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Enhanced association between perceptual stimuli and trauma-related information in individuals with posttraumatic stress disorder symptoms
J. Behav. Ther. & Exp. Psychiat. 46 (2015) 202e207
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Enhanced association between perceptual stimuli and trauma-related information in individuals with posttraumatic stress disorder symptoms* Muyu Lin a, 1, Stefan G. Hofmann b, 2, Mingyi Qian a, *, Songwei Li c, 3 a b c
Department of Psychology, Peking University, Beijing, China Department of Psychological and Brain Sciences, Boston University, Boston, USA Department of Psychology, Tsinghua University, Beijing, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 4 April 2014 Received in revised form 20 October 2014 Accepted 21 October 2014 Available online 4 November 2014
Background and objectives: Intrusive memories in traumatized individuals are often triggered by stimuli that are perceptually (rather than conceptually) similar to those present just before or during the trauma. The present study examined whether those individuals with high levels of Posttraumatic Stress Disorder (PTSD) symptoms show a memory bias recall to perceptual cues and trauma target words compared to those with low levels of PTSD. Methods: The sample consisted of 30 adult participants who were involved in motor-vehicle or workrelated accidents; 15 of the participants endorsed clinically elevated symptoms of PTSD, while a comparison group of 15 participants reported low levels of symptoms. Participants performed an associative recognition task with conceptual or perceptual cue words and trauma-related or neutral target words. Participants were tested for their recognition accuracy by reporting the corresponding target when a cue was given. Results: Both groups performed better for the perceptual word pairs than for the conceptual word pairs, irrespective of the target word type. However, only the high PTSD symptoms group exhibited an additional enhancement in performance for the perceptual word pairs with trauma-related target words. Limitations: A nonclinical sample was utilized for this study; although PTSD was assessed, diagnoses were not confirmed. In addition, there was lack of a healthy non-traumatized control group. Conclusions: These results provide partial support for the cognitive model and the notion that intrusive memories are specific to the trauma-related event rather than to a general associative learning bias. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Trauma Posttraumatic stress disorder Trigger stimuli Perceptual stimuli Conceptual stimuli Associative learning
1. Introduction Traumatized individuals often re-experience the highlydistressing and emotional fragments of trauma repetitively and involuntarily (Hellawell & Brewin, 2004; Holmes, Grey, & Young,
* This work was supported by China Scholarship Council awarded to the first author. * Corresponding author. Room 221, Philosophy Building (Zhexue Lou), Peking University, No.5 Yiheyuan Road, Beijing 100871, PR China. Tel.: þ86 10 62751093; fax: þ86 10 62761081. E-mail addresses: [email protected] (M. Lin), [email protected] (S.G. Hofmann), [email protected] (M. Qian), [email protected] (S. Li). 1 Address: R. 220, Zhexuelou Building, 5 Yiheyuan Rd., Beijing 100871, PR China. 2 Address: Forth Floor, 648 Beacon St., Boston, MA 02215, USA. 3 Address: Department of Psychology, Tsinghua University, Beijing 100871, PR China.
http://dx.doi.org/10.1016/j.jbtep.2014.10.008 0005-7916/© 2014 Elsevier Ltd. All rights reserved.
2005). These intrusive memories can occur unpredictably, even long after the dangerous situation has passed, and are usually composed of fractional sensory components, accompanied by intense emotional distress (Hellawell & Brewin, 2004; Michael & Ehlers, 2007; Van der Kolk & Fisler, 1995). Triggers of intrusive memories are often perceptual stimuli that are similar to those present shortly before or during the trauma, rather than conceptual stimuli (Ehlers & Clark, 2000; Foa, Steketee, & Rothbaum, 1989; Van der Kolk & Fisler, 1995). The cognitive models of posttraumatic stress disorder (PTSD) assume that the way an individual processes events influences the development of PTSD symptoms (e.g., Brewin, Dalgleish, & Joseph, 1996; Brewin, Gregory, Lipton, & Burgess, 2010; Ehlers & Clark, 2000). For instance, the model by Ehlers and Clark (2000) distinguishes two inversely-related processing modes; individuals with a predominance of data-driven (bottom-up) processing are more
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likely to develop PTSD than those who tend to use conceptuallydriven (top-down) processing. Data-driven processing refers to processing of the perceptual characteristics and the sensory impressions of the situation, rather than the meaning of the event. Therefore, using data-driven processing is posited to result in a perceptually-encoded and poorly-elaborated memory trace. Conceptual processing, on the other hand, refers to processing the meaning of the situation, organizing it, and placing it into a consecutive context. This is assumed to lead to contextualized memory representations (Roediger, 1990). A number of studies provide support for these two distinct processing modes (Conway & Pleydell-Pearce, 2000; Halligan, Clark, & Ehlers, 2002; Kindt, van den Hout, Arntz, & Drost, 2008). Studies exploring associative learning of trauma memory have consistently shown that traumatized individuals show strong associations between stimuli (stimuliestimuli) or between stimuli and strong affect (stimuli-responses), but only when traumarelated materials are involved (e.g., Brennen, Dybdahl, & Kapidzi c, 2007; Ehlers & Clark, 2000; Foa et al., 1989). For instance, Golier, Yehuda, Lupien, and Harvey (2003) investigated associative learning in holocaust survivors using word pairs containing neutral or holocaust-related words. The results suggested that aging PTSD patients preferentially form new associations with trauma-related rather than neutral stimuli. It has further been demonstrated that trigger stimuli are most often perceptual stimuli (Ehlers & Clark, 2000; Ehlers, Hackmann, & Michael, 2004; Foa et al., 1989; Michael, Ehlers, Halligan, & Clark, 2005) that might activate traumatic memories (Ehlers & Clark, 2000; Foa et al., 1989; Van der Kolk & Fisler, 1995). Thus, it is possible that traumatized individuals are better at memorizing associations between perceptual cues and trauma-related targets, than associations involving conceptual cues or neutral targets. The word pair learning task (associative recognition task) used by Golier et al. (2003) as well as others (e.g., Amir, Badour, & Freese, 2009; Guez et al., 2013) was developed to test whether those with PTSD more easily form new associations that contain certain types of words. In the present study, we distinguished two types of words as cue stimuli. First, we used perceptual stimuli that primarily activated memory for perceptual impressions. For instance, the perceptual word green evokes many images and scenes, such as leaves, grasslands, etc. Second, conceptual stimuli was used to evoke semantic or conceptual memories that are typically associated with more abstract and less concrete perceptual information (e.g., the word reason). The present study examined a critical aspect of the cognitive model of PTSD developed by Ehlers and Clark (2000) by testing whether those with PTSD symptoms are more likely to link target trauma-related words with perceptual cue words or whether they have a general perceptual memory bias. Using an associative learning task combined with a cue-recognition task, the first aim was to examine whether individuals with high levels of PTSD symptoms (PTSSþ group) had a stronger tendency to associate perceptual stimuli with trauma. The second aim was to scrutinize the characteristics of associative learning in individuals with PTSD symptoms. By comparing the PTSSþ group with a PTSS group who also experienced potentially traumatizing events but that did not report or only showed low levels of PTSD symptoms, we were able to examine whether it is the memory bias towards perceptual stimuli generally (e.g., memorizing perceptual stimuli better than conceptual stimuli) or the associative bias towards the association between perceptual stimuli and trauma that distinguishes the PTSSþ group from the PTSS group. Based on previous research, we hypothesized that, relative to the PTSS group, the PTSSþ group would exhibit (a) a stronger association bias towards perceptualtrauma word pairs, (b) a greater memory bias towards pairs that
