Negative words enhance recognition in nonclinical high dissociators: An fMRI study

www.elsevier.com/locate/ynimg NeuroImage 37 (2007) 323 – 334

Negative words enhance recognition in nonclinical high dissociators: An fMRI study Michiel B. de Ruiter, a,⁎ Dick J. Veltman, a,b R. Hans Phaf, c and Richard van Dyck b a

Department of Psychiatry, Academic Medical Center, Amsterdam, The Netherlands Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands c Psychonomics Department, University of Amsterdam, The Netherlands b

Received 9 January 2007; revised 10 April 2007; accepted 11 April 2007 Available online 21 May 2007 Memory encoding and retrieval were studied in a nonclinical sample of participants that differed in the amount of reported dissociative experiences (trait dissociation). Behavioral as well as functional imaging (fMRI) indices were used as convergent measures of memory functioning. In a deep vs. shallow encoding paradigm, the influence of dissociative style on elaborative and avoidant encoding was studied, respectively. Furthermore, affectively neutral and negative words were presented, to test whether the effects of dissociative tendencies on memory functioning depended on the affective valence of the stimulus material. Results showed that (a) deep encoding of negative vs. neutral stimuli was associated with higher levels of semantic elaboration in high than in low dissociators, as indicated by increased levels of activity in hippocampus and prefrontal cortex during encoding and higher memory performance during recognition, (b) high dissociators were generally characterized by higher levels of conscious recollection as indicated by increased activity of the hippocampus and posterior parietal areas during recognition, (c) nonclinical high dissociators were not characterized by an avoidant encoding style. These results support the notion that trait dissociation in healthy individuals is associated with high levels of elaborative encoding, resulting in high levels of conscious recollection. These abilities, in addition, seem to depend on the salience of the presented stimulus material. © 2007 Elsevier Inc. All rights reserved.

Introduction Although dissociative experiences have a pathological connotation, they are common in everyday life. The present study derives from the standpoint that in nonclinical individuals, dissociation is related to enhanced, instead of diminished cognitive abilities. These abilities are hypothesized to mediate memory

⁎ Corresponding author. Department of Clinical Neuropsychology, Faculty of Psychology and Education, VU University, Amsterdam, The Netherlands. Fax: +31 20 5988971. E-mail address: [email protected] (M.B. de Ruiter). Available online on ScienceDirect (www.sciencedirect.com). 1053-8119/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2007.04.064

retrieval. To this end, behavioral and neuroanatomical data were collected in a recognition task from college students that differed in their level of trait dissociation. Spiegel and Cardeña (1991) defined dissociation as a structural separation of mental processes that are ordinarily integrated. This definition encompasses both pathological and nonpathological conditions. In dissociative amnesia, psychiatric patients are assumed to block (i.e., dissociate) burdensome memories from entering conscious awareness. On the other side of the dissociative spectrum lies absorption, in which a person might be so engaged in some form of mentation (e.g., reading a book), that the current surroundings are not noticed. Apparently, they are dissociated from awareness. It is not hard to relate the latter phenomenon to cognitive abilities like attention, working memory and concentration. In line with this view, several studies from our and another group have indicated that nonclinical dissociation is linked to enhanced attention (de Ruiter et al., 2003; DePrince and Freyd, 1999) and working memory capacity (de Ruiter et al., 2004; Elzinga et al., 2007; Veltman et al., 2005). The findings that dissociative experiences are common in the population (Kihlstrom et al., 1994; Putnam et al., 1996; Ross et al., 1990; Vanderlinden et al., 1991) and that a strong genetic component is implicated (Becker-Blease et al., 2004; Jang et al., 1998), support the view that dissociation not necessarily results from traumatic life events. Memory studies on dissociation have mainly investigated the avoidant encoding hypothesis, which postulates that high-dissociative, traumatized individuals direct attention away from threatening information to prevent it from being processed on a semantic level, thus providing an explanation for the clinical observation of amnesia for traumatic life events (Cloitre, 1992; Cloitre et al., 1996). This hypothesis has been examined in several patient and student groups characterized by high levels of trait dissociation with the ‘directed forgetting’ paradigm. This approach, however, has generated mixed results. Whereas some studies did report impaired memory for trauma-related or generally affectively negative words in high dissociators (DePrince and Freyd, 2004; Moulds and Bryant, 2002, 2005), several studies failed to find indications of trauma-related memory impairment (e.g., McNally et al., 1998, 2001, 2005).

