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Electrophysiological evidence of personal experiences in the great Sichuan earthquake impacting on selective attention QIU Jiang1,2, LI Hong1,2, ZHANG QingLin1,2,†, HUANG LiHui2, GUO YaQiao2, TU Shen2, WANG Ting2 & WEI DongTao2 1 2

Key Laboratory of Cognition and Personality (SWU), Ministry of Education, Chongqing 400715, China; School of psychology, Southwest University, Chongqing 400715, China

Event-related brain potentials (ERPs) were measured when 24 Chinese subjects performed the earthquake color-matching Stroop task. All of them have experienced the great Sichuan earthquake (5.12), with 12 subjects in each of Chengdu city and Chongqing city (different earthquake experiences) groups. The behavioral data showed that the earthquake Stroop task yielded robust the earthquake interference effect as indexed by longer RT for earthquake-related (Related) words than earthquake-unrelated (Unrelated) words only in the Chengdu group. Scalp ERP analysis also revealed the neurophysiological substrate of the interference effect: a greater positivity (P350—450) in Related words as compared to Unrelated words was found between 350 and 450 ms post-stimulus over fronto-central scalp regions in the Chengdu group, while the interference effect was not found in the Chongqing group. The P350—450 might reflect an earthquake experience interference, but also attention enhancing, effect of earthquake-related words. Dipole source analysis of the difference wave (Related–Unrelated) showed that a generator was localized in the parahippocampal gyrus, which was possibly associated with flashbulb memory (personal earthquake experience). The results indicated that different personal earthquake experiences might be critical in engaging the neural mechanisms that underlie the modulation of selective attention. Sichuan earthquake, Stroop effect, selective attention, event-related potentials (ERPs)

1 Introduction Selectivity is the ability to not only focus attention on relevant information but also inhibit irrelevant information processing[1,2]. Selection capacity can ensure that behavior is controlled by relevant information. In the previous studies[3−5], a variety of selective attention tasks have been used, in which subjects were instructed to focus on certain specific relevant elements of stimuli while ignoring irrelevant information, for example, the classic Stroop task which tests the ability to focus on a relevant stimulus attribute (word color) while ignoring an irrelevant one (word meaning)[6]. Generally, the Stroop interference effect refers to an

increase of response times observed when the word meaning and the stimulus hue do not match (incongruent condition, i.e., the word “green” presented in the color red) relative to when they correspond (congruent condition, i.e., the word “red” presented in the color red[6]. The Stroop task and many modified versions of the Stroop task have been utilized by researchers to explore the nature of automatic and controlled cognitive processes[7,8], disturbances in cognition resulting from variReceived November 27, 2008; accepted February 13, 2009 doi: 10.1007/s11427-009-0076-6 † Corresponding author (email:[email protected]) Supported by the National Natural Science Foundation of China (Grant No. 30800293), the Key Project of Philosophy and Social Science of Chinese Ministry of Education (Grant No. 08JZD0026), and the Southwest University Doctoral Fund.

Citation: QIU J, LI H, ZHANG Q L, et al. Electrophysiological evidence of personal experiences in the great Sichuan earthquake impacting on selective attention. Sci China Ser C-Life Sci, 2009, 52(7): 683-690, doi: 10.1007/s11427-009-0076-6

ous psychiatric and/or neurological disorders[9], the neuro-cognitive architecture of selective attention[10], and age-related declines in inhibitor processing[11]. For example, Fehr et al.[12] 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 tends towards right frontal regions when word meanings were attributed to smoking-related issues. They indicated that this ERP component might reflect a modulation of brain activity in smokers due to smoking-related word contents. In another study, Bar-Haim et al.[13] also found that anxious individuals are typically slower to name the colors of threat-related words than of neutral words in their modified emotional version of the Stroop task, and high-anxious participants showed higher amplitudes of the P2 component to angry faces. Recently, Goldstein et al.[14] used a novel color-word drug Stroop task (subjects had to press for color of drug vs. matched neutral words) in drug-addicted subjects, and suggested the unique drug-related brain-behavior associations at the individual level. These previous studies have provided evidence that the effects of drug-addiction on the central nervous system may extend from conscious to unconscious processes in cognition[12,14,15−18]. Recently, the events of the great Sichuan earthquake on May 12, 2008, and the experiences of the people who were in close proximity to that disaster (e.g., Chengdu city) provide a unique window into the neural correlates of earthquake stressors exposure. After the great Sichuan earthquake, many people will have longer-term problems, which include obsession with the trauma, nightmares, flashbacks, emotional numbing, loss of interest in life, irritability, memory problems and hyper-vigilance. As Basoglu et al.[19] said, many people will find that their fear of earthquakes interferes with their everyday activities, including sleeping, bathing-even walking into a building. Up to now, many fMRI studies have found that increased activity in the amygdala is the most consistently observed neural correlate of posttraumatic stress disorder (PTSD), with some evidence that this activation is localized to subregions of the amygdala and is associated with alterations in medial prefrontal activity[20−24]. However, as Ganzel et al.[25] and Dohrenwend[26] said, “there has been very little work examining the neural correlates of trauma exposure in people without a clinical disorder; this is surprising, considering the known impact of 684