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contained trauma-related words, and also (c) a greater memory bias towards pairs that contained perceptual words. 2. Methods 2.1. Participants Participants were recruited from a sample of 82 patients in the orthopedics wards of three hospitals (People's Hospital of Hainan, People's Hospital of Qiongshan, and People's Hospital of Haikou). All were involved in motor vehicle accidents or had suffered work related injuries requiring hospitalization for at least three-weeks. Participants voluntarily completed the Chinese version of the Impact of Event Scale-Revised (IES-R; Huang, Zhang, Xiang, and Zhou, 2006; Weiss & Marmar, 1997), the Chinese version of the Center for Epidemiological Studies Depression Scale (CES-D; Radloff, 1977; Zhang et al., 2010), and an anthropologic and past experience questionnaire. High PTSD cutoff criterion suggested by Huang et al. (2006) was employed in the current study. Participants with scores equal to or higher than 35 on the IES-R were assigned to the PTSSþ group. For the PTSS group, the participant with the lowest score on the IES-R (i.e., 5) was approached first regarding participation in the memory game. If the participant refused to partake in the game, the participant with the next lowest score was approached. This procedure was continued until 15 individuals agreed to perform the memory task for the PTSS group. The groups were matched for gender, years of education, and age. In order to limit the heterogeneity of the sample and the potentially confounding effects of depression or other psychiatric disorders, participants were excluded if they (a) scored higher than 24 on the CES-D (according to Zhang et al. (2010), 24 and above indicates severe depression), (b) had a history of neurologic or psychiatric disorders (participants were not excluded if a PTSD history was reported, however, no participants in the current study reported a history of PTSD), (c) reported that the severity of injury was only minor or slight, or (d) suffered head trauma as a result of the accident. Exclusion criteria (b), (c), and (d) were first based on selfreport regarding “previous diagnoses” on the anthropologic and past experience questionnaire. In addition, the head trauma, injury condition, previous diagnoses and medical history were double checked by the experimenter. Among the 19 potential participants who scored equal to or higher than 35 on IES-R and the 20 potential participants who scored in the bottom, nine were excluded: two both scored higher than 24 on CES-D and also reported history of major depression, one only scored higher than 24 on CES-D, one only reported a previous major depression diagnosis, one was taking antianxiety medicine, and four declined to continue participating. The final sample consisted of 30 participants (15 in each group). The IES-R scores of the PTSSþ group (including eight males and seven females) ranged from 35 to 59, whereas those in the PTSS group (including eight males and seven females) ranged from 7 to 25 (Table 1). Baseline assessments were conducted 21 ± 17 days (range 3e73) after hospital registration; the experiments were carried out two days following the initial assessments. 2.2. Materials and measures 2.2.1. Stimulus materials The experimental software for all parts of the study was programmed with Presentation (Neurobehavioral Systems, version 0.71). Word pairs were presented as white 72-font Chinese characters against a black background on a 13.5-inch-wide screen placed approximately 40 cm from the eyes of the participants.
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Table 1 Means (SDs) for anthropological and psychometric data, and the recognition accuracy for the four word pair types.
Age Education Injury Assessment range CES-D STAI-S IES-R Perceptual-trauma Conceptual-trauma Perceptual-neutral Conceptual-neutral
PTSSþ group
PTSS group
t-test
33.60(11.46) 11.53(2.80) 3.87(0.83) 21.93 (20.91) 14.73(4.78) 44.23(8.28) 43.00(6.60) 2.60 (1.12) 1.07 (0.96) 1.13 (0.99) 0.67 (0.72)
29.73(9.86) 12.67(3.50) 3.53(0.64) 19.40 (12.63) 14.05(5.98) 42.00(7.27) 20.07(5.31) 2.00 (0.85) 1.20 (1.15) 1.73 (1.03) 1.13 (0.99)
t t t t t t t t t t t
¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
0.99, p > .3 0.98, p > .3 1.23, p > .2 0.40, p > .7 0.34, p > .7 0.78, p > .4 10.48, p < .0001 1.66, p > .1 0.35, p > .7 1.62, p > .1 1.47, p > .1
Note: PTSSþ group: group with PTSD symptoms; PTSS group: group without PTSD symptoms; Education: years of education; Assessment range: days between the accidents and the assessment; CES-D: score on the Epidemiological Studies Depression Scale; STAI-S: score on the State-Trait Anxiety Inventory-State; IES-R, scores on the Impact of Event Scale Revised. Perceptual-trauma, conceptual-trauma, perceptual-neutral, and conceptual-neutral referred to the four word pair types respectively. The df for all t-tests was 28.
Two types of words (perceptual and conceptual) were chosen as cue words. Because recall memory is better for pictures (e.g., objects) than for words (e.g., objects’ names) (Paivio, Rogers, & Smythe, 1968), we used verbal stimuli as cues only. In order to exclude potential confounding factors, we chose visual perceptual words only. Two undergraduates majoring in psychology chose 50 words from the Corpus for Studies of Modern Chinese (25 of each type). Then, these 50 words were rated on a 7-point scale from “1 ¼ evokes perceptual memory only” to “7 ¼ evokes a conceptual impression only” by 16 other undergraduates with different majors. The final word list contained those rated either in the top 10 words (for conceptual words, the mean score was 6.56 ± 0.24, and the word frequency was 93.37 ± 57.20 per million) or in the bottom 10 words (for perceptual words, the mean score was 1.42 ± 0.20, and the word frequency was 93.78 ± 54.69 per million). These two types of words had significantly different perceptualconceptual ratings, t (19) ¼ 54.62, p < .0001, but did not differ in word frequency, t (19) ¼ 0.02, p > .9. In each case, two words were used for the practice phase, and eight for the study phase. The target words were either trauma-related or neutral. The trauma-related words were based on those used by Amir et al. (2009) and Brennen et al. (2007). The words were translated and revised for the orthopedic inpatients; eight trauma related words were selected with a frequency of 19.62 ± 41.14 per million. 12 neutral words were selected (word frequency 34.90 ± 44.45 per million) matching the part of speech and frequency of the traumarelated words. The word frequency of the two target word types did not differ, t (12) ¼ 0.57, p > .6. Four of the neutral words were used for the practice phase and eight for the study stage. Cue words and target words were then paired randomly to form four different types of word pairs: perceptual-trauma, perceptualneutral, conceptual-trauma, and conceptual-neutral word pairs. To ensure that each cue and its paired target word were not naturally associated, we asked the same 16 students who had rated the cue words to give the first five perceptual and first five conceptual words that came to mind when presented with the target words (modified from Lupien et al., 1994). None of the target words generated the paired cue words used. The word pairs used in the study are listed in the Appendix.
