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Earthquake experience interference effects in a modified Stroop task: An ERP study
Neuroscience Letters 474 (2010) 121–125
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Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Earthquake experience interference effects in a modified Stroop task: An ERP study Dongtao Wei a,b , Jiang Qiu a,b,∗ , Shen Tu a,b , Fang Tian a,b , Yanhua Su a,b , Yuejia Luo c a b c
Key Laboratory of Cognition and Personality (SWU), Ministry of Education, Chongqing 400715, China School of Psychology, Southwest University, Chongqing 400715, China State Key Laboratory of Cognitive Neuroscience and Learning (BNU), Beijing, China
a r t i c l e
i n f o
Article history: Received 15 December 2009 Received in revised form 25 January 2010 Accepted 3 March 2010 Keywords: Stroop effect Cognitive control Event-related brain potentials (ERPs)
a b s t r a c t The effects of the modified Stroop task on ERP were investigated in 20 subjects who had experienced the Sichuan earthquake and a matched control group. ERP data showed that Incongruent stimuli elicited a more negative ERP deflection (N300–450) than did Congruent stimuli between 300 and 450 ms poststimulus in the earthquake group but not found in the control group, and the N300–450 might reflect conflict monitor (the information of color and meaning do not match) in the early phase of perception identification due to their sensitivity to the external stimulus. Then, Incongruent stimuli elicited a more negative ERP deflection than did Congruent stimuli between 450 and 650 ms post-stimulus in both the groups. Dipole source analysis showed that the N450–650 was mainly generated in the ACC contributed to this effect in the control group, which might be related to monitor and conflict resolution. However, in the earthquake group, the N450–650 was generated in the thalamus, which might be involved in inhibiting and compensating of the ACC which may be related to conflict resolution process. © 2010 Elsevier Ireland Ltd. All rights reserved.
Previous studies have shown that control mechanisms play an important role in the organization of action and thought, and the medial frontal cortex/anterior cingulate cortex (ACC) and the prefrontal cortex (PFC) play a critical role in the central executive control system [3,4,18]. The Stroop task is often selected as experimental paradigm to explore the nature of automatic and controlled cognitive processes [21,5,13]. The Stroop interference effect (or the Stroop effect) refers to an increase in response time observed when the word meaning of a color word and the printed color of the word do not match [22]. Measurement of ERP could provide good temporal resolution of neural activity. For example, Liotti et al. [13] found that a negative wave appeared over the medial dorsal region between 350 and 500 ms post-stimulus, with the peak at 410 ms. Dipole source analysis suggested that an independent generator present in the ACC was mainly related to conflict discovery and conflict resolution [13]. Qiu et al. also found that Incongruent condition elicited a much more negative deflection (N450) than did Congruent condition from 350 to 550 ms [20]. In a similar study, Xiao et al. [26] used a modified Stroop task in which the experimental materials are ordinary things with typical color in Chinese life most of the time. There were two kinds of stimuli, Congruent (font color is red and life color is red, font color is green and life color is green) and Incongruent (font color is red and life color is green, font color is
∗ Corresponding author at: School of Psychology, Southwest University, Beibei, Chongqing 400715, China. Tel.: +86 23 6836 7942. E-mail address: [email protected] (J. Qiu). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.03.005
green and life color is red). The results revealed that the Incongruent condition elicited more negative event-related potential deflections, N300 and N520, than the Congruent condition, which provide evidence for the dissociation of neural circuits between detection of interference and response inhibition in a Stroop task [26]. Moreover, the Stroop task and many modified versions of Stroop task have been utilized by researchers to explore the nature of automatic and controlled cognitive processes, disturbances in cognition resulting from various psychiatric and neurological disorders [7,24]. For example, Fehr et al. obtained EEG data during a color matching task using smoking related and neutral words (nicotine Stroop) in smokers and non-smoking controls, and found that a late relative positivity tending towards right frontal regions when word meanings were attributed to smoking related issues [7]. Recently, the events of great Sichuan earthquake (China) on May 12 (5/12), 2008, people who had experienced the great Sichuan earthquake (5/12) were selected as our subjects (a community sample), provide a unique window into the neural correlates of earthquake stressors exposure. As Basoglu et al. [2] also said that many people would find that their fear of earthquakes interferes with their everyday activities, including sleeping, bathing-even walking into a building. After the great Sichuan earthquake, many people might have developed post-traumatic stress disorder, which include obsession with the trauma, nightmares, flashbacks, memory problems and hypervigilance [2]. We predicted that the negative life events might have influence on cognitive and brain functions in people who had experienced the Sichuan earthquake.
