. Nestorb,c, Margaret A. Niznikiewiczb, Cynthia G. Wible b, Marek Kubickia,b,⁎ aPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, 1249 Boylston Street-3rd Floor, Boston, MA 02215, United States bClinical Neuroscience Division, Laboratory of Neuroscience, Boston VA Healthcare System-Brockton Division, Department of Psychiatry, Harvard Medical School, Brockton, MA 02301, United States cUniversity of Massachusetts Boston, 100 Morrissey Boulevard, Boston, MA 02125-3393, United States article info abstract

Article history: Disturbances in selective represent a core characteristic of schizophrenia, whose neural under- Received 17 January 2009 pinnings have yet to be fully elucidated. Consequently, we recorded brain activation using functional Received in revised form 14 May 2009 magnetic resonance imaging (fMRI) while 15 patients with schizophrenia and 15 age-matched controls Accepted 7 July 2009 performed a well-established measure of selective attention—the color Stroop task. We focused on two aspects of performance: overriding pre-potent responses () and inhibition of Keywords: prior negatively primed trials (negative priming effect). Behaviorally, controls demonstrated both significant fMRI Stroop and negative priming effects, while schizophrenic subjects only showed the Stroop effect. For the Color Stroop fi – Negative priming Stroop effect, fMRI indicated signi cantly greater activation in frontal regions medial frontal gyrus/anterior Schizophrenia cingulate gyrus and middle frontal gyrus for controls–but greater activation in medial parietal regions (posterior cingulate gyrus/precuneus) for patients. Negative priming elicited significant activation in right dorsolateral for both groups, but also in left dorsolateral prefrontal cortex for patients. These different patterns of fMRI activation may reflect faulty interaction in schizophrenia within networks of brain regions that are vital to selective attention. © 2009 Elsevier Ireland Ltd. All rights reserved.

1. Introduction patients with schizophrenia and healthy controls performed a Negative Priming (NP) Stroop Color Word test. The Stroop is a well- Founding figures of modern psychiatry, Kraepelin and Bleuler, each studied measure of selective attention in which the key stimulus items emphasized attentional disturbance as the “primary expression of the are color words (e.g., BLUE) that are printed in different color ink (e.g., schizophrenia patient's brain” (Heinrichs, 2005). More contemporary BLUE in RED ink). The classic Stroop response occurs when the times have seen the study of attention cast within the framework of the examinee is instructed to identify the color of ink (e.g., RED) of an burgeoning field of . In this framework atten- incongruent color word (e.g., BLUE). These incongruent trials impose tion represents a fundamental adaptation of the healthy brain that has heavy demands on selective attention, and elicit slower responses, evolved for the purposes of selecting salient information through both indicative of greater interference. In addition to these classic enhancement and suppression of neural activity associated with task- interference trials, the NP Stroop Color Word test also incorporates relevant and task-irrelevant representations (Gazzaley et al., 2005). incongruent trials that are negatively primed. A negatively primed This neural activity is coordinated and organized across networks of incongruent trial occurs when the ignored distracter, color name, in brain regions that traverse anterior cingulate cortex (ACC), dorsolat- the preceding trial becomes the target, color ink, in the subsequent eral prefrontal cortex (DLPFC), and medial and lateral parietal sites trial. This results in even slower response and greater interference for (Botvinick et al., 2001; Carter et al., 2001; Fan and Posner, 2004). negatively primed incongruent trials than for the classic, non- Schizophrenia may, in theory, compromise the efficiency and integrity negatively primed incongruent trials (e.g., MacLeod and MacDonald, of neural circuits underlying attentional selection, and this, in turn, 2000; MacQueen et al., 2003; van Veen, and Carter, 2005). might be expressed in widespread cognitive deficits. The current study aimed principally to examine, within and The current study used functional magnetic resonance imaging between patients and healthy controls, behavioral and neural (fMRI) to examine neural networks of selective attention while responses to these two kinds of incongruent trials. In imaging studies of healthy subjects, classic