2.2.2. Associative recognition task The task consisted of a practice phase, a study phase, and a cuerecognition phase. During the practice phase, four word pairs were
presented (two perceptual-neutral word pairs and two conceptualneutral word pairs) to familiarize participants with the procedure. In the study phase, 16 word pairs different from those in the practice phase (including all four word pair types; each type had four word pairs) were shown in random order that changed with each participant. Each word pair was shown only once for 5 s during 1.5 s intervals. Participants were asked to try their best to memorize all the word pairs and were told that later there would be a cue-recognition task about these pairs. The cue-recognition phase tested explicit memory performance for the target words from the 16 pairs that were presented. Participants were presented with two sheets of test paper: Sheet A listed all the cue words shown in the study phase, and Sheet B listed 16 target words and 4 distractors. Participants were asked to recognize the target words that had been paired with the cue words in the study phase. Recognition accuracy was calculated as the dependent variable. 2.2.3. Self-report questionnaires Trauma symptoms. The IES-R (Weiss & Marmar, 1997) is a 22item questionnaire based on the DSM-IV criteria for PTSD: intrusive thoughts, avoidance, and hyperarousal. Participants were asked to rate items based on a stressful (traumatic) event. The modified instructions that participants received were: “Individuals may experience some of the disturbances mentioned below after experiencing a stressful life event that involved actual or potential death or serious injuries, or a threat to one's physical health, associated with feelings of horror, hopelessness, or terror (e.g., motor-vehicle accidents, work-related accidents, or losing loved ones). Please choose an event that affected your emotion/mood for a while, and give a brief description below, then rate the items based on your feelings within the last 7 days. You can choose the event that caused your hospitalization, or anything that adversely impacted your mood/feelings or has worsened your life.” All of the 30 participants identified the accidents which caused their current injury as the traumatic event. Each item was rated on a weighted 4point scale (0 ¼ not at all, 4 ¼ often) for frequency of occurrence in the past 7 days. Total scores were calculated in the current study. In our sample, the Cronbach's alpha of the IES-R total was a ¼ .93. Depression. The Chinese version of the CES-D is a self-rated depression symptom questionnaire in which 20 items are rated on a 4-point Likert scale (Radloff, 1977). The questionnaire asks participants about their feelings or symptoms during the recent seven days. The Cronbach's alpha for the CES-D in the present sample was a ¼ .95. State Anxiety. The state form of the Chinese version of the StateTrait Anxiety Inventory (STAI-S; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1983; in Wang, Wang, & Ma, 1999) was used to measure the state anxiety of participants during the prior week. This scale is composed of twenty items evaluating subjective and transitory feelings such as tension, nervousness, and worry on a 4point scale. The Cronbach's alpha in the current sample was a ¼ .92. Miscellaneous measures. The anthropologic and past experience questionnaire was a self-constructed questionnaire, which included basic anthropologic information, diagnoses and medical history, and questions about how participants perceived their injury. The questionnaire screened participants for a history of trauma, neurologic, or psychiatric disorders. 2.2.4. Manipulation check In the manipulation check phase, participants rated each word on Sheet B (16 target words and 4 distractors) along the two dimensions of arousal and pleasantness, each on a scale from 0 to 4. The arousal rating was labeled “very stressful” to “very relaxing”,
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while the pleasantness dimension was rated from “very painful” to “very pleasant”. 2.3. Procedure The entire study was carried out on the orthopedic ward. Participants were informed verbally and in writing that the study may involve some unpleasant words and that as it was voluntary, they could withdraw at any point without reason. All participants gave informed consent before starting the study. The study was approved by the Committee for Protecting Human and Animal Subjects at Peking University. After receiving clear instructions on the procedure, the associative learning task was conducted using an IBM laptop. After the word pairs had all been presented, the experimental software started to count the time for a 10-min retention interval. During this time, participants filled out the Chinese version of STAI-S. After performing this task for 10-min, the cue-recognition task began, and the rest of the inventory was completed at the end of the experiment. After the manipulation check phase, participants were compensated for their time (￥10; about $ 1.61). 3. Results As planned and expected, the two groups differed significantly on IES-R scores; the PTSSþ and PTSS groups did not, however, statistically differ on any other baseline variable, including demographic variables (e.g., gender, age, education level), assessment range (i.e., days after the accidents), and trauma exposure severity (see Table 1). 3.1. Manipulation check Participants’ ratings of the target words were examined using 2 (group: PTSSþ group vs. PTSS group) 2 (target type: traumarelated vs. neutral type) repeated measures ANOVAs. Traumarelated target words were rated significantly more stressful than neutral target words, F (1, 28) ¼ 106.66, p < .0001. The group and group by target word type interaction effects were not significant. Moreover, the trauma-related target words were rated significantly more painful than neutral target words, F (1, 28) ¼ 94.37, p < .0001. Again, the group and group by target type interaction effect were not significant. 3.2. Associative bias We computed a 2 4 (group: PTSSþ group versus PTSS group word pair type: perceptual-trauma, perceptual-neutral, conceptual-trauma, and conceptual-neutral) repeated measures ANOVA to investigate whether there was an associative bias towards specific pair types. A significant effect of word pair type, F (3, 84) ¼ 26.25, p < .0001, h2partial ¼ .48, and a significant group by word pair type interaction effect, F (3, 84) ¼ 5.05, p ¼ .003, h2partial ¼ .15, together indicated that the recognition accuracy differed when the word pair type changed and that the groups showed different patterns in these recognition performances (Fig. 1). However there was no group effect, F (1, 28) ¼ 0.26, p > .6, h2partial ¼ .01. The post hoc test aimed at comparing the performance of the two groups for every word pair showed that participants from both groups recognized a similar number of the various word pair categories (Table 1). We then evaluated the effect of word pair type in each group. Repeated measures ANOVA in the PTSSþ group showed a significant effect of word pair types, F (3, 42) ¼ 29.85, p < .0001, h2partial ¼ 0.68. Pairwise comparisons using Bonferroni correction
Fig. 1. Groups by word pair type interaction. The Figure shows bar chart of recognition results for PTSSþ and PTSS groups. PeT: perceptual-trauma word pairs; PeN: perceptual-neutral word pairs; CeT: conceptual-trauma word pairs; CeN: conceptualneutral word pairs. **p < .0001 between word pairs.
showed that the recognition accuracy of perceptual-trauma word pairs was significantly greater than that of perceptual-neutral word pairs, mean difference (MD) ¼ 1.53, p < .0001, conceptual-trauma (MD ¼ 1.47, p < .0001), and conceptual-neutral word pairs (MD ¼ 1.93, p < .0001). There was no difference in the recognition accuracy of the latter three, indicating that the PTSSþ group was better at recognizing perceptual-trauma word pairs (Fig. 1). In the PTSS group, the repeated measures ANOVA also showed a significant word pair type effect, F (3, 42) ¼ 5.32, p ¼ .003, h2partial ¼ .28. Follow-up pairwise comparisons (with Bonferronicorrection) showed a significant difference between the perceptual-trauma and conceptual-neutral word pairs (MD ¼ 0.87, p ¼ .026). None of the other effects reached the level of statistical significance.