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D. Wei et al. / Neuroscience Letters 474 (2010) 121–125
Therefore, in the present study, we selected 20 Chinese people who had experienced the Sichuan earthquake as the earthquake group (a community sample), 20 individuals without earthquake experience we selected as the control group. We used the modified Stroop task [including 20 words related to Sichuan earthquake] as the experimental paradigm to explore how personal earthquake experience impact on their cognitive control. Previous studies indicated that there were stress-related decreases in gray matter volume in the ACC and PFC in nonclinical samples [8,16] and stress-related alterations in medial PFC function [15]. Thus, we hypothesized that the negative life events might have significant influence on cognitive and brain functions in people of the community sample, and the earthquake-related information might be perceived more sensitively by the earthquake group than the control group. Specifically, we predicted that earthquake-related information would interfere with their judgments in the earthquake group, and this interference ERP effect would be related to a fronto-central relative negativity in the Incongruent compared to the Congruent stimuli but not be found in the control group. 27 adult subjects from Deyang city participated in the experiment as paid volunteers. They were asked to complete a self-report questionnaire: the post-traumatic stress disorder self-rating scale (PTSD-SS) [17]. The PTSD-SS was constructed based on the definition and diagnostic criteria of PTSD described in the Diagnostic and Statistical Manual of Mental Disorders: 4th Edition (DSM-IV), they thought that invidious who have got the total score below 60 have no serious PTSD symptom (Liu et al., 1998). According to their scores, 20 subjects who have got the total score below 60 were selected as the earthquake group (20 subjects: 10 women and 10 men; aged 18–23 years; mean age, 20.8 years; mean score: 40.3 ± 11.4). We know that Deyang is one of the three major cities immediately surrounding the earthquake’s epicenter (Wenchuan, approximately 60 miles). In the control group, 14 subjects (Chongqing city) without earthquake experience we selected as the control group (20 subjects: 10 women and 10 men; aged 18–23 years; mean age, 20.4 years). Subjects gave written informed consent, were right-handed, had no current or past neurological or psychiatric illness, and had normal or corrected-to-normal vision. The experimental materials consisted of two stimuli type [including 20 words related to Sichuan earthquake, e.g., blood, pumper] with two different colors (red or green). All the words were representative of ordinary things almost with a typical color (red or green) in Chinese life most of the time. These things often appeared in the earthquake (e.g., blood, pumper). Therefore, there were two stimulus types similar to the classical Stroop task: Congruent (font color is red and life color is red, font color is green and life color is green) and Incongruent (font color is red and life color is green, font color is green and life color is red). The size of the Chinese words was Song Ti No. 20 [1.6◦ (horizontal) × 0.8◦ (vertical)], and was displayed in the center of a 17-in. screen at random. Subjects were seated in a semi-dark room facing a monitor placed 60 cm from their eyes. They were instructed to rest their right index and right middle finger on the 1 and 2 on the keyboard, separately stood for Congruent and Incongruent stimuli. Subjects were told to respond as fast and accurately as possible (key press) to Congruent or Incongruent stimuli. The order as follows: each trial began with a fixation point ‘+’ that appeared for 300 ms in the center of the screen, the word appeared 1500 ms. The subjects performed a practice phase before the formal test. The formal test consisted of two blocks, and each block had 120 judgment trials (60 trials for each task, randomized). Subjects were instructed to avoid blinking or moving their eyes and to keep their eyes fixed on the monitor, rather than looking down at their fingers during task performance. They can take a rest after finishing one block. Brain electrical activity was recorded from 64 scalp sites using tin electrodes mounted in an elastic cap (Brain Product), with the
reference on the left and right mastoids. The vertical electrooculogram (VEOG) was recorded with electrodes placed above and below the left eye, and the horizontal electrooculogram (HEOG) with electrodes placed by right side of right eye and left side of left eye. All interelectrode impedance was maintained below 5 k. The EEG and EOG were amplified using a 0.05–80 Hz bandpass and continuously sampled at 500 Hz/channel for offline analysis. Eye movement artifacts (blinks and eye movements) were rejected offline. Trials with EOG artifacts (mean EOG voltage exceeding ±80 V) and those contaminated with artifacts due to amplifier clipping, bursts of electromyographic activity, or peak-to-peak deflection exceeding ±80 V were excluded from averaging. The averaged epoch for ERP was 900 ms including 800 ms poststimulus and 100 ms prestimulus. Of course, only segments with correct responses were averaged, and at least 40 trials were available for each subject. As observed in the grand-average waveforms and topographical map (see Fig. 1), the following 15 electrode points were chosen for statistical analysis: (F3, F4, Fz, FC3, FC4, FCz, C3, C4, Cz, CP3, CP4, CPz, P3, P4 and Pz). Latencies and amplitudes (baseline to peak) of the N1 and P2, were measured separately in the 80–130 ms, 150–200 ms time windows, respectively. Mean amplitudes in the time windows of 300–450 ms and 450–650 ms were analyzed using three-way repeated-measures analysis of variance (ANOVA), respectively. The ANOVA within-subjects factors were stimulus type (Congruent/Incongruent) and electrode site. Group (earthquake group and control group) was a between-subjects factor. For all analyses, p-values were corrected for sphericity assumption violations using the Greenhouse–Geisser correction. Brian Electrical Source Analysis (BESA, version, 5.0, software) was used to perform dipole source analysis. For dipole source analysis, the four-shell ellipsoidal head model was used. The BESA algorithm begins by placing a set of dipoles in an initial set of locations and orientations, with only the magnitude being unspecified. The algorithm then calculates a forward solution scalp distribution for these dipoles, computing a magnitude for each dipole at each point in time such that the sum of the dipoles yields a scalp distribution that fits, as closely as possible, the observed distribution for each point in time. The scalp distributions from the model are then compared with the observed