Stroop incongruent trials activate a well- specified, widely distributed network of brain regions of the medial ⁎ Corresponding author. Psychiatry Neuroimaging Laboratory, Department of frontal gyrus including the ACC, DLPFC and parietal cortex (Carter Psychiatry, Brigham and Women's Hospital, Harvard Medical School, 1249 Boylston et al., 1995; Gruber et al., 2002; Pardo et al.,1990). In addition, findings Street-3rd Floor, Boston, MA 02215, United States. Tel.: +1 617 525 6117; fax: +1 617 525 6150. from healthy subjects have revealed a particularly strong relationship E-mail address: [email protected] (M. Kubicki). of right DLPFC activation and negative priming (Egner and Hirsch,

0925-4927/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.pscychresns.2009.07.005 L. Ungar et al. / Psychiatry Research: Neuroimaging 181 (2010) 24–29 25

2005). For patients, behavioral studies have indicated greater Table 1 interference on the Stroop, as reflected by longer reaction times for Task design. incongruent trials (Barch et al., 2004; Hepp et al., 1996; Salo et al., 2002), which has been linked in fMRI studies to reduced activation within the ACC (Carter et al., 1997; Henik and Salo, 2004). To our knowledge, no fMRI studies have examined the NP Stroop condition in schizophrenia. However, behavioral studies have pointed to a very interesting pattern of findings in patients for negatively primed, incongruent trials on the Stroop test. That is, these data have indicated that whereas healthy controls show the expected negative priming effect of slowest response to these trials in which a previous distracter is now the target, patients with schizophrenia do not: that as the distractor (word text); in the incongruent condition, the target is, the data indicated significantly reduced negative priming, with the differed from the distracter. In our version of the experiment, in addition patients failing to show their slowest response for those trials in to standard stimuli congruency manipulation allowing us to estimate which a previous distracter is now the target (Laplante et al., 1992; the Stroop effect, we manipulated order of the incongruent stimuli, to MacQueen et al., 2003; Salo et al., 2002). estimate the negative priming effect. In the negative-priming condition, The precise basis for the disease-related reduction in negative the target of an incongruent trial became the distracter of an priming is still unclear. Behaviorally, many interpretations have immediately preceding incongruent trial. (Table 1) No color targets or emphasized negative priming abnormalities in schizophrenia as names were ever repeated in consecutive trials. Before the scanning, evidence of failures in selective attention, specifically in sustained each session started with detailed instructions where the subjects were inhibition over time (Laplante et al., 1992; MacQueen et al., 2003; Salo asked to identify the color in which the word was printed. Subjects were et al., 2002). For patients with schizophrenia, the extent, if any, to allowed a practice session, which was immediately followed by the which patterns of brain activation might differ as a function of type of experimental session. Response time and accuracy were recorded. The incongruent trial may enhance understanding of the role of failures of Stroop Effect was defined as the difference in the response times inhibition in the disease-related impairment of selective attention. between incongruent and congruent trials. Negative priming was Accordingly, then, in this article, we combine fMRI and the NP Stroop defined as the difference in response times for those incongruent test to examine the dynamics of selective attention in patient and primed trials in which the target (ink color of word) had been the control groups. We hypothesize that each of the incongruent trials will distracter (word name) in the preceding trial. The task was presented in be linked to differential brain activation within prefrontal regions. In four runs, each with 73 events that included 22 congruent trials and 51 particular, we predict that in relation to healthy controls, patients will incongruent trials (22 manipulated for negative priming). The inter-trial show reduced ACC activation for the classic Stroop incongruent trials interval (ITI) was jittered to be between 3 and 6 s (mean 4.4 s). Runs whereas negative priming trials will be related to aberrant DLPFC were different from each other, and their orders were counterbalanced activation. between subjects. The total length of the experiment was 22 min. The task was presented in four runs, each with 73 events that included 22 2. Methods congruent trials and 51 incongruent trials (22 manipulated for negative priming). The ITI was jittered to be between 3 and 6 s (mean 4.4 s). 