3.3. Memory bias towards different cues and targets The recognition data were submitted to a 2 2 2 (group: PTSSþ group versus PTSS group cue word type: perceptual cue versus conceptual cue word target word type: trauma-related versus neutral) ANOVA with repeated measures on the first factor in order to test whether there was a memory bias towards a cue type or a target type. The cue word type effect, F (1, 28) ¼ 32.98, p < .0001, h2partial ¼ .54, and target word type effect were significant, F (1, 28) ¼ 34.97, p < .0001, h2partial ¼ .56, indicating that word pairs with a perceptual cue word or a trauma-related target word were more easily memorized. The group effect was not significant, F (1, 28) ¼ 0.26, p > .6, h2partial ¼ .01, suggesting that the two groups had similar recognition accuracy toward each word pair. The cue word by target word interaction effect was significant, F (1, 28) ¼ 8.15, p ¼ .008, h2partial ¼ 0.23. Simple main effect analyses with Bonferroni-correction showed that all participants recognized perceptual cues better than conceptual cues, regardless of the target types (for trauma-related targets, MD ¼ 1.17, p < .0001; and for neutral targets, MD ¼ 0.53, p ¼ .004). The effect of target word by group interaction effect was significant, F (1, 28) ¼ 16.99, p < .0001, h2partial ¼ .38. Further analyses for this target word by group interaction showed that the PTSSþ group had a significant difference regarding the recognition performance between trauma targets and neutral targets, MD ¼ 1.87, p < .0001, whereas the PTSS group did not have a different recognition accuracy between two target types, MD ¼ 0.33, p > .2. However, the word cue by group interaction effect was not significant, F (1, 28) ¼ 1.03, p > .3,
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h2partial ¼ .04. No significant effect on the triple interaction effect was found, F (1, 28) ¼ 1.41, p ¼ .061, h2partial ¼ .12. 4. Discussion The goal of the current study was to examine the difference between traumatized individual with high versus low PTSD symptomatology on accuracy of recognition for perceptual cues and trauma-related target words. We hypothesized that the PTSSþ group would show a memory bias towards word pairs that contained trauma-related or perceptual words, and show an associative bias toward perceptual-trauma word pairs. In contrast, we did not expect the PTSS group to differ in the four word type pairs. As expected, the analysis of associative recognition indicated that the two groups have different memory patterns. The PTSSþ group showed better recognition accuracy of perceptual-trauma word pairs as compared to the other three word pairs. However, there was no difference between the other three, indicating that traumatized individuals who developed PTSD symptoms more easily associate perceptual stimuli with trauma-related information. This result is in accord with our hypothesis and may have implications for understanding intrusive memories. The current study showed that the PTSSþ group was better able to form new associations between perceptual stimuli and trauma information compared to other combinations. This association bias might be the mechanism underlying intrusive memories and the trigger stimuli, as it has been commonly reported that perceptual rather than conceptual stimuli compose most of the triggers of intrusive memory (Brewin et al., 1996; Ehlers & Clark, 2000; Ehlers et al., 2004; Foa et al., 1989). Future research with an objective of clarifying and/or understanding the voluntary and involuntary memory encoding of trauma could help guide the development of exposure based treatments for PTSD. Compared to the PTSS group, the PTSSþ group exhibited trauma-related facilitation in explicit memory. This is consistent with many previous studies (e.g., Brennen et al., 2007; Ehlers & Clark, 2000; Foa et al., 1989; Golier et al., 2003) and suggests that attention is easily drawn to stimuli that foreshadow or remind in€ 2002). dividuals about the trauma (Paunovic, Lundh, & Ost, As for the memory pattern of the PTSS group when compared with the PTSSþ group, the results point to a memory bias toward perceptual word pairs. Although there was no significant difference between the recognition of two targets words, the emotional memory-enhancement effect along with the bias for perceptual stimuli may explain the greater recognition of perceptual-trauma word pairs as compared to conceptual-neutral word pairs among participants in the PTSS group. This is in line with the notion that people are generally better at memorizing negative information than neutral information (Hamann, 2001; Kensinger & Corkin, 2003) Consistent with the model of PTSD proposed by Ehlers and Clark (2000), we observed that individuals with PTSD symptoms generally find it easier to memorize perceptual than conceptual words. In our study, participants only had a short time to process and memorize the word pairs, and it is possible that this time was insufficient for information to enter the deeper phase of conceptual processing. Therefore, it is possible that words that contained more concrete and perceptual information could be more easily recognized than words that contained conceptual and abstract information (e.g., Paivio, 1965), just as pictures are more easily remembered than words (e.g., Paivio, et al., 1968). The two groups did not differ in their recognition of word pair types, suggesting that the symptoms may not generally influence the non-practiced short-delay associative memory. This finding is in accordance with many previous studies (e.g., Amir et al., 2009;
Johnsen, Kanagaratnam, & Asbjørnsen, 2008; LaGarde, Doyon, & Brunet, 2010). It should be noted, however, that the differences were only significant between word pairs but not between groups. Therefore, it is not possible to exclude learning difficulties as an explanation of the findings. An alternative way to explain the results may be that the perceptual cues were easier to memorize than conceptual cues because the former tend to be more concrete and the later more abstract (e.g., Paivio, 1965). In addition, the memory enhancement for trauma-related targets may be due to the emotional word enhancement effect as discussed above (e.g., Kensinger & Corkin, 2003). These effects could partially explain the cue by target interaction found in all the participants together, and the absent between group effect. However, the two groups still showed different patterns when compared with each other. For instance, the memory enhancement of trauma-related targets was found only in PTSSþ group and for the PTSS group only the cue types reach the level of significance. The following limitations should be considered when interpreting these results. First, the sample size was modest, which limits the generalizability of the findings. Second, the PTSSþ group reported elevated levels of PTSD symptoms on the IES-R suggestive of a PTSD diagnosis, but a clinician based interview diagnosis of PTSD was not conducted. Prior studies suggest that the occurrence of PTSD symptoms one month post-trauma is one of the major predictors of subsequence PTSD (e.g., Hamanaka et al., 2006; Rothbaum, Foa, Riggs, Murdock, & Walsh, 1992) and many individuals with PTSD symptoms within months presented similar memory characteristics which were associated with chronic PTSD (e.g., Brandes, et al., 2002). However, some people recover spontaneously, whereas others show delayed PTSD. Therefore, the observed effects may be a weakened reflection of real-life trauma situations. Future studies using patient samples of clinically diagnosed PTSD would strengthen the results. Moreover, there was no healthy control group without any exposure to potentially traumatizing events. However, since our primary aim was to explore the differential features between traumatized individuals who developed PTSD symptoms and those who did not, a comparison between these two groups appeared sufficient for this purpose. In addition, we did not have raters rate the cue words on an emotional dimension, and participants were not instructed to rate the target words on a perceptual-conceptual level. However, we did not intend to compare the accuracy of cue words and target words. Therefore, it is not believed that this omission impacted the main purpose or the results of the study. Finally, only verbal stimuli was used to minimize potential confounders, so it is possible that picture stimuli might have produced different results. More profound understanding on the memory mechanism of PTSD will benefit from future studies using various memory materials and investigating both short-term and long-term memory characteristics. In sum, the current study showed that individuals with PTSD symptoms exhibit a biased association between perceptual stimuli and trauma words, whereas low symptom participants do not. Our findings provide partial support for the notion that intrusive memories are specific to the trauma-related event and perceptual cues of that trauma rather than to a general perceptual memory bias. These results are in line with the cognitive model by Ehlers and Clark (2000). Acknowledgments The data were collected partly for the first author's undergraduate thesis under the guidance of the third and the forth authors. The first author would like to thank and acknowledge Zhenzhen Liu, Yu Liu, Xiaonan Liu, Dr. Elizabeth A. Mundy, Dr. Iain Bruce,
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Hongbo Yu and Dr. Arlene T. Gordon-Hollingsworth for their kind assistance and support during the development of this study and in revising the manuscript. This manuscript was supported in part by China Scholarship Council (201306010054) awarded to the first author.