negative life events on psychological distress and disorder in the overall population”. Therefore, in the present study, we devised a modified earthquake color-matching Stroop task to investigate how personal experience modulates the neural circuitry of selective attention by using ERPs. It is known that ERPs may provide a means to evaluate timing of cognitive processes prior to a response. In the ERP technique, recordings are made of the electrical activity of the brain that is time locked to the presentation of an external stimulus. Thus, ERP data provide additional metrics to assess where in the information processing sequence earthquake experiences affect cognition. In general, the P300 amplitude reflects the amount of attentional resources employed in a given task, and provides information about differing amounts of mental effort required for various color/meaning pairings. The P300 ERP can provide considerable insight into Stroop interference because it provides independent measures of stimulus evaluation time and attentional requirements[27,28]. In addition, the P300 latency has been shown to vary with the duration of perceptual processes, but is insensitive to the duration of motor processes[28]. That is, the P300 ERP may be used to test whether the Stroop interference effect originates from response- or stimulus-related processing. Based on previous studies[12−14,22−24], we hypothesized that earthquake-related word meanings would interfere with color matching, and that this should be reflected in an ERP activation pattern comparable to previous findings by the Stroop task. Specifically, the earthquake interference effect of longer reaction times in the Related word condition could be observed. This interference effect would be related to an early posterio-central relative negativity and a late frontal relative positivity in Related words compared to the Unrelated condition. In addition, this study would explore whether different earthquake experiences (the Chengdu city group and the Chongqing city group) have different influence on cognitive functions (e.g., selective attention, memory, cognitive control) in people without a clinical disorder.

2 Materials and methods 2.1 Subjects Approximately one month after the Sichuan earthquake, twelve undergraduates (6 females, 6 males) aged 19−24 years (mean age, 22.5 years) from Sichuan Normal

QIU Jiang et al. Sci China Ser C-Life Sci | Jul. 2009 | vol. 52 | no. 7 | 683-690

University in Chengdu city participated in the experiment as paid volunteers. All of them had experienced the Sichuan earthquake (on Monday, 12 May, 2008). There were cracks on walls of some residential buildings in the downtown areas in Chengdu city. In addition, twelve healthy undergraduates (7 women, 5 men) aged 22−28 years (mean age, 24.5 years) from Southwest University in Chongqing city also participated in the experiment as a control group. Chongqing city, 370 km away from the source, only rocked in the earthquake with no building collapsed. All 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. 2.2 Stimuli and procedure The experimental materials consisted of two kinds of different stimuli (including 35 words related or unrelated to the Sichuan earthquake tragedy, e.g., 余震(artershock), 跨塌 (collapse); 风筝 (kite), 钓鱼 (fishing)) with two different colors (including red and green). Each word included two Chinese characters, and there were no significant differences for the main characteristics of these stimuli (e.g., mean stroke and frequency). 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-inch 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 red and green color, and the stimulus-response key assignments were counterbalanced across subjects. They were told that a grey cross would always appear first in the center of the screen serving as a fixation point, and then one word written in different colors. The order is as follows: the fixation point appeared at 300 ms, and the word appeared at 1500 ms. Subjects were asked to ignore the meaning of the words and identify the color in which the stimulus was written as fast and accurately as possible and responded by pressing the button of the corresponding color. The experiment was divided into a practice phase and a test phase. The practice phase was designed to rehearse the mapping of colors onto fingers and pressing of the response buttons. When the participant was familiar with the procedure of the experiment, the practice phase was ended. The formal test consisted of three blocks, and every block had 60 judgment trials