scalp distributions at each time point to see how well they match. In order to focus on the scalp electrical activity related to the processing of the interference effect, the averaged ERPs evoked by Congruent stimuli were subtracted from the ERPs evoked by Incongruent stimuli. Principal component analysis (PCA) was employed in the time windows of 300–450 ms and 450–650 ms in order to estimate the minimum number of dipoles. When the dipole points are determined, software will automatically determine the dipoles location. The relevant residual variance (RV) criterion was used. The accuracy rates for Congruent and Incongruent stimuli were 80 ± 7.2% and 81 ± 9.2% in the earthquake group, respectively, in the control group, 75 ± 10.4% and 82 ± 6.7% for Congruent and Incongruent stimuli. The repeated-measures ANOVA for the mean accuracy rates revealed no interaction effect in stimuli type [F(1, 38) = 1.24, p > 0.05], and the main effect of group on accuracy was also not significant [F(1, 38) = 1.71, p > 0.05]. The mean reaction times (RTs) were 808 ± 93 ms for Congruent stimuli and 870 ± 98 ms for Incongruent stimuli in the earthquake group, and 870 ± 93 ms for Congruent stimuli and 910 ± 98 ms for Incongruent stimuli in the control group. The interaction between stimuli type × group was not significant [F(1, 38) = 1.61, p > 0.05], and the main effect of group on reaction time was also not significant [F(1, 38) = 3.06, p > 0.05]. As shown in Fig. 1, the N1 and P2 were elicited by two conditions. The results of the ANOVAs showed that there was no interaction effect between stimuli type × group for these components [F(1, 38) = 0.47, p > 0.05; F(1, 38) = 1.98, p > 0.05; F(1, 38) = 0.84,
D. Wei et al. / Neuroscience Letters 474 (2010) 121–125
p > 0.05; F(1, 38) = 0.97, p > 0.05]. The results indicated that early visual processing were similar between the stimuli type under the two conditions. Between 300 and 450 ms, the interaction between stimuli type × group was significant [F(1, 38) = 4.78, p < 0.05]. The results of a simple effect test showed that Incongruent elicited a more negative ERP deflection than did Congruent (Incongruent: 2.08 ± 0.76 V; Congruent: 3.71 ± 0.73 V in the earthquake group; Incongruent: 2.15 ± 0.76 V; Congruent: 2.57 ± 0.73 V in the control group). Between 450 and 650 ms there was no interaction effect between stimuli type × group [F(1, 38) = 0.06, p > 0.05], and there were main effects of stimuli type [F(1, 38) = 28.76, p < 0.001]. The results indicated that Incongruent elicited a more negative ERP deflection than did Congruent in both the groups. The source analysis using BESA software was, respectively, performed on the ERP difference wave of Incongruent and Congruent stimuli under two groups. PCA was employed in the 300–450 ms time window in the earthquake group. PCA indicated that one component was needed to explain 93.3% of the variance in the data. Therefore, one dipole was fitted with no restriction to the direction and location of dipole. The result indicated that this dipole located approximately in the caudate (location according Talairach coordinates: x = 10.5, y = 4.7, z = 5.0). This model explained the data best and accounted for most of the variance with RV of 13.2% and revealed maximal dipoles moment strength at about 397 ms. In addition, in the earthquake group, PCA indicated that one component was need to explain 96.6% of the variance in the 450–650 ms. The result indicated that this dipole located approximately in the thalamus (x = 17.8, y = −22.3, z = 3.3). This model explained the data best and accounted for most of the variance with RV of 4.1% and revealed maximal dipoles moment strength at about 520 ms. However, in the control group, PCA was employed in the time window of 450–650 ms. The result indicated that this dipole located approximately in the ACC (x = 23.4, y = −11.8, z = 34.2). This model explained the data best and accounted for most of the variance with RV of 12.1% and revealed maximal dipoles moment strength at about 570 ms. The display of the residual maps showed no further dipolar activity and no further dipoles could be fitted in the investigated time window.
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In the present study, the robust behavioral and electrophysiological effects of interference were obtained in the modified Stroop task. Incongruent stimuli elicited a more negative ERP deflection than did Congruent stimuli between 300 and 450 ms post-stimulus in the earthquake group but not found in the control group. Moreover, Incongruent stimuli elicited a more negative ERP deflection than did Congruent stimuli between 450 and 650 ms post-stimulus in both the groups. We would discuss the implication of these findings in the modified Stroop task (Fig. 2). First, in the earthquake group, the ERP data showed that Incongruent stimuli elicited a relative negativity in comparison to the Congruent stimuli (N300–450) between 300 and 450 ms poststimulus. We thought that the N300–450 might be similar to the N2 component. Previous studies [9,23] indicated that the N2 component might be related to conflict monitoring in the conflict tasks. For example, the amplitude of the enhanced when the flankers are mapped to a different response than the target item [23], they thought that the N2 was sensitive to the degree of conflict between response alternative. Kopp et al. indicated that N2 amplitude is increased on the Incongruent flanker condition than the Congruent flanker condition, they thought that the N2 possibly reflecting the inhibition of automatically [9]. In a similar study, Xiao et al. also found that Incongruent condition elicited a much more negative deflection (N300) than did Congruent stimuli from 350 to 450 ms, they indicated that N300 might reflect conflict monitor [26]. Moreover, dipole source analysis showed that the N300–450 was mainly generated in the caudate. Lawrence et al. [12] used functional MRI to reveal the neural substrates of nicotine’s effects on a sustained attention task. They thought that mildly abstinent smokers showed less task-induced brain activation in the parietal cortex and caudate than did nonsmokers [12]. Moreover, many psychopathology studies [6,10] had reported the thalamic pulvinar nucleus and caudate had also been linked to selective attention, they suggested that nicotine enhanced activation in these regions to facilitate the maintenance of alertness. Therefore, in our study, in comparison to the control group, after the great Sichuan earthquake, subjects who had experienced Sichuan earthquake were highly sensitive to earthquake-related information. Therefore, subjects might be interfered by the Incongruent stimuli in the early
Fig. 1. Grand-average ERP to Congruent and Incongruent stimuli at Fz, FCz, Cz and CPz in the two groups.