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Moreover, also enhanced, instead of impaired memory performance has been reported (Cloitre et al., 1996; Elzinga et al., 2000; Korfine and Hooley, 2000) which has led to the suggestion by our group that high dissociators are characterized by high levels of elaboration learning at encoding and retrieval, which is enabled by highly developed working memory and attention capacities and results in generally higher levels of conscious recollection (de Ruiter et al., 2006; Elzinga et al., 2000). Two explanations may be put forward to account for the inconsistent findings on dissociation and memory retrieval. Firstly, dissociative abilities may be counteracted by the psychiatric status of the participants under study. For instance, patients may be less concentrated during a test session than healthy individuals, and the neuroendocrinological effects of stress episodes on memory (e.g., Wolf, 2003) may also have detrimental effects. Moreover, patient groups are often older and have lower educational levels, characteristics that are also likely to have detrimental effects on memory performance. Secondly, the directed forgetting paradigm may not be the best approach to investigate the effect of dissociation on elaborative and avoidant encoding. Because in this paradigm, participants are instructed to forget or remember a stimulus after it has been presented, initial encoding of the stimulus has already occurred. In addition, directed forgetting entails an intentional learning paradigm: participants are aware of the fact they are engaged in a memory task, which may influence their performance (e.g., because of demand characteristics or the application of alternative mnemonic strategies). To circumvent these problems, in the present study memory retrieval was examined in a group of nonclinical participants, and we employed a levels of processing paradigm (Craik and Lockhart, 1972), in which participants have to make a semantic (i.e., deep) or a non-semantic (i.e., shallow) decision regarding verbal stimuli. Semantic judgments (in this case: affective evaluation), by definition, require elaborative encoding and should reveal the enhancement of this process by dissociative abilities. By adding a non-semantic or shallow encoding condition, we were also able to investigate avoidant encoding. Performing a difficult non-semantic task possibly enabled high dissociators to employ their abilities to ignore stimulus meaning, in particular of negative stimuli. This would be in line with the reported high working memory capacity of high dissociators, as a high working memory capacity is related to an increased ability to inhibit irrelevant stimuli (e.g., Conway et al., 2001). Moreover, presenting both affectively neutral and negative stimuli permitted us to examine if the amount of elaborative and avoidant encoding depended on stimulus valence. Although in a previous study (de Ruiter et al., 2003), attention was drawn towards instead of away from affectively negative stimuli in a shallow encoding condition, in the current study we used a shallow encoding task that was more difficult than the one in de Ruiter et al. (2003) (alphabetical judgment instead of detection of the letter ‘A’). This approach might be better suited to mimic avoidant encoding in a laboratory setting. In the present study, we sought to investigate the elaborative encoding view on dissociation on a behavioral and a neuroanatomical level. Previous neuroimaging work points to the involvement of the left inferior frontal gyrus (LIFG) in verbal encoding, reflecting semantic elaboration in working memory, as well as the medial temporal lobe (MTL), reflecting intermediate memory storage (e.g., Addis and McAndrews, 2006; Kirchhoff and Buckner, 2006; Rugg, 2002; Squire and Knowlton, 2000). At retrieval, MTL activity has been described as well, thought to reflect memory

recovery, whereas posterior parietal cortex has been suggested to be involved in the actual experience of conscious memory (e.g., Daselaar et al., 2004; Rugg et al., 2002; Shannon and Buckner, 2004; Wagner et al., 2005). Because of their enhanced attentional and working memory capacities, the general hypothesis of the present study was that high dissociators are characterized by high levels of semantic elaboration at encoding and high levels of conscious recollection at retrieval. This would result in high levels of LIFG and MTL activity at encoding, and high levels of memory performance and MTL and parietal cortex activity, at retrieval. Employing a shallow encoding condition enabled us to investigate if dissociative abilities were also related to avoidant encoding, leading to low levels of LIFG and MTL activity at encoding, and low levels of memory performance and MTL and parietal cortex activity, at retrieval. In sum, to investigate the influence of nonclinical dissociation on elaborative and avoidant encoding, a deep vs. shallow encoding paradigm was employed while measuring fMRI in low- and highdissociative college students both at encoding and retrieval. We expected high dissociators to show higher levels of semantic elaboration at deep encoding, as reflected by higher activity levels in LIFG and MTL compared to low dissociators. At retrieval, we expected higher levels of recollection for high than low dissociators for deeply encoded items, as reflected by higher memory performance, and higher concomitant activity levels in MTL and parietal cortex. A demanding shallow encoding task enabled us to test if high levels of trait dissociation were related to avoidant encoding, which predicts lower activity levels in LIFG and MTL for high compared to low dissociators at encoding and a subsequent decrease in memory performance and MTL and parietal activation at retrieval. Affectively neutral and negative stimuli were presented to test if our predictions depended on the valence of the presented stimulus material. Method Participants Participants were selected on the basis of their scores on the Dissociation Questionnaire (Dis-Q; Vanderlinden et al., 1993), which was administered in a general ‘test week’ (in exchange for course credit) and in unrelated experiments to approximately 200 psychology students. The Dis-Q is a Dutch self-report measure of dissociative experiences. It consists of 63 items and has four subscales: Identity confusion, Loss of control, Amnesia, and Absorption. Internal consistency of the Dis-Q is good (Cronbach's alpha is 0.96 for the total scale). The test–retest reliability is 0.94 for the total score. A congruent validity (r = 0.85) between Dis-Q and another dissociation questionnaire (DES; Bernstein and Putnam, 1986) was obtained by Vanderlinden et al. (1993). Participants scoring in highest and lowest quartiles were contacted for participation. Eventually, 23 students with low (Dis-Q 1.25 ± 0.13, mean age 21.9 ± 2.5, 15 females) and 20 students with high (Dis-Q 2.30 ± 0.37, mean age 21.4 ± 3.8, 10 females) Dis-Q scores participated in the experiment. All participants reported to be right handed. They were informed that they were invited on the basis of their score on the questionnaire but they were unaware whether they scored high or low. During the experiment, the experimenter was also unaware of the scores of the participants. Participants received course credit or money (€12,–) for their participation. Participants had normal or corrected-to-normal vision, indicated