Appendix. Chinese (English) pairs used in the study
Word pair types
Pairs used in the study phase
白云(cloud) e 死亡(death), 图画(picture) e 车祸(accident), 绿色(green) e 绝望(despair), 鲜花(flower) e 骨折(fracture) 概念(concept) e 离婚(divorce), 科学(science) e 撞击(crash), 原因(reason) e 犯罪(criminal), 义务(obligation) e 截肢(amputation) Perceptual- 眼睛(eye) e 居住(living), 小狗(dog) e 交易(trade), neutral 月亮(moon) e 条例(rule), 大海(sea) e 竹竿(bamboo bar) Conceptual- 哲学(philosophy) e 记载(recording), 方法(methodology) e neutral 朝廷(royal court), 事件(event) e 冷藏(refrigerate), 直接(direct) e 古装(ancient costume) Pairs used in the practice phase 椰子(coconut) e 鸡蛋(egg), 生活(life) e 元旦(new year), 劳动(labor) e 动物(animal), 电视(television) e 植物(botany) Perceptualtrauma Conceptualtrauma
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Enhanced association between perceptual stimuli and trauma-related information in individuals with posttraumatic stress disorder symptoms* Muyu Lin a, 1, Stefan G. Hofmann b, 2, Mingyi Qian a, *, Songwei Li c, 3 a b c
Department of Psychology, Peking University, Beijing, China Department of Psychological and Brain Sciences, Boston University, Boston, USA Department of Psychology, Tsinghua University, Beijing, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 4 April 2014 Received in revised form 20 October 2014 Accepted 21 October 2014 Available online 4 November 2014
Background and objectives: Intrusive memories in traumatized individuals are often triggered by stimuli that are perceptually (rather than conceptually) similar to those present just before or during the trauma. The present study examined whether those individuals with high levels of Posttraumatic Stress Disorder (PTSD) symptoms show a memory bias recall to perceptual cues and trauma target words compared to those with low levels of PTSD. Methods: The sample consisted of 30 adult participants who were involved in motor-vehicle or workrelated accidents; 15 of the participants endorsed clinically elevated symptoms of PTSD, while a comparison group of 15 participants reported low levels of symptoms. Participants performed an associative recognition task with conceptual or perceptual cue words and trauma-related or neutral target words. Participants were tested for their recognition accuracy by reporting the corresponding target when a cue was given. Results: Both groups performed better for the perceptual word pairs than for the conceptual word pairs, irrespective of the target word type. However, only the high PTSD symptoms group exhibited an additional enhancement in performance for the perceptual word pairs with trauma-related target words. Limitations: A nonclinical sample was utilized for this study; although PTSD was assessed, diagnoses were not confirmed. In addition, there was lack of a healthy non-traumatized control group. Conclusions: These results provide partial support for the cognitive model and the notion that intrusive memories are specific to the trauma-related event rather than to a general associative learning bias. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Trauma Posttraumatic stress disorder Trigger stimuli Perceptual stimuli Conceptual stimuli Associative learning
1. Introduction Traumatized individuals often re-experience the highlydistressing and emotional fragments of trauma repetitively and involuntarily (Hellawell & Brewin, 2004; Holmes, Grey, & Young,
* This work was supported by China Scholarship Council awarded to the first author. * Corresponding author. Room 221, Philosophy Building (Zhexue Lou), Peking University, No.5 Yiheyuan Road, Beijing 100871, PR China. Tel.: þ86 10 62751093; fax: þ86 10 62761081. E-mail addresses: [email protected] (M. Lin), [email protected] (S.G. Hofmann), [email protected] (M. Qian), [email protected] (S. Li). 1 Address: R. 220, Zhexuelou Building, 5 Yiheyuan Rd., Beijing 100871, PR China. 2 Address: Forth Floor, 648 Beacon St., Boston, MA 02215, USA. 3 Address: Department of Psychology, Tsinghua University, Beijing 100871, PR China.
http://dx.doi.org/10.1016/j.jbtep.2014.10.008 0005-7916/© 2014 Elsevier Ltd. All rights reserved.
2005). These intrusive memories can occur unpredictably, even long after the dangerous situation has passed, and are usually composed of fractional sensory components, accompanied by intense emotional distress (Hellawell & Brewin, 2004; Michael & Ehlers, 2007; Van der Kolk & Fisler, 1995). Triggers of intrusive memories are often perceptual stimuli that are similar to those present shortly before or during the trauma, rather than conceptual stimuli (Ehlers & Clark, 2000; Foa, Steketee, & Rothbaum, 1989; Van der Kolk & Fisler, 1995). The cognitive models of posttraumatic stress disorder (PTSD) assume that the way an individual processes events influences the development of PTSD symptoms (e.g., Brewin, Dalgleish, & Joseph, 1996; Brewin, Gregory, Lipton, & Burgess, 2010; Ehlers & Clark, 2000). For instance, the model by Ehlers and Clark (2000) distinguishes two inversely-related processing modes; individuals with a predominance of data-driven (bottom-up) processing are more
M. Lin et al. / J. Behav. Ther. & Exp. Psychiat. 46 (2015) 202e207
likely to develop PTSD than those who tend to use conceptuallydriven (top-down) processing. Data-driven processing refers to processing of the perceptual characteristics and the sensory impressions of the situation, rather than the meaning of the event. Therefore, using data-driven processing is posited to result in a perceptually-encoded and poorly-elaborated memory trace. Conceptual processing, on the other hand, refers to processing the meaning of the situation, organizing it, and placing it into a consecutive context. This is assumed to lead to contextualized memory representations (Roediger, 1990). A number of studies provide support for these two distinct processing modes (Conway & Pleydell-Pearce, 2000; Halligan, Clark, & Ehlers, 2002; Kindt, van den Hout, Arntz, & Drost, 2008). Studies exploring associative learning of trauma memory have consistently shown that traumatized individuals show strong associations between stimuli (stimuliestimuli) or between stimuli and strong affect (stimuli-responses), but only when traumarelated materials are involved (e.g., Brennen, Dybdahl, & Kapidzi c, 2007; Ehlers & Clark, 2000; Foa et al., 1989). For instance, Golier, Yehuda, Lupien, and Harvey (2003) investigated associative learning in holocaust survivors using word pairs containing neutral or holocaust-related words. The results suggested that aging PTSD patients preferentially form new associations with trauma-related rather than neutral stimuli. It has further been demonstrated that trigger stimuli are most often perceptual stimuli (Ehlers & Clark, 2000; Ehlers, Hackmann, & Michael, 2004; Foa et al., 1989; Michael, Ehlers, Halligan, & Clark, 2005) that might activate traumatic memories (Ehlers & Clark, 2000; Foa et al., 1989; Van der Kolk & Fisler, 1995). Thus, it is possible that traumatized individuals are better at memorizing associations between perceptual cues and trauma-related targets, than associations involving conceptual cues or neutral targets. The word pair learning task (associative recognition task) used by Golier et al. (2003) as well as others (e.g., Amir, Badour, & Freese, 2009; Guez et al., 2013) was developed to test whether those with PTSD more easily form new associations that contain certain types of words. In the present study, we distinguished two types of words as cue stimuli. First, we used perceptual stimuli that primarily activated memory for perceptual impressions. For instance, the perceptual word green evokes many images and scenes, such as leaves, grasslands, etc. Second, conceptual stimuli was used to evoke semantic or conceptual memories that are typically associated with more abstract and less concrete perceptual information (e.g., the word reason). The present study examined a critical aspect of the cognitive model of PTSD developed by Ehlers and Clark (2000) by testing whether those with PTSD symptoms are more likely to link target trauma-related words with perceptual cue words or whether they have a general perceptual memory bias. Using an associative learning task combined with a cue-recognition task, the first aim was to examine whether individuals with high levels of PTSD symptoms (PTSSþ group) had a stronger tendency to associate perceptual stimuli with trauma. The second aim was to scrutinize the characteristics of associative learning in individuals with PTSD symptoms. By comparing the PTSSþ group with a PTSS group who also experienced potentially traumatizing events but that did not report or only showed low levels of PTSD symptoms, we were able to examine whether it is the memory bias towards perceptual stimuli generally (e.g., memorizing perceptual stimuli better than conceptual stimuli) or the associative bias towards the association between perceptual stimuli and trauma that distinguishes the PTSSþ group from the PTSS group. Based on previous research, we hypothesized that, relative to the PTSS group, the PTSSþ group would exhibit (a) a stronger association bias towards perceptualtrauma word pairs, (b) a greater memory bias towards pairs that