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Fig. 2. Results of the dipole source analysis of the difference wave (Incongruent vs. Congruent). The bottom left shows the source activity waveforms, whereas the right figure displays the mean locations of the dipole. Left: the dipole is located approximately in the caudate (x = 10.5, y = 4.7, z = 5.0) in the earthquake group in the time range of 350–450 ms. Middle: the dipole is located in the thalamus (x = 17.8, y = −22.3, z = 3.3) in the earthquake group in the time range of 450–650 ms. Right: results of the dipole source analysis of the difference wave (Incongruent vs. Congruent) in the control group in the time range of 450–650 ms. The dipole is located approximately in the ACC (x = 23.4, y = −11.8, z = 34.2).
phase of perception identification. Consequently, the N300–450 might reflect conflict monitor about the Incongruent stimuli of the earthquake-related information. Then, activation of the caudate might be related to the maintenance of an alert state. Second, our results also showed that Incongruent stimuli elicited a more negative ERP deflection (N450–650) than did Congruent stimuli in both the groups. To some extent, the interference ERP effect (N450–650) in our study was similar to previous findings [13,20,26,25]. For example, Liotti and Markela demonstrated two modulations of the ERPs that are consistently associated with conflict processing in the Stroop task: the N450 wave and the sustained potential [13]. Qiu et al. also found that Incongruent condition elicited a much more negative deflection than did Congruent stimuli from 350 to 550 ms [20]. Therefore, in the present study, we thought that the N450–650 might reflect conflict resolution process. Most important and interesting, in the control group, dipole source analysis showed that the N450–650 was mainly generated in the ACC. However, in the earthquake group, dipole source analysis showed that the N450–650 was mainly generated in the thalamus. Markela-Lerenc et al. indicated that the N400–650 interference effect was similar to the classical ERP Stroop interference effect which originated from activity generated in ACC [19]. The ACC may act in concert to detect dissociable forms of conflict [14]. Moreover, previous work had found that the ACC was mainly related to conflict discovery and conflict resolution when subjects performed the Stroop task [13,1]. In our study, subjects concentrated on the life color attribute and had to inhibit the interference of the font color attribute, therefore, activation of the ACC is required to control irrelevant information interference and make the right judgment according to the information of color. However, in the earthquake group, the N450–650 was mainly generated in the thalamus. Lanius et al. [11] suggested that the processing of executive control might be thought to involve cortical as well as thalamic brain areas, and thought that high levels of emotion experience altered thalamic sensory processing, and the transmission of sensory information to ACC might be interrupted in the PTSD. Lanius et al. also thought that abnormal functioning of the thalamus had significant effects on emotional behavior through its connections with ACC [11]. Moreover, many psychopathology studies [6,10] had reported the thalamic pulvinar nucleus and caudate had also been linked to selective attention, they suggested that nicotine enhanced activation in these regions to facilitate the maintenance of alertness during RVIP task performance. Therefore, in our study, N450–650 may reflect conflict resolution process in the earthquake group. After the great Sichuan earthquake, subjects concentrated on the life color attribute and had to inhibit the interference of the font color attribute, activation of the thalamus might be involved in inhibiting the anterior systems of executive control focused on the ACC and compensation of ACC which is related to control con-
flict resolution process. Therefore, we thought that the Sichuan earthquake might have significant influence on cognitive and brain functions in people of the community sample. In the present study, the ACC and the thalamus were activated by the modified Stroop task, as determined by the method of dipole source localization. However, it should be stressed that dipole source analysis is an inverse problem because there is no unique solution. Due to inherent limitations of source localization, the brain areas implicated by source localization are only tentative. Regarding the involvement of brain regions in response to the modified Stroop interference effect, the current results provide only a model rather than empirical data. To summarize, this study investigated spatiotemporal patterns of brain activation when 40 Chinese subjects (two community samples) performed the modified Stroop task using scalp and dipole source analysis of ERPs. The results showed that there were the N300–450 and N450–650 Stroop interference effect in both the groups, while the Stroop interference effect, respectively, elicited different regional activities of brain. Consistent with previous findings, our result indicated that the negative life events (Sichuan earthquake) might have significant influence on cognitive and brain functions in people of the community sample. Acknowledgements This research was supported by the Key Discipline Fund of National 211 Project, Funded by Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning. References [1] G. Badzakova-Trajkov, K.J. Barnett, K.E. Waldie, I.J. Kirk, An ERP investigation of the Stroop task: the role of the cingulate in attentional allocation and conflict resolution, Brain Research 1253 (2009) 139–148. [2] M. Basoglu, E. Salcioglu, M. Livanou, A randomised controlled study of singlesession behavioural treatment of earthquake-related posttraumatic stress disorder using an earthquake simulator, Psychological Medicine 37 (2007) 203–213. [3] M.M. Botvinick, T.S. Braver, C.S. Carter, D.M. Barch, Conflict monitoring and cognitive control, Psychological Review 108 (2001) 624–652. [4] C.S. Carter, T.S. Braver, D.M. Barch, M.M. Botvinick, D. Noll, J.D. Cohen, Anterior cingulate cortex, error detection, and the online monitoring of performance, Science 280 (1998) 747–749. [5] J.D. Cohen, K. Dunbar, J.L. McClelland, On the control of automatic processes: a parallel distributed processing account of the Stroop effect, Psychological Review 3 (1990) 332–361. [6] J.T. Coull, R.S. Frackowiak, C.D. Frith, Monitoring for target objects: activation of right frontal and parietal cortices with increasing time on task, Neuropsychologia 36 (1998) 1325–1334. [7] T. Fehr, P. Wiedenmann, M. Herrmann, Nicotine Stroop and addiction memory—an ERP study, International Journal of Psychophysiology 62 (2006) 224–232. [8] B.L. Ganzel, P. Kim, G.H. Glover, E. Temple, Resilience after 9/11: multimodal neuroimaging evidence for stress-related change in the healthy adult brain, NeuroImage 40 (2008) 788–795.