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not to be dyslexic, not to use prescription medication or recreational drugs, to have no history of mental or sustained physical illness, and had Dutch as their first language. Written informed consent was obtained from all participants. Material The stimuli consisted of 240 Dutch words. Half of the words had a neutral connotation; the other half had a negative connotation. The valence of the stimulus material was validated in a perceptual clarification task (Ter Laak, 1992, unpublished Master's thesis), in which these words were recognized most consistently and rapidly under minimal presentation conditions as neutral and negative words. Word length varied between 3 and 14 letters. Neutral and negative words were matched for word length, word type (verbs, adjectives and nouns) and frequency of usage. The use of abstract words was avoided. In each of the words, two letters were underlined. Half of the neutral and half of the negative words contained underlined letters that were in ascending alphabetical order (e.g., satan). The other half of the neutral and negative words contained underlined letters that were in descending alphabetical order (e.g., monster). For each participant, a subset of 40 neutral and 40 negative words was randomly selected for the deep encoding task (affective evaluation). For both subsets, half of the words contained underlined letters that were in ascending alphabetical order and half of the words contained underlined letters that were in descending alphabetical order. Another subset of 40 neutral and 40 negative words was randomly selected for the shallow encoding task (alphabetical decision). Again, for both subsets, half of the words contained underlined letters that were in ascending alphabetical order and half of the words contained underlined letters that were in descending alphabetical order. Finally, the remaining 40 neutral and 40 negative stimuli were designated as ‘new’ words. Later in the experimental session, all words were presented in a surprise recognition task. Before each experiment, the trials were randomly intermixed into blocks. For the encoding tasks, these blocks consisted of four neutral words, four negative words and four baseline items (two ‘press left’ and two ‘press right’ trials) in randomized order. Consequently, during both encoding tasks ten blocks of twelve stimuli were presented in a row. For the recognition task, the blocks consisted of four neutral and four negative words from the deep encoding task, four neutral and four negative words from the shallow encoding task, four neutral and four negative new words and four baseline trials in randomized order. Consequently, during the recognition task ten blocks of 28 stimuli were presented in a row. To prevent primacy and recency effects in the recognition task, three buffer words preceded and followed both encoding tasks. In addition, to let participants get used to the unexpected recognition task, two buffer words preceded this task. Procedure Participants were informed beforehand that the goal of the experiment was to gain insight into neural correlates of language processing. Prior to scanning, all participants practiced both encoding tasks outside the scanner on a personal computer. In the scanner, a device with response buttons was positioned near the right hand of the participant. In all task blocks, participants had to respond in a forced choice fashion by pushing the left button with the index finger or the right button with the middle finger. Stimuli

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were presented in a self-paced fashion, although a time limit of three seconds was maintained in case of non-responses. On each trial, response options were indicated at the bottom of the screen by an arrow pointing to the left (‘negative’; ‘descending’; ‘seen’/‘negatief’, ‘aflopend’, ‘gezien’) and right (‘neutral’; ‘ascending’, ‘not seen’/‘neutraal’, ‘oplopend’, ‘niet gezien’). It was explained beforehand that pushing the left button corresponded to the left arrow and pushing the right button corresponded to the right arrow. Scores were only registered when the participant responded within the 3-s time limit. After the time limit had passed or the response was made, a 2-s interstimulus interval (ISI) started, taken from stimulus offset to the onset of the next stimulus. Forty baseline trials were added to each task (both encoding tasks as well as the recognition task). In a baseline trial, participants were presented with a cue to press either the left button (‘⋘left’/‘⋘links’) or the right button (‘right⋙’/‘rechts⋙’). Both types of baseline trials occurred equally often. After a pause of approximately 15 min, during which a structural MRI scan was acquired, the recognition task was presented unannounced. Participants were required to judge whether or not each word had appeared previously in one of the encoding tasks. The order of the two encoding tasks was counterbalanced across participants within each participant group. Before each MRI recording (encoding, structural MRI, recognition) and after the recognition task, participants were asked to rate their subjective distress on a 100-point scale (SUD-S; 0 = not at all distressed, 100 = extremely distressed). Scanning details Functional MR imaging was performed at the Dept. of Radiology of the outpatient clinic of the Vrije Universiteit Academic Hospital, using a 1.5-T Sonata whole-body system (Siemens AG, Erlangen, Germany) equipped with a head volume coil. Axial multislice T2*-weighted images were obtained with a gradient-echo planar sequence (TE = 60 ms, TR = 3.306 s, 64 × 64 matrix, 38 slices, 3 × 3 mm in-plane resolution, slice thickness 3 mm with a 1-mm interslice gap), covering the entire brain. Each session consisted of two functional MRI subsessions. During the first subsession, scans for both encoding task were acquired, whereas during the second subsession, scans for the recognition task were acquired. Between the subsessions, a T1-weighted structural 3D gradient-echo MR scan (0.78 × 0.78 × 2 mm voxel size) was acquired. Data analysis Behavioral data With respect to the encoding tasks, error rates and mean reaction times (RT) for correct responses were fed into separate omnibus ANOVAs with the between-subject factor Group (low and high dissociative) and the within subject factors Task (deep and shallow encoding) and Word type (neutral and negative), resulting in 2 × 2 × 2 designs. With respect to the recognition task, based on proportions of hits and false alarms, old/new discrimination accuracy ‘Pr’ (= Hit − FA) and response bias ‘Br’ (= FA / (1 − Pr)) were calculated separately for deeply and shallowly encoded neutral and negative items according to two-high-threshold theory (Snodgrass and Corwin, 1988). These two signal detection measures were analyzed separately in three-way ANOVAs, employing the between-participant factor group (two levels: low and high dissociative) and the two within-participant factors study