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contained trauma-related words, and also (c) a greater memory bias towards pairs that contained perceptual words. 2. Methods 2.1. Participants Participants were recruited from a sample of 82 patients in the orthopedics wards of three hospitals (People's Hospital of Hainan, People's Hospital of Qiongshan, and People's Hospital of Haikou). All were involved in motor vehicle accidents or had suffered work related injuries requiring hospitalization for at least three-weeks. Participants voluntarily completed the Chinese version of the Impact of Event Scale-Revised (IES-R; Huang, Zhang, Xiang, and Zhou, 2006; Weiss & Marmar, 1997), the Chinese version of the Center for Epidemiological Studies Depression Scale (CES-D; Radloff, 1977; Zhang et al., 2010), and an anthropologic and past experience questionnaire. High PTSD cutoff criterion suggested by Huang et al. (2006) was employed in the current study. Participants with scores equal to or higher than 35 on the IES-R were assigned to the PTSSþ group. For the PTSS group, the participant with the lowest score on the IES-R (i.e., 5) was approached first regarding participation in the memory game. If the participant refused to partake in the game, the participant with the next lowest score was approached. This procedure was continued until 15 individuals agreed to perform the memory task for the PTSS group. The groups were matched for gender, years of education, and age. In order to limit the heterogeneity of the sample and the potentially confounding effects of depression or other psychiatric disorders, participants were excluded if they (a) scored higher than 24 on the CES-D (according to Zhang et al. (2010), 24 and above indicates severe depression), (b) had a history of neurologic or psychiatric disorders (participants were not excluded if a PTSD history was reported, however, no participants in the current study reported a history of PTSD), (c) reported that the severity of injury was only minor or slight, or (d) suffered head trauma as a result of the accident. Exclusion criteria (b), (c), and (d) were first based on selfreport regarding “previous diagnoses” on the anthropologic and past experience questionnaire. In addition, the head trauma, injury condition, previous diagnoses and medical history were double checked by the experimenter. Among the 19 potential participants who scored equal to or higher than 35 on IES-R and the 20 potential participants who scored in the bottom, nine were excluded: two both scored higher than 24 on CES-D and also reported history of major depression, one only scored higher than 24 on CES-D, one only reported a previous major depression diagnosis, one was taking antianxiety medicine, and four declined to continue participating. The final sample consisted of 30 participants (15 in each group). The IES-R scores of the PTSSþ group (including eight males and seven females) ranged from 35 to 59, whereas those in the PTSS group (including eight males and seven females) ranged from 7 to 25 (Table 1). Baseline assessments were conducted 21 ± 17 days (range 3e73) after hospital registration; the experiments were carried out two days following the initial assessments. 2.2. Materials and measures 2.2.1. Stimulus materials The experimental software for all parts of the study was programmed with Presentation (Neurobehavioral Systems, version 0.71). Word pairs were presented as white 72-font Chinese characters against a black background on a 13.5-inch-wide screen placed approximately 40 cm from the eyes of the participants.
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Table 1 Means (SDs) for anthropological and psychometric data, and the recognition accuracy for the four word pair types.
Age Education Injury Assessment range CES-D STAI-S IES-R Perceptual-trauma Conceptual-trauma Perceptual-neutral Conceptual-neutral
PTSSþ group
PTSS group
t-test
33.60(11.46) 11.53(2.80) 3.87(0.83) 21.93 (20.91) 14.73(4.78) 44.23(8.28) 43.00(6.60) 2.60 (1.12) 1.07 (0.96) 1.13 (0.99) 0.67 (0.72)
29.73(9.86) 12.67(3.50) 3.53(0.64) 19.40 (12.63) 14.05(5.98) 42.00(7.27) 20.07(5.31) 2.00 (0.85) 1.20 (1.15) 1.73 (1.03) 1.13 (0.99)
t t t t t t t t t t t
¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
0.99, p > .3 0.98, p > .3 1.23, p > .2 0.40, p > .7 0.34, p > .7 0.78, p > .4 10.48, p < .0001 1.66, p > .1 0.35, p > .7 1.62, p > .1 1.47, p > .1
Note: PTSSþ group: group with PTSD symptoms; PTSS group: group without PTSD symptoms; Education: years of education; Assessment range: days between the accidents and the assessment; CES-D: score on the Epidemiological Studies Depression Scale; STAI-S: score on the State-Trait Anxiety Inventory-State; IES-R, scores on the Impact of Event Scale Revised. Perceptual-trauma, conceptual-trauma, perceptual-neutral, and conceptual-neutral referred to the four word pair types respectively. The df for all t-tests was 28.
Two types of words (perceptual and conceptual) were chosen as cue words. Because recall memory is better for pictures (e.g., objects) than for words (e.g., objects’ names) (Paivio, Rogers, & Smythe, 1968), we used verbal stimuli as cues only. In order to exclude potential confounding factors, we chose visual perceptual words only. Two undergraduates majoring in psychology chose 50 words from the Corpus for Studies of Modern Chinese (25 of each type). Then, these 50 words were rated on a 7-point scale from “1 ¼ evokes perceptual memory only” to “7 ¼ evokes a conceptual impression only” by 16 other undergraduates with different majors. The final word list contained those rated either in the top 10 words (for conceptual words, the mean score was 6.56 ± 0.24, and the word frequency was 93.37 ± 57.20 per million) or in the bottom 10 words (for perceptual words, the mean score was 1.42 ± 0.20, and the word frequency was 93.78 ± 54.69 per million). These two types of words had significantly different perceptualconceptual ratings, t (19) ¼ 54.62, p < .0001, but did not differ in word frequency, t (19) ¼ 0.02, p > .9. In each case, two words were used for the practice phase, and eight for the study phase. The target words were either trauma-related or neutral. The trauma-related words were based on those used by Amir et al. (2009) and Brennen et al. (2007). The words were translated and revised for the orthopedic inpatients; eight trauma related words were selected with a frequency of 19.62 ± 41.14 per million. 12 neutral words were selected (word frequency 34.90 ± 44.45 per million) matching the part of speech and frequency of the traumarelated words. The word frequency of the two target word types did not differ, t (12) ¼ 0.57, p > .6. Four of the neutral words were used for the practice phase and eight for the study stage. Cue words and target words were then paired randomly to form four different types of word pairs: perceptual-trauma, perceptualneutral, conceptual-trauma, and conceptual-neutral word pairs. To ensure that each cue and its paired target word were not naturally associated, we asked the same 16 students who had rated the cue words to give the first five perceptual and first five conceptual words that came to mind when presented with the target words (modified from Lupien et al., 1994). None of the target words generated the paired cue words used. The word pairs used in the study are listed in the Appendix.