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Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Earthquake experience interference effects in a modified Stroop task: An ERP study Dongtao Wei a,b , Jiang Qiu a,b,∗ , Shen Tu a,b , Fang Tian a,b , Yanhua Su a,b , Yuejia Luo c a b c
Key Laboratory of Cognition and Personality (SWU), Ministry of Education, Chongqing 400715, China School of Psychology, Southwest University, Chongqing 400715, China State Key Laboratory of Cognitive Neuroscience and Learning (BNU), Beijing, China
a r t i c l e
i n f o
Article history: Received 15 December 2009 Received in revised form 25 January 2010 Accepted 3 March 2010 Keywords: Stroop effect Cognitive control Event-related brain potentials (ERPs)
a b s t r a c t The effects of the modified Stroop task on ERP were investigated in 20 subjects who had experienced the Sichuan earthquake and a matched control group. ERP data showed that Incongruent stimuli elicited a more negative ERP deflection (N300–450) than did Congruent stimuli between 300 and 450 ms poststimulus in the earthquake group but not found in the control group, and the N300–450 might reflect conflict monitor (the information of color and meaning do not match) in the early phase of perception identification due to their sensitivity to the external stimulus. Then, Incongruent stimuli elicited a more negative ERP deflection than did Congruent stimuli between 450 and 650 ms post-stimulus in both the groups. Dipole source analysis showed that the N450–650 was mainly generated in the ACC contributed to this effect in the control group, which might be related to monitor and conflict resolution. However, in the earthquake group, the N450–650 was generated in the thalamus, which might be involved in inhibiting and compensating of the ACC which may be related to conflict resolution process. © 2010 Elsevier Ireland Ltd. All rights reserved.
Previous studies have shown that control mechanisms play an important role in the organization of action and thought, and the medial frontal cortex/anterior cingulate cortex (ACC) and the prefrontal cortex (PFC) play a critical role in the central executive control system [3,4,18]. The Stroop task is often selected as experimental paradigm to explore the nature of automatic and controlled cognitive processes [21,5,13]. The Stroop interference effect (or the Stroop effect) refers to an increase in response time observed when the word meaning of a color word and the printed color of the word do not match [22]. Measurement of ERP could provide good temporal resolution of neural activity. For example, Liotti et al. [13] found that a negative wave appeared over the medial dorsal region between 350 and 500 ms post-stimulus, with the peak at 410 ms. Dipole source analysis suggested that an independent generator present in the ACC was mainly related to conflict discovery and conflict resolution [13]. Qiu et al. also found that Incongruent condition elicited a much more negative deflection (N450) than did Congruent condition from 350 to 550 ms [20]. In a similar study, Xiao et al. [26] used a modified Stroop task in which the experimental materials are ordinary things with typical color in Chinese life most of the time. There were two kinds of stimuli, Congruent (font color is red and life color is red, font color is green and life color is green) and Incongruent (font color is red and life color is green, font color is
∗ Corresponding author at: School of Psychology, Southwest University, Beibei, Chongqing 400715, China. Tel.: +86 23 6836 7942. E-mail address: [email protected] (J. Qiu). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.03.005
green and life color is red). The results revealed that the Incongruent condition elicited more negative event-related potential deflections, N300 and N520, than the Congruent condition, which provide evidence for the dissociation of neural circuits between detection of interference and response inhibition in a Stroop task [26]. Moreover, the Stroop task and many modified versions of Stroop task have been utilized by researchers to explore the nature of automatic and controlled cognitive processes, disturbances in cognition resulting from various psychiatric and neurological disorders [7,24]. For example, Fehr et al. obtained EEG data during a color matching task using smoking related and neutral words (nicotine Stroop) in smokers and non-smoking controls, and found that a late relative positivity tending towards right frontal regions when word meanings were attributed to smoking related issues [7]. Recently, the events of great Sichuan earthquake (China) on May 12 (5/12), 2008, people who had experienced the great Sichuan earthquake (5/12) were selected as our subjects (a community sample), provide a unique window into the neural correlates of earthquake stressors exposure. As Basoglu et al. [2] also said that many people would find that their fear of earthquakes interferes with their everyday activities, including sleeping, bathing-even walking into a building. After the great Sichuan earthquake, many people might have developed post-traumatic stress disorder, which include obsession with the trauma, nightmares, flashbacks, memory problems and hypervigilance [2]. We predicted that the negative life events might have influence on cognitive and brain functions in people who had experienced the Sichuan earthquake.