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status (two levels: deep/shallow) and valence (two levels: neutral/ negative). Reaction time data were analyzed employing a four-way ANOVA with the between-participant factor group (two levels: low and high dissociative) and the three repeated measures factors valence (two levels: neutral and negative), response type (two levels: old and new) and study status (three levels: deep, shallow and new). Experimental effects on RT resembled earlier findings. Because effects involving group not even approached statistical significance, however, RT results will not be reported here. Imaging data After discarding the first three scans of each time series to allow for a steady state to be induced, images were realigned, and spatially normalized into MNI space. The data were smoothed spatially with an 8-mm isotropic Gaussian kernel. Subsequently, data were band pass filtered and analyzed in the context of the General Linear Model, using delta functions convolved with the canonical hemodynamic response to model responses during each condition. For each participant, linear contrasts were computed for experimental effects. The resulting contrast images were then fed into a second level (random effects) analysis in SPM2 (Wellcome Department of Cognitive Neurology, http://www.fil.ion.ucl.ac.uk/ spm) and experimental effects were assessed for each group, as well as group by task interactions. Main effects for each group are reported at p b 0.05 corrected for multiple comparisons using the false discovery rate method (Genovese et al., 2002), with a cluster size restriction of 10 voxels. Interaction effects are reported at p b 0.001 uncorrected, masked with the appropriate main effect. Results Behavioral data Unless indicated otherwise, mean values and standard deviations are presented. SUD scores Subjective levels of distress (SUD-S), ranging from 0 to 100%, were subjected to an ANOVA with the between-subject factor Group (low and high dissociative) and the within-subject factor Time (before encoding, before structural scan, before recognition and after recognition) resulting in a 2 × 4 design. Scores did not reliably differ between low and high dissociators (before encoding: 26.5 ± 23.0 vs. 30.3 ± 19.7, F b 1; before structural scan: 26.5 ± 23.0 vs. 30.3 ± 19.7, F b 1; before recognition: 23.2 ± 20.9 vs. 30.2 ± 17.9, F(1,41) = 1.37, NS; after recognition: 17.1 ± 20.4 vs. 25.5 ± 16.6; F(1,41) = 2.19, NS). Encoding The proportion of correct responses and mean reaction times (RT) for correct responses was fed into separate omnibus ANOVAs with the between-subject factor Group (low and high dissociative) and the within-subject factors Task (deep and shallow encoding) and Word type (neutral and negative), resulting in 2 × 2 × 2 designs. The proportion of correct responses was higher in the deep than in the shallow encoding task (deep encoding: 0.92 ± 0.10, shallow encoding: 0.88 ± 0.19; F(1,41) = 4.69, p b 0.05). Responses were almost twice as slow at shallow than deep encoding, indicating that alphabetical decision was much more difficult than affective evaluation (deep encoding 976 ms ± 24, shallow encoding

1647 ms ± 29; F(1,41) = 390.67, p b 0.001). With affective evaluation, more neutral words were classified correctly than negative words (0.95 ± 0.01 vs. 0.88 ± 0.02) for low as well as high dissociators, probably reflecting the difficulty in selecting unambiguously negative stimulus material. In the alphabetical decision task slightly more negative than neutral words were classified correctly (0.89 ± 0.02 vs. 0.86 ± 0.02, F(1,41) = 7.09, p b 0.05), but this increase in performance was accompanied by a slowing of RT (neutral words: 1626 ± 31 ms, negative words: 1667 ± 29 ms; F(1,41) = 9.81, p b 0.005), demonstrating an emotional interference effect. No significant differences were found between low and high dissociators regarding proportion of correct responses and reaction times. Recognition Based on proportions of hits (old words correctly judged ‘old’) and false alarms (new words incorrectly judged ‘old’) in the recognition task, sensitivity ‘Pr’ (= Hit − FA) and response bias ‘Br’ (= FA / (1 − Pr)) were calculated separately for deeply and shallowly encoded neutral and negative items (Snodgrass and Corwin, 1988). Hit rates, false alarm rates, sensitivity (Pr) and response bias (Br) are shown in Table 1; sensitivity (Pr) is also depicted in Fig. 1. Response bias and sensitivity were subjected to separate omnibus ANOVAs. Conforming to expectations, sensitivity was much higher for deeply than shallowly encoded words (F(1,41) = 688.2, p b 0.001). Moreover, negative words were better remembered than neutral words (neutral words: Pr = 0.31 ± 0.02, negative words: Pr = 0.39 ± 0.01; F(1,41) = 18.8, p b 0.001). An Encoding × Valence interaction indicated that the beneficial effect of valence on memory performance was larger for deeply than shallowly studied items (F(1,41) = 7.06, p b 0.05). Most importantly, a Group × Encoding × Valence interaction (F(1,41) = 4.47, p b 0.05) indicated that for deeply encoded items, the valence effect on recognition memory was larger for high than low dissociators (F(1,41) = 6.37, p b 0.05), whereas it was about the same for shallowly encoded items (F(1,41) b 1, NS, see Fig. 1). Performing separate tests for low and high dissociators showed that the valence effect on Pr for deeply encoded words was not significant for low dissociators (F(1,22) = 2.94, p = 0.1), whereas it was for high dissociators (F(1,19) = 23.58, p b 0.0005). In order to determine whether the Group × Valence effect on Pr was mainly driven by neutral or negative stimuli, separate group comparisons were carried out for deeply encoded neutral and negative stimuli. Neither tests resulted in significant results (neutral items: F(1,41) = 2.21, NS; negative Table 1 Mean proportions (SD in parentheses) of hit rates, false alarm rates, sensitivity (Pr) and response bias (Br) for the different stimulus categories for low and high dissociators Group

Low dissociators

High dissociators

Stimulus valence

Neutral

Negative

Neutral

Negative

Hits deep Hits shallow False alarms Accuracy deep (Pr) Accuracy shallow (Pr) Response bias deep (Br) Response bias shallow (Br)

0.64 (0.14) 0.19 (0.10) 0.08 (0.06) 0.56 (0.13) 0.11 (0.09) 0.20 (0.15)

0.80 (0.09) 0.34 (0.12) 0.19 (0.11) 0.61 (0.11) 0.15 (0.11) 0.49 (0.19)