2.2.2. Associative recognition task The task consisted of a practice phase, a study phase, and a cuerecognition phase. During the practice phase, four word pairs were
presented (two perceptual-neutral word pairs and two conceptualneutral word pairs) to familiarize participants with the procedure. In the study phase, 16 word pairs different from those in the practice phase (including all four word pair types; each type had four word pairs) were shown in random order that changed with each participant. Each word pair was shown only once for 5 s during 1.5 s intervals. Participants were asked to try their best to memorize all the word pairs and were told that later there would be a cue-recognition task about these pairs. The cue-recognition phase tested explicit memory performance for the target words from the 16 pairs that were presented. Participants were presented with two sheets of test paper: Sheet A listed all the cue words shown in the study phase, and Sheet B listed 16 target words and 4 distractors. Participants were asked to recognize the target words that had been paired with the cue words in the study phase. Recognition accuracy was calculated as the dependent variable. 2.2.3. Self-report questionnaires Trauma symptoms. The IES-R (Weiss & Marmar, 1997) is a 22item questionnaire based on the DSM-IV criteria for PTSD: intrusive thoughts, avoidance, and hyperarousal. Participants were asked to rate items based on a stressful (traumatic) event. The modified instructions that participants received were: “Individuals may experience some of the disturbances mentioned below after experiencing a stressful life event that involved actual or potential death or serious injuries, or a threat to one's physical health, associated with feelings of horror, hopelessness, or terror (e.g., motor-vehicle accidents, work-related accidents, or losing loved ones). Please choose an event that affected your emotion/mood for a while, and give a brief description below, then rate the items based on your feelings within the last 7 days. You can choose the event that caused your hospitalization, or anything that adversely impacted your mood/feelings or has worsened your life.” All of the 30 participants identified the accidents which caused their current injury as the traumatic event. Each item was rated on a weighted 4point scale (0 ¼ not at all, 4 ¼ often) for frequency of occurrence in the past 7 days. Total scores were calculated in the current study. In our sample, the Cronbach's alpha of the IES-R total was a ¼ .93. Depression. The Chinese version of the CES-D is a self-rated depression symptom questionnaire in which 20 items are rated on a 4-point Likert scale (Radloff, 1977). The questionnaire asks participants about their feelings or symptoms during the recent seven days. The Cronbach's alpha for the CES-D in the present sample was a ¼ .95. State Anxiety. The state form of the Chinese version of the StateTrait Anxiety Inventory (STAI-S; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1983; in Wang, Wang, & Ma, 1999) was used to measure the state anxiety of participants during the prior week. This scale is composed of twenty items evaluating subjective and transitory feelings such as tension, nervousness, and worry on a 4point scale. The Cronbach's alpha in the current sample was a ¼ .92. Miscellaneous measures. The anthropologic and past experience questionnaire was a self-constructed questionnaire, which included basic anthropologic information, diagnoses and medical history, and questions about how participants perceived their injury. The questionnaire screened participants for a history of trauma, neurologic, or psychiatric disorders. 2.2.4. Manipulation check In the manipulation check phase, participants rated each word on Sheet B (16 target words and 4 distractors) along the two dimensions of arousal and pleasantness, each on a scale from 0 to 4. The arousal rating was labeled “very stressful” to “very relaxing”,
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while the pleasantness dimension was rated from “very painful” to “very pleasant”. 2.3. Procedure The entire study was carried out on the orthopedic ward. Participants were informed verbally and in writing that the study may involve some unpleasant words and that as it was voluntary, they could withdraw at any point without reason. All participants gave informed consent before starting the study. The study was approved by the Committee for Protecting Human and Animal Subjects at Peking University. After receiving clear instructions on the procedure, the associative learning task was conducted using an IBM laptop. After the word pairs had all been presented, the experimental software started to count the time for a 10-min retention interval. During this time, participants filled out the Chinese version of STAI-S. After performing this task for 10-min, the cue-recognition task began, and the rest of the inventory was completed at the end of the experiment. After the manipulation check phase, participants were compensated for their time (￥10; about $ 1.61). 3. Results As planned and expected, the two groups differed significantly on IES-R scores; the PTSSþ and PTSS groups did not, however, statistically differ on any other baseline variable, including demographic variables (e.g., gender, age, education level), assessment range (i.e., days after the accidents), and trauma exposure severity (see Table 1). 3.1. Manipulation check Participants’ ratings of the target words were examined using 2 (group: PTSSþ group vs. PTSS group) 2 (target type: traumarelated vs. neutral type) repeated measures ANOVAs. Traumarelated target words were rated significantly more stressful than neutral target words, F (1, 28) ¼ 106.66, p < .0001. The group and group by target word type interaction effects were not significant. Moreover, the trauma-related target words were rated significantly more painful than neutral target words, F (1, 28) ¼ 94.37, p < .0001. Again, the group and group by target type interaction effect were not significant. 3.2. Associative bias We computed a 2 4 (group: PTSSþ group versus PTSS group word pair type: perceptual-trauma, perceptual-neutral, conceptual-trauma, and conceptual-neutral) repeated measures ANOVA to investigate whether there was an associative bias towards specific pair types. A significant effect of word pair type, F (3, 84) ¼ 26.25, p < .0001, h2partial ¼ .48, and a significant group by word pair type interaction effect, F (3, 84) ¼ 5.05, p ¼ .003, h2partial ¼ .15, together indicated that the recognition accuracy differed when the word pair type changed and that the groups showed different patterns in these recognition performances (Fig. 1). However there was no group effect, F (1, 28) ¼ 0.26, p > .6, h2partial ¼ .01. The post hoc test aimed at comparing the performance of the two groups for every word pair showed that participants from both groups recognized a similar number of the various word pair categories (Table 1). We then evaluated the effect of word pair type in each group. Repeated measures ANOVA in the PTSSþ group showed a significant effect of word pair types, F (3, 42) ¼ 29.85, p < .0001, h2partial ¼ 0.68. Pairwise comparisons using Bonferroni correction
Fig. 1. Groups by word pair type interaction. The Figure shows bar chart of recognition results for PTSSþ and PTSS groups. PeT: perceptual-trauma word pairs; PeN: perceptual-neutral word pairs; CeT: conceptual-trauma word pairs; CeN: conceptualneutral word pairs. **p < .0001 between word pairs.
showed that the recognition accuracy of perceptual-trauma word pairs was significantly greater than that of perceptual-neutral word pairs, mean difference (MD) ¼ 1.53, p < .0001, conceptual-trauma (MD ¼ 1.47, p < .0001), and conceptual-neutral word pairs (MD ¼ 1.93, p < .0001). There was no difference in the recognition accuracy of the latter three, indicating that the PTSSþ group was better at recognizing perceptual-trauma word pairs (Fig. 1). In the PTSS group, the repeated measures ANOVA also showed a significant word pair type effect, F (3, 42) ¼ 5.32, p ¼ .003, h2partial ¼ .28. Follow-up pairwise comparisons (with Bonferronicorrection) showed a significant difference between the perceptual-trauma and conceptual-neutral word pairs (MD ¼ 0.87, p ¼ .026). None of the other effects reached the level of statistical significance.