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Therefore, in the present study, we selected 20 Chinese people who had experienced the Sichuan earthquake as the earthquake group (a community sample), 20 individuals without earthquake experience we selected as the control group. We used the modified Stroop task [including 20 words related to Sichuan earthquake] as the experimental paradigm to explore how personal earthquake experience impact on their cognitive control. Previous studies indicated that there were stress-related decreases in gray matter volume in the ACC and PFC in nonclinical samples [8,16] and stress-related alterations in medial PFC function [15]. Thus, we hypothesized that the negative life events might have significant influence on cognitive and brain functions in people of the community sample, and the earthquake-related information might be perceived more sensitively by the earthquake group than the control group. Specifically, we predicted that earthquake-related information would interfere with their judgments in the earthquake group, and this interference ERP effect would be related to a fronto-central relative negativity in the Incongruent compared to the Congruent stimuli but not be found in the control group. 27 adult subjects from Deyang city participated in the experiment as paid volunteers. They were asked to complete a self-report questionnaire: the post-traumatic stress disorder self-rating scale (PTSD-SS) [17]. The PTSD-SS was constructed based on the definition and diagnostic criteria of PTSD described in the Diagnostic and Statistical Manual of Mental Disorders: 4th Edition (DSM-IV), they thought that invidious who have got the total score below 60 have no serious PTSD symptom (Liu et al., 1998). According to their scores, 20 subjects who have got the total score below 60 were selected as the earthquake group (20 subjects: 10 women and 10 men; aged 18–23 years; mean age, 20.8 years; mean score: 40.3 ± 11.4). We know that Deyang is one of the three major cities immediately surrounding the earthquake’s epicenter (Wenchuan, approximately 60 miles). In the control group, 14 subjects (Chongqing city) without earthquake experience we selected as the control group (20 subjects: 10 women and 10 men; aged 18–23 years; mean age, 20.4 years). Subjects gave written informed consent, were right-handed, had no current or past neurological or psychiatric illness, and had normal or corrected-to-normal vision. The experimental materials consisted of two stimuli type [including 20 words related to Sichuan earthquake, e.g., blood, pumper] with two different colors (red or green). All the words were representative of ordinary things almost with a typical color (red or green) in Chinese life most of the time. These things often appeared in the earthquake (e.g., blood, pumper). Therefore, there were two stimulus types similar to the classical Stroop task: Congruent (font color is red and life color is red, font color is green and life color is green) and Incongruent (font color is red and life color is green, font color is green and life color is red). The size of the Chinese words was Song Ti No. 20 [1.6◦ (horizontal) × 0.8◦ (vertical)], and was displayed in the center of a 17-in. screen at random. Subjects were seated in a semi-dark room facing a monitor placed 60 cm from their eyes. They were instructed to rest their right index and right middle finger on the 1 and 2 on the keyboard, separately stood for Congruent and Incongruent stimuli. Subjects were told to respond as fast and accurately as possible (key press) to Congruent or Incongruent stimuli. The order as follows: each trial began with a fixation point ‘+’ that appeared for 300 ms in the center of the screen, the word appeared 1500 ms. The subjects performed a practice phase before the formal test. The formal test consisted of two blocks, and each block had 120 judgment trials (60 trials for each task, randomized). Subjects were instructed to avoid blinking or moving their eyes and to keep their eyes fixed on the monitor, rather than looking down at their fingers during task performance. They can take a rest after finishing one block. Brain electrical activity was recorded from 64 scalp sites using tin electrodes mounted in an elastic cap (Brain Product), with the
reference on the left and right mastoids. The vertical electrooculogram (VEOG) was recorded with electrodes placed above and below the left eye, and the horizontal electrooculogram (HEOG) with electrodes placed by right side of right eye and left side of left eye. All interelectrode impedance was maintained below 5 k. The EEG and EOG were amplified using a 0.05–80 Hz bandpass and continuously sampled at 500 Hz/channel for offline analysis. Eye movement artifacts (blinks and eye movements) were rejected offline. Trials with EOG artifacts (mean EOG voltage exceeding ±80 V) and those contaminated with artifacts due to amplifier clipping, bursts of electromyographic activity, or peak-to-peak deflection exceeding ±80 V were excluded from averaging. The averaged epoch for ERP was 900 ms including 800 ms poststimulus and 100 ms prestimulus. Of course, only segments with correct responses were averaged, and at least 40 trials were available for each subject. As observed in the grand-average waveforms and topographical map (see Fig. 1), the following 15 electrode points were chosen for statistical analysis: (F3, F4, Fz, FC3, FC4, FCz, C3, C4, Cz, CP3, CP4, CPz, P3, P4 and Pz). Latencies and amplitudes (baseline to peak) of the N1 and P2, were measured separately in the 80–130 ms, 150–200 ms time windows, respectively. Mean amplitudes in the time windows of 300–450 ms and 450–650 ms were analyzed using three-way repeated-measures analysis of variance (ANOVA), respectively. The ANOVA within-subjects factors were stimulus type (Congruent/Incongruent) and electrode site. Group (earthquake group and control group) was a between-subjects factor. For all analyses, p-values were corrected for sphericity assumption violations using the Greenhouse–Geisser correction. Brian Electrical Source Analysis (BESA, version, 5.0, software) was used to perform dipole source analysis. For dipole source analysis, the four-shell ellipsoidal head model was used. The BESA algorithm begins by placing a set of dipoles in an initial set of locations and orientations, with only the magnitude being unspecified. The algorithm then calculates a forward solution scalp distribution for these dipoles, computing a magnitude for each dipole at each point in time such that the sum of the dipoles yields a scalp distribution that fits, as closely as possible, the observed distribution for each point in time. The scalp distributions from the model are then compared with the observed scalp distributions at