0.58 (0.14) 0.16 (0.09) 0.09 (0.07) 0.49 (0.17) 0.07 (0.09) 0.17 (0.12)

0.82 (0.06) 0.29 (0.16) 0.16 (0.09) 0.66 (0.08) 0.13 (0.13) 0.44 (0.19)

0.09 (0.06) 0.22 (0.11) 0.09 (0.07) 0.19 (0.11)

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Fig. 1. Memory performance (Sensitivity, Pr) in the recognition task of low and high dissociators for deeply and shallowly encoded neutral and negative words. Error bars show SEM.

items: F(1,41) = 2.61, NS). Therefore, it could not be determined which stimulus category mainly attributed to the Group × Valence interaction. Response bias was higher for deeply than shallowly encoded items (F(1,41) = 189.53, p b 0.05), and higher for affectively negative than neutral words (F(1,41) = 103.15, p b 0.05), indicating a higher tendency to generate a ‘yes’ response to these items. An interaction between encoding and valence (F(1,41) = 103.15, p b 0.05) reflected the fact that the tendency to respond ‘yes’ was particularly high for deeply encoded negative words. No significant differences were found between low and high dissociators regarding response bias (all Fs b 1). RTs indicated that ‘yes’ responses were generated faster than ‘no’ responses, irrespective of response correctness (F(1,34) = 10.24, p b 0.05). A Response × Condition interaction reflected relatively fast hits to deeply encoded words and fast rejections of new words (F(1,33) = 44.29, p b 0.05). Finally, Fast ‘yes’ response to negative words and slow ‘yes’ responses to neutral words accounted for a Response × Valence interaction (F(1,34) = 35.79, p b 0.05) and mirrored the higher response bias to negative than neutral stimuli. No group differences occurred regarding RT data.

Imaging data Results for random effects (RFX) analyses of the imaging data are summarized in Tables 2–5 and correspond to the 3D visualizations and sections depicting BOLD activity in Figs. 2 and 3. Tables 2 and 4 show RFX analyses for low and high dissociators separately. Tables 3 and 5 show RFX analyses on group interactions. For the sake of brevity, significant BOLD activations presented in Tables 2 and 4 are limited to brain areas that show significant group interactions. Because of their theoretical importance, inferior frontal gyrus activity at encoding (Table 2) and MTL activity at encoding and retrieval (Tables 2 and 4) is always listed. The direct contrast ‘recognition of deeply encoded negative vs. neutral words’ did not yield any significant task, nor group effects and is therefore not listed. Deep encoding of neutral stimuli In Fig. 2a, deep encoding of neutral stimuli contrasted against a non-mnemonic baseline is depicted for low and high dissociators (upper and lower panel, respectively). Broadly speaking, four brain areas can be distinguished that are in agreement with earlier findings on semantic processing (Jobard et al., 2003). Most importantly, robust activation of the left inferior frontal gyrus was found, reflecting the semantic elaboration of the neutral words. The medial frontal cortex was also activated, including the anterior

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cingulate and medial frontal gyrus. Another main area of activation was the left fusiform gyrus, situated in the ventral route, which probably reflects the visual analysis of written word forms (orthographic processing). Lastly, activation of the occipital cortex can be discerned, which reflects the fact that visual information is being presented. However, because most of these areas were not involved in the group interactions, they are not listed in Table 2a. Low dissociators generally showed higher levels of brain activation, reflected not only in larger clusters of activity, but also in spreading of activity to the right hemisphere. Significant group interactions in favor of the low dissociators were observed in the left temporal cortex, right occipital cortex and the right inferior frontal gyrus (Table 3a). Deep encoding of negative stimuli Deep encoding of negative stimuli tended to activate similar prefrontal regions as the neutral stimuli (e.g., LIFG) but to a greater extent, particularly for the high dissociators (Table 2b and Fig. 2b). In addition, high-dissociative participants showed activation in the left hippocampus. When directly comparing groups, high dissociators showed more activity in left inferior frontal gyrus (Table 3b), but the difference in hippocampal activity failed to reach significance. Shallow encoding A large cortical network was activated by the alphabetical decision task compared to the low level baseline (Fig. 2c). No differences were found between processing of neutral and negative words. Moreover, no significant group interactions were found. Affective valence in deep encoding To investigate the effect of a negative affective valence on semantic elaboration in low and high dissociators, we directly compared deep encoding of affectively negative and neutral verbal stimuli (Fig. 2d, left panel). A negative affective valence increased activity in prefrontal areas, i.e., LIFG and MFC (Table 2d). High dissociators showed a greater increase in MFC than low dissociators, as well as bilateral (as opposed to left-sided only) inferior frontal gyrus activity. Several areas in the temporal lobe were also more active for high dissociators. All these observations were supported by direct group comparisons (Table 3d). Importantly, in the latter analyses, greater right hippocampal activity was also found for high-dissociative participants (Fig. 2d, right panel), indicating a higher amount of intermediate memory storage for high than low dissociators. Affective valence across deep and shallow encoding To investigate the effect of affective valence irrespective of the amount of semantic elaboration, we compared all negative to all neutral stimuli presented at encoding. A network was activated that was similar to the valence effect in deep encoding (Fig. 2e, left panel and Tables 2e and 3e). In addition, activity in the left amygdala was found for high dissociators (Fig. 2e, left panel). At a slightly lower statistical threshold (p b 0.005), this difference in amygdala activation was also apparent in the group comparison (Table 3e). Recognition of deeply encoded neutral words Fig. 3a depicts activation of a large cortical network associated with recognition of deeply encoded neutral words (by comparing hits to deeply encoded neutral words to correct rejections of new