2.1. Subjects Runs were different from each other, and their orders were counterbalanced between subjects. Fifteen male patients diagnosed with chronic schizophrenia, using DSM-IV criteria based on SCID-P interviews and a review of the 2.3. FMRI study medical records (mean age 43 (±7), mean age of onset 21.7 (±3.3), mean neuroleptic dose (mg/day in chlorpromazine equivalents 632 Imaging was performed using a 3-T whole body MRI Echospeed (±307)) and 15 male control subjects (mean age 43 (±6)) were system (General Electric Medical Systems, Milwaukee, WI). First a matched on gender (all male), handedness, PSES, and age. All subjects sagittal anatomical localizer image was acquired, and then the 134 EPI gave written informed consent prior to participation in the study, and BOLD scans (32 oblique coronal slices; 4 mm thick; TR 2.5 s; TE 30 ms; all were compensated for their time. Criteria for subjects' inclusion flip angle 90°) were acquired perpendicular to the AC–PC line. During were as follows: right-handedness, ages between 18 and 55 years, no scanning the subjects performed the negative-priming–color Stroop neurological illness, no alcohol or drug dependence in the last 5 years task. The first four scans of each run were discarded, and the rest were and no abuse in the past year. subjected to statistical analysis. Words within the scanner were presented to the subjects with MR- 2.2. Negative-priming color Stroop paradigm compatible visual goggles (Avotec, Inc., Florida, www.avotec.org) using Presentation software (version 0.76, build 11.30.03; Neurobe- The color Stroop/negative priming paradigm is a modified, compu- havioral Systems, www.neurobs.com). Responses were collected terized version of the single trial/event-related classic color Stroop using an MRI compatible fiber optic response four-button diamond paradigm, where color names compete and interfere with the incon- configuration pad (Current Designs Inc., Philadelphia, PA, www. gruent ink colors in which they are written. In our experiment, stimuli curdes.com. consisted of four color names (red, green, blue, or yellow) presented in Data were analyzed using Statistical Parametric Mapping (SPM2). one of these four colors (size 44 font) on a black background. Subjects Each subject's data were co-registered to the first scan of the first session were asked to report the color in which the word was written, by (in order to correct for head movement), normalized to the Montreal pressing the corresponding response button, ignoring the name of the Neurological Institute (MNI) template using a nonlinear, 12-parameter color itself. Each word (written in 44 Arial font against the black affine transformation registration, and smoothed with a 12-mm FWHM background, presented at the 5° angle) appeared centrally on a screen Gaussian filter. Activation maps using the General Linear Model (SPM2) until the subject responded, but not longer than the inter-trial interval including contrasts of tested conditions were constructed for each (ITI), which was jittered between 3 and 6 s (mean 4.4 s). A fixation point subject; where congruent and incongruent (for Stroop effect), as well as was present in the center of the screen any time a word was not being incongruent with and without negative priming (negative priming shown. In the congruent condition, the target (word color) was the same effect) conditions were first contrasted against each other on the subject 26 L. Ungar et al. / Psychiatry Research: Neuroimaging 181 (2010) 24–29 level (fixed effect contrast), and then subjected to the second level, significant activation in both the right and the left DLPFC (Brodmann random effect analysis on the group level. Another set of random effect area 6; Table 2, Fig. 2), while the healthy subjects only showed analyses compared separately Stroop as well as Negative Priming significant activation in the right DLPFC (Table 2, Fig. 3). contrasts between groups. Activation of control subjects and schizo- phrenia patients were subtracted from each other to identify differential 4. Discussion activation in both the Stroop (congruent vs. incongruent) and negative- priming (incongruent non-primed vs primed) conditions. Both whole We recorded patterns of fMRI brain activation while subjects brain analyses and ROI analyses (WFUPickAtlas SPM2 toolbox) that performed the NP version of the Stroop task. Behaviorally, both focused on the ACC and the DLPFC were performed, and statistical healthy control and patient groups showed the classic Stroop effect, as results were reported using the cluster level interference method reflected by slower reaction time for incongruent trials (e.g., name (statistical threshold (pb0.05) corrected for the number of continuous color font of the word RED printed in BLUE ink). The healthy control voxels, as implemented in SPM (Friston et al., 1995)). group also showed the expected negative priming effect of having their slowest responses to those incongruent trials for which the 3. Results distracter from the prior trial (e.g., color word RED) became the target (BLUE printed in RED ink) in the current trial. By contrast, the patient 3.1. Behavioral data group failed to show evidence of negative priming, as they did not have their slowest responses to negatively primed incongruent trials. There was no significant difference in overall response time bet- For the fMRI data, both types of incongruent trials–classic Stroop and ween the two groups (t=−1.162; df =28; p=0.260) with a mean negative primes–elicited different patterns of brain activation across response time of 1099.52 ms (±131.29 ms) for normal control subjects the two groups depending on whether the to-be-identified ink color and 1210.58 ms (±346.03 ms) for the schizophrenic subjects. The had been a distracter on the prior trial. mean difference in response times between congruent and incon- Most important, the current results pointed to group differences in gruent trials for normal control subjects was 111.39 ms (±47.06 ms) fMRI patterns activated by these different incongruent trials. First, and for schizophrenia patients was 122.74 ms (±71.22 ms). The mean beginning with the classic incongruent trials, in comparison to healthy difference in response times between the incongruent trials with the controls, the patients showed decreased activation in the ACC and negative priming manipulation and those without for the normal medial frontal gyrus, yet increased activation in medial parietal areas, control subjects was 30.62 ms (±50.62 ms) and for schizophrenic most notably the posterior cingulate gyrus. The decreased ACC subjects was 17.87 ms (±49.03 ms). activation is consistent with other studies of patients with schizo- Statistical tests revealed a strong main effect of Stroop interfer- phrenia (Carter et al., 1997; Henik and Salo, 2004), and increased ence (F (1, 34)=27.35, pb0.0001), and no group by condition inter- posterior cingulate gyrus/precuneus activation has also been reported action (F (1, 34)=0.54, pb0.47). For negative priming, there was a before, but with less consistency (Erkwoh et al., 2002; Gur et al., main effect of negative priming (F (1,34)=5.16, pb0.03), and a 2007). Together, these three regions are to represent key significant group by NP interaction (F (1,34)=5.65, pb0.023). The nodes in a prefrontal executive attention network that supports significant interaction effect indicated that whereas the control group critical cognitive functions of control and performance monitoring showed increased slowing for the negative priming trials, the patients that are thought to underlie and (Botvinick et al., did not. To follow up on the interaction effect, we have conducted 2001; Nestor et al., 2007). paired within-sample t-tests for each group for the NP effect. While Second, for negative priming trials, the fMRI findings indicated that normal controls showed a strong NP effect (pbt=−4.709, pb0.0001), schizophrenia patients showed activation in both the right and left the patient group did not show this effect (t=0.06, pb0.95). DLFPC, while healthy control subjects showed significant activation only in the right DLPFC. To the best of our knowledge, these data 3.2. Imaging data represent the first fMRI investigation of Stroop negative priming in schizophrenia, and thus cannot be directly compared with the earlier Schizophrenia patients showed less activation associated with the literature. However, for the healthy control group, the strong Stroop effect for incongruent trials that were not negatively primed relationship of right DLPFC activation and negative priming replicates than normal controls in the medial frontal gyrus/ACC as well as in the recent findings reported by Egner and Hirsch (2005). In addition, and middle frontal gyrus around the inferior frontal sulcus (Brodmann consistent with other behavioral