each time point to see how well they match. In order to focus on the scalp electrical activity related to the processing of the interference effect, the averaged ERPs evoked by Congruent stimuli were subtracted from the ERPs evoked by Incongruent stimuli. Principal component analysis (PCA) was employed in the time windows of 300–450 ms and 450–650 ms in order to estimate the minimum number of dipoles. When the dipole points are determined, software will automatically determine the dipoles location. The relevant residual variance (RV) criterion was used. The accuracy rates for Congruent and Incongruent stimuli were 80 ± 7.2% and 81 ± 9.2% in the earthquake group, respectively, in the control group, 75 ± 10.4% and 82 ± 6.7% for Congruent and Incongruent stimuli. The repeated-measures ANOVA for the mean accuracy rates revealed no interaction effect in stimuli type [F(1, 38) = 1.24, p > 0.05], and the main effect of group on accuracy was also not significant [F(1, 38) = 1.71, p > 0.05]. The mean reaction times (RTs) were 808 ± 93 ms for Congruent stimuli and 870 ± 98 ms for Incongruent stimuli in the earthquake group, and 870 ± 93 ms for Congruent stimuli and 910 ± 98 ms for Incongruent stimuli in the control group. The interaction between stimuli type × group was not significant [F(1, 38) = 1.61, p > 0.05], and the main effect of group on reaction time was also not significant [F(1, 38) = 3.06, p > 0.05]. As shown in Fig. 1, the N1 and P2 were elicited by two conditions. The results of the ANOVAs showed that there was no interaction effect between stimuli type × group for these components [F(1, 38) = 0.47, p > 0.05; F(1, 38) = 1.98, p > 0.05; F(1, 38) = 0.84,
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p > 0.05; F(1, 38) = 0.97, p > 0.05]. The results indicated that early visual processing were similar between the stimuli type under the two conditions. Between 300 and 450 ms, the interaction between stimuli type × group was significant [F(1, 38) = 4.78, p < 0.05]. The results of a simple effect test showed that Incongruent elicited a more negative ERP deflection than did Congruent (Incongruent: 2.08 ± 0.76 V; Congruent: 3.71 ± 0.73 V in the earthquake group; Incongruent: 2.15 ± 0.76 V; Congruent: 2.57 ± 0.73 V in the control group). Between 450 and 650 ms there was no interaction effect between stimuli type × group [F(1, 38) = 0.06, p > 0.05], and there were main effects of stimuli type [F(1, 38) = 28.76, p < 0.001]. The results indicated that Incongruent elicited a more negative ERP deflection than did Congruent in both the groups. The source analysis using BESA software was, respectively, performed on the ERP difference wave of Incongruent and Congruent stimuli under two groups. PCA was employed in the 300–450 ms time window in the earthquake group. PCA indicated that one component was needed to explain 93.3% of the variance in the data. Therefore, one dipole was fitted with no restriction to the direction and location of dipole. The result indicated that this dipole located approximately in the caudate (location according Talairach coordinates: x = 10.5, y = 4.7, z = 5.0). This model explained the data best and accounted for most of the variance with RV of 13.2% and revealed maximal dipoles moment strength at about 397 ms. In addition, in the earthquake group, PCA indicated that one component was need to explain 96.6% of the variance in the 450–650 ms. The result indicated that this dipole located approximately in the thalamus (x = 17.8, y = −22.3, z = 3.3). This model explained the data best and accounted for most of the variance with RV of 4.1% and revealed maximal dipoles moment strength at about 520 ms. However, in the control group, PCA was employed in the time window of 450–650 ms. The result indicated that this dipole located approximately in the ACC (x = 23.4, y = −11.8, z = 34.2). This model explained the data best and accounted for most of the variance with RV of 12.1% and revealed maximal dipoles moment strength at about 570 ms. The display of the residual maps showed no further dipolar activity and no further dipoles could be fitted in the investigated time window.
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In the present study, the robust behavioral and electrophysiological effects of interference were obtained in the modified Stroop task. Incongruent stimuli elicited a more negative ERP deflection than did Congruent stimuli between 300 and 450 ms post-stimulus in the earthquake group but not found in the control group. Moreover, Incongruent stimuli elicited a more negative ERP deflection than did Congruent stimuli between 450 and 650 ms post-stimulus in both the groups. We would discuss the implication of these findings in the modified Stroop task (Fig. 2). First, in the earthquake group, the ERP data showed that Incongruent stimuli elicited a relative negativity in comparison to the Congruent stimuli (N300–450) between 300 and 450 ms poststimulus. We thought that the N300–450 might be similar to the N2 component. Previous studies [9,23] indicated that the N2 component might be related to conflict monitoring in the conflict tasks. For example, the amplitude of the enhanced when the flankers are mapped to a different response than the target item [23], they thought that the N2 was sensitive to the degree of conflict between response alternative. Kopp et al. indicated that N2 amplitude is increased on the Incongruent flanker condition than the Congruent flanker condition, they thought that the N2 possibly reflecting the inhibition of automatically [9]. In a similar study, Xiao et al. also found that Incongruent condition elicited a much more negative deflection (N300) than did Congruent stimuli from 350 to 450 ms, they indicated that N300 might reflect conflict monitor [26]. Moreover, dipole source analysis showed that the N300–450 was mainly generated in the caudate. Lawrence et al. [12] used functional MRI to reveal the neural substrates of nicotine’s effects on a sustained attention task. They thought that mildly abstinent smokers showed less task-induced brain activation in the parietal cortex and caudate than did nonsmokers [12]. Moreover, many psychopathology studies [6,10] had reported the thalamic pulvinar nucleus and caudate had also been linked to selective attention, they suggested that nicotine enhanced activation in these regions to facilitate the maintenance of alertness. Therefore, in our study, in comparison to the control group, after the great Sichuan earthquake, subjects who had experienced Sichuan earthquake were highly sensitive to earthquake-related information. Therefore, subjects might be interfered by the Incongruent stimuli in the early
Fig. 1. Grand-average ERP to Congruent and Incongruent stimuli at Fz, FCz, Cz and CPz in the two groups.