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Table 2 Encoding phase Region

l/r

(a) Deep encoding neutral N baseline Prefrontal Inferior l

r Temporal Occipital

l r

(b) Deep encoding negative N baseline Prefrontal Inferior l

r

Hippocampus

Low

High

Talairach

Z-score

BA

Talairach

Z-score

BA

− 45 24 −12 − 36 27 −6 − 51 39 −6

5.81* 5.53* 5.40*

47 47 47

4.71* 4.58* 3.73* 3.97* 3.80* 3.72*

47 47 11 46 9 45

48 18 − 9 42 21 − 15 − 57 − 36 3 24 − 96 21 39 − 84 −9 45 − 84 0

− 42 21 3 − 36 30 − 9 − 42 39 − 18 − 48 30 18 − 48 15 27 − 54 21 15

4.38* 3.67* 3.68* 6.13* 5.17* 5.02*

47 47 22 19 19 19

39 − 90 − 6 39 − 87 12 39 − 84 0

3.60* 3.38(*) 3.33(*)

18 19 19

− 51 24 −9 − 39 12 30 − 57 30 12 33 30 − 6 39 33 − 12

6.97* 6.04* 5.65* 4.10* 3.82*

47 9 46 47 47

− 36 30 − 9 − 57 33 6

5.45* 5.27*

47 45

33 24 −6 45 21 −6 54 30 18 48 39 21 − 27 − 15 − 15 − 33 − 21 − 12 − 18 − 12 − 18

4.63* 4.23* 3.79* 3.24* 3.57* 3.48* 3.54*

47 47 46 46

− 54 15 − 9 − 57 30 9 − 54 30 − 6 − 48 48 − 15 48 18 −3 − 9 57 63 − 15 51 27 − 9 63 21 − 9 24 51 − 63 − 36 − 6 − 33 6 − 33

4.5* 4.0* 4.0* 4.1* 4.2* 4.7* 4.2* 4.2* 4.4* 4.6* 4.0*

47 45 47 11 47 9 9 10 8 21 21

− 54 30 − 6 − 57 30 9

4.47* 4.40*

47 45

− 9 60 33 − 6 51 30 − 54 15 − 9 − 30 18 − 27 − 42 21 − 21 − 51 15 − 30 − 60 − 36 − 6 − 54 − 21 − 9 − 57 − 15 − 15 − 18 − 6 − 18

5.18* 4.21* 4.31* 4.20* 3.18(*) 3.56* 4.50* 3.80* 3.77* 4.13*

9 9 38 38 38 38 21 21 21

l

(c) Shallow encoding neutral + negative N baseline: no statistics reported (see text) (d) Deep encoding: negative N neutral Prefrontal Inferior l

− 54 21 −6 − 27 15 −21

4.7(*) 4.5(*)

47 47

− 15 60 30 − 9 57 15

4.2(*) 4.1(*)

10 10

− 63 − 33 − 6

3.69(*)

21

(e) Deep + shallow encoding: negative N neutral Prefrontal l − 54 30 −6 − 42 30 −15 − 39 24 –21 Medial l − 15 63 27 − 9 57 12 Temporal l − 63 − 36 − 3

4.77* 3.71* 3.61* 4.18(*) 4.02(*) 4.46*

47 47 47 10 10 21

Medial

r l

Temporal

l

Amygdala

l

Areas showing significant (p b 0.001) increase in activity in low- and high-dissociative participants. BA = Brodmann area (* = p b 0.05 corrected, (*) = p b 0.1 corrected, (1) = p b 0.005). (a) Deep encoding: neutral words compared to baseline, (b) deep encoding: negative words compared to baseline, (c) shallow encoding: words compared to baseline pooled for valence, (d) deep encoding: negative versus neutral words, (e) deep and shallow encoding pooled: negative versus neutral words.

M.B. de Ruiter et al. / NeuroImage 37 (2007) 323–334 Table 3 Encoding phase Region

Z-score

BA

Low N High (a) Deep encoding neutral N baseline Prefrontal Inferior r 36 39 − 6 Temporal l − 57 12 − 6 − 51 −30 3 − 60 −36 6 Occipital r 24 − 96 21

l/r

Talairach

3.5 3.56 3.46 3.35 3.95

47 22 22 22 19

High N Low (b) Deep encoding negative N baseline Frontal inferior l − 27 54 − 12

3.14

47

High N Low (d) Deep encoding: negative N neutral Prefrontal Medial l − 9 42 33 Inferior r 48 18 − 3 Temporal − 33 6 − 33 Hippocampus l − 33 −33 −9 r 24 − 15 − 18

3.1 3.2 4.0 3.4 3.3

9 47 21

High N Low (e) Deep + shallow encoding: negative N neutral Medial prefrontal l − 9 42 33 Insula l − 39 −3 −3 Temporal l − 63 0 − 6 − 63 −21 −15 Amygdala l − 21 −6 −18

3.21 3.62 3.21 3.11 2.94(1)

9 13 21 39

(c) Shallow encoding neutral + negative N baseline No significant group interactions

Areas showing significant (p b 0.001) group interactions between low- and high-dissociative participants. BA = Brodmann area. (1) = p b 0.005. (a) Deep encoding: neutral words compared to baseline, (b) deep encoding: negative words compared to baseline, (c) shallow encoding: neutral and negative words compared to baseline, (d) deep encoding: negative versus neutral words, (E) deep and shallow encoding pooled: negative versus neutral words.

neutral words). Next to the prefrontal areas that were also active at deep encoding (i.e., LIFG en MFC), dorsolateral prefrontal cortex activity was also apparent. Posterior parietal activity could also be discerned, in the inferior parietal lobule as well as medial posterior parietal cortex (posterior cingulate and precuneus complex). In general, activity was left lateralized, like in the deep encoding task, although right hemisphere activation was more apparent than for encoding. Group interactions for recognition of deeply encoded neutral words in favor of the high-dissociative group were found in two areas held to be associated with conscious recollection, namely the left posterior parahippocampal area (Fig. 3a, right panel), and the left inferior parietal lobule (Fig. 3a, left panel). Moreover, high dissociators showed more activity in the left temporal pole (Tables 4a and 5a). Recognition of deeply encoded negative words Recognition of deeply encoded negative stimuli elicited similar, albeit less extensive, cortical activation compared with recognition of neutral stimuli (see Fig. 3b). Z-scores for low dissociators were generally higher, but no significant group interactions occurred.