studies (e.g., Salo et al., 2002), the area 9) (Table 2, Fig. 1), but showed greater activation in the medial patients in this investigation showed reduced negative priming; that parietal regions, which include the posterior cingulate and precuneus is, they showed less slowing in response times for distracter-turned- (Table 2, Fig. 1). For negative priming, schizophrenia patients showed target trials. These abnormalities of negative priming may reflect either a hypothesized disease-related reduction in the potency of distracter inhibition (May et al., 1995) or failure in implicit retrieval from a previous instance of a conflicting stimulus (Egner and Hirsch, Table 2 Results of fMRI analysis. 2005; Salo et al., 2002; Steel et al., 2001). Neither of these interpretations for the negative priming abnormalities of the patient Region MNI (x,y,z) Z score group can be ruled out by the experimental design of the current Stroop effect study. Control N Schizophrenia patients Both incongruent trials induce response competition, pitting the Medial frontal gyrus/ACC (4,44,24) 2.95 Right middle frontal lobe (42,18,32) 4.18 dominant and natural response of reading a color word against the Schizophrenia patients N control decidedly weaker and unnatural response of identifying the color of Posterior cingulate/precuneus (18,−78,24) 3.97 its font. Both trials require resolving competing and conflicting task demands for which the ACC of the prefrontal executive attention Negative priming Schizophrenia patient activation network is thought to play a particularly critical role. In addition, the Right DLPFC (26,0,56) 3.23 fMRI data suggested medial and dorsolateral prefrontal sites may Left DLPFC (−26,−8,56) 2.72 mediate negative priming. The fMRI findings that these two types of Control activation incongruent trials elicited differential brain activation may have Right DLPFC (30,6,58) 3.40 important functional significance. For example, simulation studies L. Ungar et al. / Psychiatry Research: Neuroimaging 181 (2010) 24–29 27

Fig. 1. Left panel–activation due to Stroop effect–ACG/medial frontal gyrus and right DLPFC activations in control subjects greater than in schizophrenia. Random effect group analysis (controls vs. schizophrenia patients) superimposed on single subject Talairach brain (provided by SPM2). Right panel–activation due to Stroop effect–posterior cingulate gyrus/ precuneus activations in schizophrenia subjects greater than in controls. Random effect group t-test (schizophrenia patients vs controls) results superimposed on single subject Talairach brain (provided by SPM2).

Fig. 2. Activation due to Negative priming in schizophrenia—right and left middle frontal gyrus. Group t-test results on single subject Talairach brain (provided by SPM2). 28 L. Ungar et al. / Psychiatry Research: Neuroimaging 181 (2010) 24–29

observed in our experiment in schizophrenia patients may reflect insufficient “suspension” of its baseline activity, either due to the impaired recruitment of brain systems required for target detection (Gur et al., 2007), or altered connectivity between anterior and posterior medial regions of the brain (Garrity et al., 2007). It is worth acknowledging that our study has multiple limitations–our population is chronic, medicated, and is limited to males only–thus results might not be easily generalized to the entire schizophrenia pop- ulation, and medication as well as age could be the additional confounds of the study results. Sample size is also relatively small (15 controls and 15 schizophrenia patients), although comparable with other published fMRI clinical studies. In summary, the study combined fMRI and the NP Stroop test in order to examine neural circuitry underlying selective attention in patients with schizophrenia. The results revealed a distinct pattern of behavioral response and brain activation for the patients in compar- ison to healthy controls, which suggested evidence of a specific impairment in selective attention in schizophrenia. We cannot, however, rule out the contribution of group differences in task strategy as contributing to the current results. Other limitations of the current study include the relatively small group sizes as well as that all patients were males with long histories of anti-psychotic medication prescribed for the treatment of their chronic schizophrenia. Future studies are needed to examine the robustness of these behavioral and brain abnormalities in selective attention and how they might be related to the core cognitive problem of the disease.