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Fig. 2. Results of the dipole source analysis of the difference wave (Incongruent vs. Congruent). The bottom left shows the source activity waveforms, whereas the right figure displays the mean locations of the dipole. Left: the dipole is located approximately in the caudate (x = 10.5, y = 4.7, z = 5.0) in the earthquake group in the time range of 350–450 ms. Middle: the dipole is located in the thalamus (x = 17.8, y = −22.3, z = 3.3) in the earthquake group in the time range of 450–650 ms. Right: results of the dipole source analysis of the difference wave (Incongruent vs. Congruent) in the control group in the time range of 450–650 ms. The dipole is located approximately in the ACC (x = 23.4, y = −11.8, z = 34.2).
phase of perception identification. Consequently, the N300–450 might reflect conflict monitor about the Incongruent stimuli of the earthquake-related information. Then, activation of the caudate might be related to the maintenance of an alert state. Second, our results also showed that Incongruent stimuli elicited a more negative ERP deflection (N450–650) than did Congruent stimuli in both the groups. To some extent, the interference ERP effect (N450–650) in our study was similar to previous findings [13,20,26,25]. For example, Liotti and Markela demonstrated two modulations of the ERPs that are consistently associated with conflict processing in the Stroop task: the N450 wave and the sustained potential [13]. Qiu et al. also found that Incongruent condition elicited a much more negative deflection than did Congruent stimuli from 350 to 550 ms [20]. Therefore, in the present study, we thought that the N450–650 might reflect conflict resolution process. Most important and interesting, in the control group, dipole source analysis showed that the N450–650 was mainly generated in the ACC. However, in the earthquake group, dipole source analysis showed that the N450–650 was mainly generated in the thalamus. Markela-Lerenc et al. indicated that the N400–650 interference effect was similar to the classical ERP Stroop interference effect which originated from activity generated in ACC [19]. The ACC may act in concert to detect dissociable forms of conflict [14]. Moreover, previous work had found that the ACC was mainly related to conflict discovery and conflict resolution when subjects performed the Stroop task [13,1]. In our study, subjects concentrated on the life color attribute and had to inhibit the interference of the font color attribute, therefore, activation of the ACC is required to control irrelevant information interference and make the right judgment according to the information of color. However, in the earthquake group, the N450–650 was mainly generated in the thalamus. Lanius et al. [11] suggested that the processing of executive control might be thought to involve cortical as well as thalamic brain areas, and thought that high levels of emotion experience altered thalamic sensory processing, and the transmission of sensory information to ACC might be interrupted in the PTSD. Lanius et al. also thought that abnormal functioning of the thalamus had significant effects on emotional behavior through its connections with ACC [11]. Moreover, many psychopathology studies [6,10] had reported the thalamic pulvinar nucleus and caudate had also been linked to selective attention, they suggested that nicotine enhanced activation in these regions to facilitate the maintenance of alertness during RVIP task performance. Therefore, in our study, N450–650 may reflect conflict resolution process in the earthquake group. After the great Sichuan earthquake, subjects concentrated on the life color attribute and had to inhibit the interference of the font color attribute, activation of the thalamus might be involved in inhibiting the anterior systems of executive control focused on the ACC and compensation of ACC which is related to control con-
flict resolution process. Therefore, we thought that the Sichuan earthquake might have significant influence on cognitive and brain functions in people of the community sample. In the present study, the ACC and the thalamus were activated by the modified Stroop task, as determined by the method of dipole source localization. However, it should be stressed that dipole source analysis is an inverse problem because there is no unique solution. Due to inherent limitations of source localization, the brain areas implicated by source localization are only tentative. Regarding the involvement of brain regions in response to the modified Stroop interference effect, the current results provide only a model rather than empirical data. To summarize, this study investigated spatiotemporal patterns of brain activation when 40 Chinese subjects (two community samples) performed the modified Stroop task using scalp and dipole source analysis of ERPs. The results showed that there were the N300–450 and N450–650 Stroop interference effect in both the groups, while the Stroop interference effect, respectively, elicited different regional activities of brain. Consistent with previous findings, our result indicated that the negative life events (Sichuan earthquake) might have significant influence on cognitive and brain functions in people of the community sample. Acknowledgements This research was supported by the Key Discipline Fund of National 211 Project, Funded by Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning. References [1] G. Badzakova-Trajkov, K.J. Barnett, K.E. Waldie, I.J. Kirk, An ERP investigation of the Stroop task: the role of the cingulate in attentional allocation and conflict resolution, Brain Research 1253 (2009) 139–148. [2] M. Basoglu, E. Salcioglu, M. Livanou, A randomised controlled study of singlesession behavioural treatment of earthquake-related posttraumatic stress disorder using an earthquake simulator, Psychological Medicine 37 (2007) 203–213. [3] M.M. Botvinick, T.S. Braver, C.S. Carter, D.M. Barch, Conflict monitoring and cognitive control, Psychological Review 108 (2001) 624–652. [4] C.S. Carter, T.S. Braver, D.M. Barch, M.M. Botvinick, D. Noll, J.D. Cohen, Anterior cingulate cortex, error detection, and the online monitoring of performance, Science 280 (1998) 747–749. [5] J.D. Cohen, K. Dunbar, J.L. McClelland, On the control of automatic processes: a parallel distributed processing account of the Stroop effect, Psychological Review 3 (1990) 332–361. [6] J.T. Coull, R.S. Frackowiak, C.D. Frith, Monitoring for target objects: activation of right frontal and parietal cortices with increasing time on task, Neuropsychologia 36 (1998) 1325–1334. [7] T. Fehr, P. Wiedenmann, M. Herrmann, Nicotine Stroop and addiction memory—an ERP study, International Journal of Psychophysiology 62 (2006) 224–232. [8] B.L. Ganzel, P. Kim, G.H. Glover, E. Temple, Resilience after 9/11: multimodal neuroimaging evidence for stress-related change in the healthy adult brain, NeuroImage 40 (2008) 788–795.
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