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Recognition of deeply vs. shallowly encoded words To obtain a pure estimate of recollection, our last analysis focused on the difference in neural activity between correctly recognized deeply and shallowly encoded words. Because memory for shallowly encoded items was too poor to obtain reliable estimates for neutral and negative hits separately (Table 1), we pooled these categories. As can be discerned in Fig. 3c, left panel, multiple posterior parietal regions that have been associated with conscious recollection were elicited in the high-dissociative group, whereas hardly any activation was found for the low-dissociative group. Also, multiple temporal areas were active for the high dissociators. Moreover, right posterior hippocampus and left amygdala activity was found for the high group (Fig. 3c, right and middle panel). It should be noted that these activations were only marginally significant after correction for multiple comparisons (Table 4c). Direct group comparisons indicated that an area in the right temporal cortex was more active for high than low dissociators (Table 5c) and with slightly lower thresholds, we also found interactions regarding the inferior parietal lobule, right posterior hippocampus and left amygdala. Discussion The goal of the present study was to investigate behavioral and neural correlates of memory functioning in a nonclinical population that differed in the extent of dissociative experiences. Employing a deep vs. shallow encoding paradigm, we were able to examine the influence of trait dissociation on elaborative and avoidant encoding, respectively. Our results provide evidence for the elaborative encoding hypothesis only. No behavioral or neuroanatomical indications were found for increased avoidant processing during shallow encoding by high dissociators. When the stimuli had been subjected to deep encoding, high dissociators showed a significantly larger increase in memory performance that was induced by affective stimulus valence. On the basis of the performance data alone, however, it could not be deduced whether this effect was mainly carried by neutral or negative stimuli. BOLD activations at encoding provided additional information about the neural processes that resulted in improved memory for negatively valenced stimuli in high dissociators. In all participants, these stimuli activated LIFG more than neutral stimuli, probably reflecting increased elaboration in working memory (Kirchhoff and Buckner, 2006; Rugg, 2002). This increased working memory activity likely led to the higher recognition rate for negative than neutral stimuli in both groups of participants. This is in agreement with studies reporting a direct positive relation between working memory and long-term memory (e.g., Feldman Barrett et al., 2004; Raaijmakers and Shiffrin, 1981; Ranganath et al., 2005). In high dissociators, this increased activity was more pronounced and spread to the right inferior frontal gyrus (RIFG), likely reflecting an even more profound elaboration of negative compared neutral stimuli as compared to low dissociators, and greater activation of the right anterior hippocampus, indicating increased memory storage. Also, medial frontal cortex (MFC) showed more activity in response to affectively negative (as compared to neutral) stimuli for the high- vs. the low-dissociative group, possibly reflecting higher levels of top–down regulation of affect (see Bush et al., 2000; Davidson and Irwin, 1999). Interestingly, the effect of dissociative style on the encoding of neutral stimuli showed the reverse pattern: high dissociators showed less cortical activation (RIFG as well as temporal and

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Table 4 Recognition phase Region

l/r

(a) Deep neutral N new neutral Temporal l

Parietal Inferior lobule

l

Hippocampus

l

Low

High

Talairach

Z-score

BA

Talairach

− 51 − 36 − 6 − 63 − 36 − 6 − 60 − 36 − 15

4.83* 4.73* 4.38*

21 21 21

− 63 −33 −9 − 51 18 − 12

4.46* 4.54*

21 38

− 36 − 60 57 − 30 − 57 42 − 48 − 45 54

5.10* 4.94* 4.92*

7 7 40

− 33 − 36 − 45 − 18 − 27

4.95* 4.92* 4.50* 3.02(1) 2.91(1)

40 7 40

48 3 − 30 63 − 15 − 9 66 − 24 −9

4.16(*) 3.62(*) 3.44(*)

21 21 21

57 − 63 27 51 − 57 30 42 − 66 24 57 − 48 42 − 24 −3 −12 − 24 −6 −21 24 − 33 − 15

4.00(*) 3.88(*) 3.88(*) 3.53(*) 4.08(*) 3.86(*) 3.29(*)

39 40 39 40

(b) Deep negative N new negative: no statistics reported (see text) (c) Deep N shallow Temporal

r

57 − 42 − 12

3.59

20

Parietal Inferior lobule

r

30 − 63 45

4.23

7

Amygdala

l

Hippocampus

r

−54 −66 −45 −33 −36

Z-score

42 48 42 −3 −3

BA

Areas showing significant (p b 0.001) increase in activity in low- and high-dissociative participants. BA = Brodmann area. (* = p b 0.05 corrected, (*) = p b 0.1 corrected, (1) = p b 0.005). (a) Deeply encoded neutral words (hits) compared to new neutral words (correct rejections), (b) deeply encoded words compared to shallowly encoded words (hits pooled for affective valence).