Acknowledgements

The authors acknowledge support from the National Institute of Health (R03 MH068464-01 to MK, R03 MH 078036 to MN, K05 MH070047, R01 MH 40799 to MN and MK and P50MH080272 (CIDAR Fig. 3. Activation due to negative priming in control subjects—right middle frontal gyrus. Award, CW, MN and MK), and the VA Schizophrenia Center Grant Group t-test results superimposed on single subject Talairach brain (provided by SPM2). (CW, MN). This work is also part of the National Alliance for Medical Image Computing (NAMIC), funded by the National Institutes of Health through the NIH Roadmap for Medical Research, Grant U54 EB005149 (MK). have suggested a similar division of labor of ACC-mediated monitoring and conflict resolution on one hand, and lateral prefrontal-mediated control and inhibition on the other hand (see Botvinick et al., 2001). References These simulations have revealed a prefrontal executive attention network that enables the ultimate selection of the weaker yet correct Barch, D.M., Carter, C.S., Cohen, J.D., 2004. Factors influencing Stroop performance in response of font color over the dominant but incorrect response of schizophrenia. 18 (3), 477–484. color word via coordinated activity of anterior cingulate and Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S., Cohen, J.D., 2001. Conflict moni- – prefrontal sites: as simulated, the anterior cingulate monitors toring and cognitive control. Psychological Review 108 (3), 624 652. Carter, C.S., MacDonald, A.W., Ross, L.L., Stenger, V.A., 2001. Anterior cingulate cortex performance, and then provides feedback for prefrontal sites for on- activity and impaired self-monitoring of performance in patients with schizophrenia: line adjustments in control and inhibition (Botvinick et al., 2001). an event-related fMRI study. American Journal of Psychiatry 158 (9), 1423–1428. Thus, for patients with schizophrenia, their abnormal patterns of Carter, C.S., Mintun, M., Cohen, J.D., 1995. Interference and facilitation effects during selective attention: an H215O PET study of Stroop task performance. NeuroImage fMRI activation for these incongruent trials may signify disease- 2(4),264–272. related disturbance in a prefrontal executive attention network. Carter, C.S., Mintun, M., Nichols, T., Cohen, J.D.,1997. Anterior cingulate gyrus dysfunction Moreover, these imaging results conform well with recent structural and selective attention deficits in schizophrenia: [15O]H2O PET study during single- trial Stroop task performance. American Journal of Psychiatry 154 (12), 1670–1675. evidence of abnormalities in the cingulum bundle, a key white matter Cavanna, A.E., Trimble, M.R., 2006. The precuneus: a review of its functional anatomy tract connecting the anterior cingulate to other frontal sites of the and behavioural correlates. Brain 129 (Pt 3), 564–583. executive attention network (Kubicki et al., 2003). Consistent with the Egner, T., Hirsch, J., 2005. Where memory meets attention: neural substrates of negative fi priming. Journal of Cognitive Neuroscience 17 (11), 1774–1784. current ndings, these structural abnormalities have in turn corre- Erkwoh, R., Sabri, O., Schreckenberger, M., Setani, K., Assfalg, S., Sturz, L., Fehler, S., lated with poorer performance on neuropsychological measures of Plessmann, S., 2002. Cerebral correlates of selective attention in schizophrenic attention in patients with chronic schizophrenia (Nestor et al., 2004; patients with formal thought disorder: a controlled H2 15O-PET study. Psychiatry – Nestor et al., 2007). In addition, for the patient group, incongruent Research 115 (3), 137 153. Fan, J., Posner, M., 2004. Human attentional networks. Psychiatry Praxis 31, S210–S2104 trials elicited a relative increase in activity in the medial parietal Suppl 2. cortex (posterior cingulate/precuneus) that was not observed in Friston, K., Holmes, A., Worsley, K.J., Poline, J.P., Frith, C.D., Frackowiak, R.S.J., 1995. healthy controls. These regions have been theorized to be involved in Statistical parametric maps in functional imaging: a general linear approach. Mapping 2, 189–210. conscious awareness (Cavanna and Trimble, 2006; Vogt and Laureys, Garrity, A.G., Pearlson, G.D., McKiernan, K., Lloyd, D., Kiehl, K.A., Calhoun, V.D., 2007. 2005), and as part of the “default network” have shown metabolic Aberrant “default mode” functional connectivity in schizophrenia. American activation during rest, and relative decrease of activation during goal- Journal of Psychiatry 164 (3), 450–457. Gazzaley, A., Cooney, J.W., McEvoy, K., Knight, R.T., D Esposito, M., 2005. Top-down directed action in healthy controls (Greicius et al., 2003; Gusnard et enhancement and suppression of the magnitude and speed of neural activity. al., 2001). A relative increase in the activity within this region Journal of Cognitive Neuroscience 17 (3), 507–517. L. Ungar et al. / Psychiatry Research: Neuroimaging 181 (2010) 24–29 29

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