(30 Related color words and 30 Unrelated color words, randomized). In each block, one Related or Unrelated word did not appeare repeatedly. Subjects were instructed to avoid blinking and eye movement of any sort and to keep their eyes fixated on the monitor rather than looking down at their fingers during task performance. They were able to rest after finishing each block. 2.3 Electrophysiological recording and analysis Brain electrical activity was recorded from 64 scalp sites using tin electrodes mounted in an elastic cap (BrainVision: Brain Products GmbH, Gilching, Germany), 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 the right side of the right eye and the left side of the left eye. All interelectrode impedance was maintained below 5 kΩ. The EEG and EOG were amplified using a 0.05— 80 Hz bandpass and continuously sampled at 500 Hz/ channel for off-line analysis. Eye movement artifacts (blinks and eye movements) were rejected offline. Trials with EOG artifacts (mean EOG voltage exceeding ± 80 μV) and those contaminated with artifacts due to amplifier clipping, bursts of electromyographic activity, or peak-to-peak deflection exceeding ±80 μV were excluded from averaging. The averaged epoch for ERP was 600 ms, including 500 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, condition. On the basis of the ERPs grand averaged waveforms and topographical map (Figure 1 and 2), the following 17 electrode points were chosen for statistical analysis: AF3, AF4, F3, Fz, F4, FC3, FCz, FC4, C3, Cz, C4, CP3, CPz, CP4, P3, Pz, P4. The ANOVA factors were the task type (two levels: Related words and Unrelated words) and the electrode site, and the earthquake experience (Chengdu city and Chongqing city) was a between-subjects factor. For all analyses, P-value was corrected for deviations according to Greenhouse Geisser. 2.4 Dipole source analysis Brain Electrical Source Analysis program (BESA: MEGIS Software GmbH, Graefelfing, Germany) was used to perform dipole source analysis. For dipole source analysis, the four-shell ellipsoidal head model


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was used. In order to focus on the scalp electrical activity related to the processing of the earthquake interference effect, the averaged ERPs evoked by Unrelated words were subtracted from the ERPs evoked by Related words in the Chengdu group. Principal component analysis (PCA) was employed at the interval from 350 to 450 ms in order to estimate the minimum number of dipoles. We know that PCA is a comprehensively studied, ‘data driven’ technique, and its applicability to electroencephalographic (EEG) data has been acknowledged widely among researchers. PCA utilizes all the information from 64 channels, and is thereby able to identify components not necessarily even visible in the grand averages of ERP data. When the dipole points are determined, software will automatically determine the dipoles location. The relevant residual variance criterion was used.

3 Results 3.1 Behavioral data In the mean reaction time analysis, the ANOVA revealed a significant task type × earthquake experience effect (F(1,22) = 6.90, P < 0.05). The simple effect test showed that a very robust earthquake interference effect was obtained as indicated by longer mean RTs for Related words (464 ± 17) than Unrelated words (423 ± 13) in the Chengdu group. In addition, the accuracy rates for

Figure 1 686

Related words and Unrelated words were (97.8 ± 0.6)% and (97.0 ± 0.7)%, respectively, in the Chengdu group, and (98.5 ± 1.1)% and (98.3 ± 2.4)%, respectively, in the Chongqing group. The repeated-measures ANOVA for the mean accuracy rates revealed no significant differences between Related and Unrelated words (F(1,22) = 0.84, P > 0.05), and there was also no significant task type × earthquake experience effect (F(1,22) = 0.34, P > 0.05). 3.2 Electrophysiological scalp data The grand-average waveforms and topographic maps of difference wave Related vs. Unrelated showed the following spatiotemporal distribution for the ERP data (Figures 1 and 2). As shown in Figure 2, N100 and P160 were elicited by two conditions. Latencies and amplitudes (baseline to peak) of the anterior N100 and P160 were measured separately in the 80—120 ms and 130— 180 ms time windows, respectively. However, the results of the ANOVAs showed that there were no main effects of the task type and earthquake experience for these components. The results indicated that early visual processing was similar between the two conditions (Related and Unrelated) for the N100 and P160 ERP wavelengths. A greater positivity to Related than to Unrelated in the 350−450 ms time window over fronto-central scalp regions was mainly observed. Mean amplitudes in the