3.3. Memory bias towards different cues and targets The recognition data were submitted to a 2 2 2 (group: PTSSþ group versus PTSS group cue word type: perceptual cue versus conceptual cue word target word type: trauma-related versus neutral) ANOVA with repeated measures on the first factor in order to test whether there was a memory bias towards a cue type or a target type. The cue word type effect, F (1, 28) ¼ 32.98, p < .0001, h2partial ¼ .54, and target word type effect were significant, F (1, 28) ¼ 34.97, p < .0001, h2partial ¼ .56, indicating that word pairs with a perceptual cue word or a trauma-related target word were more easily memorized. The group effect was not significant, F (1, 28) ¼ 0.26, p > .6, h2partial ¼ .01, suggesting that the two groups had similar recognition accuracy toward each word pair. The cue word by target word interaction effect was significant, F (1, 28) ¼ 8.15, p ¼ .008, h2partial ¼ 0.23. Simple main effect analyses with Bonferroni-correction showed that all participants recognized perceptual cues better than conceptual cues, regardless of the target types (for trauma-related targets, MD ¼ 1.17, p < .0001; and for neutral targets, MD ¼ 0.53, p ¼ .004). The effect of target word by group interaction effect was significant, F (1, 28) ¼ 16.99, p < .0001, h2partial ¼ .38. Further analyses for this target word by group interaction showed that the PTSSþ group had a significant difference regarding the recognition performance between trauma targets and neutral targets, MD ¼ 1.87, p < .0001, whereas the PTSS group did not have a different recognition accuracy between two target types, MD ¼ 0.33, p > .2. However, the word cue by group interaction effect was not significant, F (1, 28) ¼ 1.03, p > .3,
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h2partial ¼ .04. No significant effect on the triple interaction effect was found, F (1, 28) ¼ 1.41, p ¼ .061, h2partial ¼ .12. 4. Discussion The goal of the current study was to examine the difference between traumatized individual with high versus low PTSD symptomatology on accuracy of recognition for perceptual cues and trauma-related target words. We hypothesized that the PTSSþ group would show a memory bias towards word pairs that contained trauma-related or perceptual words, and show an associative bias toward perceptual-trauma word pairs. In contrast, we did not expect the PTSS group to differ in the four word type pairs. As expected, the analysis of associative recognition indicated that the two groups have different memory patterns. The PTSSþ group showed better recognition accuracy of perceptual-trauma word pairs as compared to the other three word pairs. However, there was no difference between the other three, indicating that traumatized individuals who developed PTSD symptoms more easily associate perceptual stimuli with trauma-related information. This result is in accord with our hypothesis and may have implications for understanding intrusive memories. The current study showed that the PTSSþ group was better able to form new associations between perceptual stimuli and trauma information compared to other combinations. This association bias might be the mechanism underlying intrusive memories and the trigger stimuli, as it has been commonly reported that perceptual rather than conceptual stimuli compose most of the triggers of intrusive memory (Brewin et al., 1996; Ehlers & Clark, 2000; Ehlers et al., 2004; Foa et al., 1989). Future research with an objective of clarifying and/or understanding the voluntary and involuntary memory encoding of trauma could help guide the development of exposure based treatments for PTSD. Compared to the PTSS group, the PTSSþ group exhibited trauma-related facilitation in explicit memory. This is consistent with many previous studies (e.g., Brennen et al., 2007; Ehlers & Clark, 2000; Foa et al., 1989; Golier et al., 2003) and suggests that attention is easily drawn to stimuli that foreshadow or remind in€ 2002). dividuals about the trauma (Paunovic, Lundh, & Ost, As for the memory pattern of the PTSS group when compared with the PTSSþ group, the results point to a memory bias toward perceptual word pairs. Although there was no significant difference between the recognition of two targets words, the emotional memory-enhancement effect along with the bias for perceptual stimuli may explain the greater recognition of perceptual-trauma word pairs as compared to conceptual-neutral word pairs among participants in the PTSS group. This is in line with the notion that people are generally better at memorizing negative information than neutral information (Hamann, 2001; Kensinger & Corkin, 2003) Consistent with the model of PTSD proposed by Ehlers and Clark (2000), we observed that individuals with PTSD symptoms generally find it easier to memorize perceptual than conceptual words. In our study, participants only had a short time to process and memorize the word pairs, and it is possible that this time was insufficient for information to enter the deeper phase of conceptual processing. Therefore, it is possible that words that contained more concrete and perceptual information could be more easily recognized than words that contained conceptual and abstract information (e.g., Paivio, 1965), just as pictures are more easily remembered than words (e.g., Paivio, et al., 1968). The two groups did not differ in their recognition of word pair types, suggesting that the symptoms may not generally influence the non-practiced short-delay associative memory. This finding is in accordance with many previous studies (e.g., Amir et al., 2009;
Johnsen, Kanagaratnam, & Asbjørnsen, 2008; LaGarde, Doyon, & Brunet, 2010). It should be noted, however, that the differences were only significant between word pairs but not between groups. Therefore, it is not possible to exclude learning difficulties as an explanation of the findings. An alternative way to explain the results may be that the perceptual cues were easier to memorize than conceptual cues because the former tend to be more concrete and the later more abstract (e.g., Paivio, 1965). In addition, the memory enhancement for trauma-related targets may be due to the emotional word enhancement effect as discussed above (e.g., Kensinger & Corkin, 2003). These effects could partially explain the cue by target interaction found in all the participants together, and the absent between group effect. However, the two groups still showed different patterns when compared with each other. For instance, the memory enhancement of trauma-related targets was found only in PTSSþ group and for the PTSS group only the cue types reach the level of significance. The following limitations should be considered when interpreting these results. First, the sample size was modest, which limits the generalizability of the findings. Second, the PTSSþ group reported elevated levels of PTSD symptoms on the IES-R suggestive of a PTSD diagnosis, but a clinician based interview diagnosis of PTSD was not conducted. Prior studies suggest that the occurrence of PTSD symptoms one month post-trauma is one of the major predictors of subsequence PTSD (e.g., Hamanaka et al., 2006; Rothbaum, Foa, Riggs, Murdock, & Walsh, 1992) and many individuals with PTSD symptoms within months presented similar memory characteristics which were associated with chronic PTSD (e.g., Brandes, et al., 2002). However, some people recover spontaneously, whereas others show delayed PTSD. Therefore, the observed effects may be a weakened reflection of real-life trauma situations. Future studies using patient samples of clinically diagnosed PTSD would strengthen the results. Moreover, there was no healthy control group without any exposure to potentially traumatizing events. However, since our primary aim was to explore the differential features between traumatized individuals who developed PTSD symptoms and those who did not, a comparison between these two groups appeared sufficient for this purpose. In addition, we did not have raters rate the cue words on an emotional dimension, and participants were not instructed to rate the target words on a perceptual-conceptual level. However, we did not intend to compare the accuracy of cue words and target words. Therefore, it is not believed that this omission impacted the main purpose or the results of the study. Finally, only verbal stimuli was used to minimize potential confounders, so it is possible that picture stimuli might have produced different results. More profound understanding on the memory mechanism of PTSD will benefit from future studies using various memory materials and investigating both short-term and long-term memory characteristics. In sum, the current study showed that individuals with PTSD symptoms exhibit a biased association between perceptual stimuli and trauma words, whereas low symptom participants do not. Our findings provide partial support for the notion that intrusive memories are specific to the trauma-related event and perceptual cues of that trauma rather than to a general perceptual memory bias. These results are in line with the cognitive model by Ehlers and Clark (2000). Acknowledgments The data were collected partly for the first author's undergraduate thesis under the guidance of the third and the forth authors. The first author would like to thank and acknowledge Zhenzhen Liu, Yu Liu, Xiaonan Liu, Dr. Elizabeth A. Mundy, Dr. Iain Bruce,
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Hongbo Yu and Dr. Arlene T. Gordon-Hollingsworth for their kind assistance and support during the development of this study and in revising the manuscript. This manuscript was supported in part by China Scholarship Council (201306010054) awarded to the first author.
Appendix. Chinese (English) pairs used in the study
Word pair types
Pairs used in the study phase
白云(cloud) e 死亡(death), 图画(picture) e 车祸(accident), 绿色(green) e 绝望(despair), 鲜花(flower) e 骨折(fracture) 概念(concept) e 离婚(divorce), 科学(science) e 撞击(crash), 原因(reason) e 犯罪(criminal), 义务(obligation) e 截肢(amputation) Perceptual- 眼睛(eye) e 居住(living), 小狗(dog) e 交易(trade), neutral 月亮(moon) e 条例(rule), 大海(sea) e 竹竿(bamboo bar) Conceptual- 哲学(philosophy) e 记载(recording), 方法(methodology) e neutral 朝廷(royal court), 事件(event) e 冷藏(refrigerate), 直接(direct) e 古装(ancient costume) Pairs used in the practice phase 椰子(coconut) e 鸡蛋(egg), 生活(life) e 元旦(new year), 劳动(labor) e 动物(animal), 电视(television) e 植物(botany) Perceptualtrauma Conceptualtrauma
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