Grand average ERP to Related, Unrelated conditions at Fz, FCz, CPz and Pz in the Chengdu and the Chongqing groups. QIU Jiang et al. Sci China Ser C-Life Sci | Jul. 2009 | vol. 52 | no. 7 | 683-690

time window of 350−450 ms were analyzed using threeway repeated-measures ANOVAs. Results showed that there was a significant task type × earthquake experience effect (F(1,22) = 4.51, P < 0.05). The results of a simple effect test showed that Related words elicited a more positive ERP deflection than did Unrelated words (Related words: (8.01 ± 1.61) μV; Unrelated words: (5.26 ± 1.52) μV) in the Chengdu group. However, there was no difference between Related and Unrelated words in the Chongqing group (Related words: (5.64 ± 1.25) μV; Unrelated words: (5.71 ± 1.37) μV). In addition, the interaction task type and the electrode site were not significant, F(16,176) = 1.24, P > 0.05. 3.3 Dipole source analysis The source analysis using BESA software was performed on the ERP difference wave of Related and Unrelated conditions. PCA was employed in the 350−450 ms time window. PCA indicated that one principal component was needed to explain 97.4% 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 was located approximately in the parahippocampal gyrus (location according to Talairach coordinates: x = −19.1, y = 0.6, z = −16.6) and revealed the maximal dipole moment strength at about 390 ms. This model explained the data best and accounted for most of the variance with a residual variance (RV) of 12.8% at the peak activity of this dipole ( Figure 3). The display of the residual maps showed no further dipolar activity and no further dipoles could be fitted in the investigated time window.

4 Discussion In the present study, robust behavioral and electrophysiological effects of earthquake interference were seen in Chengdu subjects performing the earthquake color-matching Stroop task. Behavioral data showed the longer RT for Related words than Unrelated words in the Chengdu group. Most important and interesting, a greater positivity (P350—450) in Related as compared to Unrelated words was also found between 350 and 450 ms post-stimuli over fronto-central scalp regions. In addition, dipole source analysis of the difference wave (Related-Unrelated) found that a generator localized in the parahippocampal gyrus contributed to this effect. We would discuss the implication of these findings in the earthquake color-matching Stroop task in the Chengdu group. Previous studies (e.g., West and Alain[29]; Liotti et al.[30]; Wes[31]; Markela-Lerenc et al[32]; Qiu et al.[33]) mainly demonstrated two modulations of the ERPs that are consistently associated with conflict processing in the Stroop task (i.e. N450 and sustained potential)[29−33]. The N450 peaks between 400 and 500 ms after stimulus onset and reflects a phasic frontocentral negativity that differentiates incongruent trials from neutral trials. This ERP component seems to be related to response detection and may arise from the activity in prefrontal areas. The sustained potential is elicited about 500 ms after stimulus onset and reflects a sustained parietal positivity-lateral frontal negativity. Activity of the neural generator of the sustained potential was reported in lateral-frontal and extrastriate areas. However, in the

Figure 2 Topographical maps of the voltage amplitudes for Related vs. Unrelated condition difference wave at 380 ms, 400 ms and 420 ms at Fz in the Chengdu group.


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Figure 3 Results of the dipole source analysis of the difference wave (Related vs. Unrelated) in the Chengdu group. D, The source activity waveforms, whereas the right figure displays the mean locations of the dipole. The dipole is located approximately in the parahippocampal gyrus (x=−19.1, y=0.6, z=−16.6).

present study, we found that Related words elicited a more positive ERP deflection (P350—450) than did Unrelated words between 350—450 ms over frontocentral scalp regions in Chengdu city. This result was not consisent with previous findings (e.g., the distinct N450 Stroop interference effect, see Liotti et al.[30]; Qiu et al.[33]). We thought that the P350-450 earthquake interference effect might not reflect conflict processing and response selection. Observing from the ERPs grand averaged waveforms, we found that the P350—450 was actually the third positive component in the waveform, and it therefore might be an P300 component [28,34]. Previous studies have indicated that the P300 is often linked to memory updating, encoding, or retrieval, given their appearance in tasks making demands on stimulus evaluation and memory updating resources[28,34]. In fact, our behavioral result was similar to the findings of several clinical studies, indicating that individuals across different clinical populations were significantly slower in responding to stimuli idiosyncratic to their respective disease when they performed the different versions of the Stroop task. Our ERP result was also consistent with these studies[12,35,36]. Warren and McDonough[35] reported that smokers showed a relatively high P412 amplitude being confronted with smoking-related pictures, and thought that the smokers’ P412 to smoking-related stimuli appeared to reflect the action of an automatic process which locks-in on salient stimuli (smoking-related pictures). In Franken’s study, cocaine as well as heroin addicts showed an augmented late slow positive wave when presenting substance-related pictures[36]. 688

He indicated that the augmented late slow positive wave might reflect motor preparation and a hyperattentive state towards drug-related stimuli. Fehr et al. also found that smokers in contrast to controls showed a frontal relative positivity during time windows between 200 and 500 ms, and suggested that the frontal positivity, which was modulated by the stimuli, might be related to interference resolution processes (smoking-related word meanings would interfere with color matching), induced by words associated with addiction memory contents[12]. In our study, subjects were required to ignore the meaning of the word and judge the color in which the word was written as fast as possible. Although we found that there was a very robust earthquake interference effect, there was seemingly no any cognitive conflict (e.g., the word color-meaning conflict in the Stroop task) in performing the earthquake Stroop task. When Related words appeared, subjects could not inhibit irrelevant information processing (e.g., earthquake-related word meanings would interfere with color matching) effectively, thus Related words elicit greater mobilization of attentional resources than did Unrelated words. The increased RT might be explained by impairment in involuntary attention controlling. Therefore, based on previous similar studies[12,35,36], we thought that the P350−450 might reflect an earthquake experience interference, but also attention enhancing effect of earthquake-related words in Chengdu subjects, which might be associated with flashbulb memory and enhanced sensitivity for earthquake information. While the earthquake interference effect was not found in the Chongqing group. It is clear that the subjects who were in Chengdu city had much stronger personal experience of the earthquake exposure than did the subjects in Chongqing city. In addition, our dipole source analysis showed that the P350—450 was generated in the parahippocampal gyrus. This result also indicated that the P350—450 earthquake interference effect was not the classical ERP Stroop interference effect which originated from activity generated in the anterior cingulate cortex and prefrontal cortex[37,38]. The parahippocampal activation has been reported in many studies of memory, and suggested that the hippocampal/parahippocampal regions, posterior cingulated region, and the cerebellum may contribute to retrieving the memory trace related to the representation[39,40]. Other research indicated that the parahippocampal cortex itself may play an important role in spa-


tial memory[41,42]. Niki and Luo[43] have performed fMRI and showed activation of the left parahippocampal gyrus during recall of recent autobiographical episodes. Sakamoto et al.[44] also found that significant activation correlated with the masked traumatic stimuli in the parahippocampal region including the left parahippocampal gyrus and tail of the left hippocampus in the posttraumatic stress disorder (PTSD) group. They suggested that the left parahippocampal area associated with episodic and autobiographical memory might be abnormally easily activated[44,45]. Based on these findings, our results indicated that personal experience of the great Sichuan earthquake might make subject sensitivity for earthquake information, and direct personal earthquake experience (flashbulb memories retrieval) might be critical in engaging the neural mechanisms that underlie the modulation of selective attention. As Brown and Kulik pointed out, “flashbulb memories (memories for the circumstance in which one first learned of a very surprising and consequential event) were proposed to be exceptionally vivid and detailed, resistant to forgetting, and formed by a special biological mechanism”[46]. Therefore, our results also proved why many people (e.g., PTSD) would have longer-term problems, e.g.,

emotional numbing, irritability, memory problems and hyper-vigilance after disasters. This study investigated spatiotemporal patterns of brain activation during the earthquake color-matching Stroop task using scalp and dipole source analysis of ERPs. ERP data showed that Related words elicited a more positive ERP deflection (P350—450) than did Unrelated words between 350 and 450 ms in the Chengdu city group. Dipole source analysis showed that a generator was localized in the parahippocampal gyrus. These results indicated that the negative life events have serious influence on psychological and cognitive functions in people without a clinical disorder, and direct personal experience made subjects sensitive to earthquake information. 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. In the future, further studies should be done using both ERPs and fMRI to examine the role of the parahippocampal gyrus in cognitive processing of disaster information, and to determine whether other brain areas are involved in the earthquake color-matching Stroop task.

Stimuli Appendix Related earthquake words: 地震, 余震, 摇晃, 跨塌, 消毒, 自救, 塌陷, 逃生, 废墟, 封城, 倒塌, 强震, 灾民, 波及, 灾难, Unrelated earthquake words: 风筝, 钓鱼, 整顿, 崛起, 台灯, 刺猬, 婚姻, 责任, 森林, 繁琐, 外贸, 气象, 假设, 军旗, 品位, 1

绝望, 死亡, 救援, 灾区, 防疫, 悲伤, 惊恐, 损坏遇难, 裂缝, 掩埋, 位移, 震级, 孤儿, 帐篷, 震源, 流血, 抗震, 露宿, 瘟疫. 词典, 饮料, 继承, 家庭, 想法, 管理, 媒体, 帮助, 服务, 实验, 科技, 古墓, 声明, 选拔, 表格, 业绩, 思维, 生命, 帮助, 文件.

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