occipital areas) when encoding affectively neutral stimuli than high dissociators. Apparently, neutral stimuli received less semantic elaboration in working memory from high than low dissociators. Thus, whereas behavioral data were inconclusive about the separate contributions of neutral and negative stimuli on memory performance differences in high and low dissociators, the Table 5 Recognition phase Region

l/r

High N low Talairach

Z-score

(a) Deep neutral N new neutral Temporal l Parietal l Hippocampus l

−51 12 − 18 3.1 −36 − 51 30 3.45 −21 − 33 − 3 3.15 −33 − 36 − 9 3.1 (b) Deep negative N new negative: no significant group interactions

(c) Deep N shallow Temporal Inferior parietal lobule

Amygdala Hippocampus

r r

l r

48 3 − 30 60 − 45 27 54 − 48 30 57 − 48 45 −24 − 3 − 12 24 − 33 − 15

3.31 2.71(1) 2.59(1) 2.9(1) 2.8(1) 2.61(1)

BA 38 40

21 40 40 40

Areas showing significant (p b 0.001) group interactions between low- and high-dissociative participants. BA = Brodmann area. (1) = p b 0.005. (a) Deeply encoded neutral words (hits) compared to new neutral words (correct rejections), (b) deeply encoded words compared to shallowly encoded words (hits pooled for affective valence).

neurophysiological data at encoding suggested that both encoding of neutral and negative stimuli differed according to the amount of trait dissociation, with high levels of dissociation resulting in more semantic elaboration of negative stimuli and less semantic elaboration of neutral stimuli in working memory, as indicated by differential levels of inferior frontal gyrus activity. These results are reminiscent of two working memory studies that demonstrated a beneficial effect of trait dissociation on performance only for higher working memory loads (Elzinga et al., 2007; Veltman et al., 2005). In an event-related potential study (de Ruiter et al., 2003), moreover, high dissociators not only showed larger amplitudes in response to words containing the letter ‘A’, indicating more intense stimulus evaluation, but also smaller components to words not containing the letter ‘A’, compared to low dissociators. These joint results suggest that dissociative abilities may only surface when working memory is sufficiently loaded, be it by presenting difficult tasks or attention grabbing stimulus material. When demands on working memory are low, on the other hand, trait dissociation may translate into less intense stimulus processing and decreased task performance. For instance, high dissociators might easily drift away in mild states of state dissociation like daydreaming when the task at hand is not sufficiently demanding. When contrasting the effect of negative with neutral stimuli across encoding conditions, increased left amygdala activity was found for the high compared to the low group. Apparently, the intrinsically mildly arousing properties of verbal stimuli were only powerful enough to activate the amygdala when all negative stimuli at encoding were used in the contrast and only in high dissociators. The finding of left amygdala activation by verbal

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Fig. 2. Encoding phase. 3D renderings and coronal cross-sections of BOLD activation for p b 0.001. BA = Brodmann area. Low dis. = low dissociators, high dis. = high dissociators. (a) Deep encoding: neutral words compared to baseline, (b) deep encoding: negative words compared to baseline, (c) shallow encoding: words compared to baseline pooled for valence, (d) deep encoding: negative vs. neutral words, (e) deep and shallow encoding pooled: negative vs. neutral words.

stimuli fits with the view of the left, as opposed to the right amygdala being particularly involved in conscious, top–down stimulus evaluation (Morris et al., 1998; Wright et al., 2001). It thus seems that a negative stimulus valence receives high levels of conscious processing in high dissociators which may be related to the high level of recollection of negative stimuli in the recognition task for this group. Shallowly encoded items were remembered considerably worse than deeply encoded items by all participants, although they actually saw the stimuli for a longer time because the task was much more difficult to perform. This indicates that our deep vs. shallow encoding manipulation was very successful. High dissociators, however, did not show a steeper decrease in memory performance compared to low dissociators, which is at odds with the hypothesis of an avoidant encoding style (Cloitre, 1992; Elzinga et al., 2007). Functional MRI data at shallow encoding also failed to show indications for decreased memory encoding for the high compared to the low dissociators, as decreased LIFG activity. LIFG activity was not found altogether at shallow encoding, confirming the non-semantic nature of this task. Floor effects thus might have obscured indications of avoidant encoding in high dissociators. Alternatively, avoidant encoding might only be apparent in traumatized individuals, and, as such, not be the result of dissociative abilities per se. Also, amnesia for traumatic experiences may be better explained by retrieval inhibition

mechanisms, i.e., high-dissociative patients may inhibit the processing of trauma-related memories by virtue of their strong attentional and working memory capacities (Elzinga et al., 2007). Functional MRI results for the recognition task were less easy to relate to memory performance than the encoding tasks but very informative about the relation between dissociative abilities and conscious recollection. Correct recognition of deeply encoded neutral stimuli activated the left posterior hippocampus and the inferior parietal lobule complex to a greater extent for high than low dissociators, suggesting that high dissociators are characterized by high levels of memory retrieval and conscious recollection, respectively (e.g., Wagner et al., 2005). Recognition of deeply encoded negative stimuli recruited a less extensive cortical network than recognition of neutral stimuli, although memory performance was higher for negative than neutral items in both groups. It might be argued that contrasting hits to old negative words with correct rejections to new negative words obscured the effects of recollection for negative items, because newly presented negative words were processed by brain areas that are also associated with recollection (for a similar suggestion, see Maratos et al., 2000). As a result of overall weak effects, detection of group differences with regard to recognition of negative stimuli may also have been impeded. Although contrasting correctly recognized old items with correctly rejected new items is the standard approach for inferring

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Fig. 3. Recognition phase. 3D renderings and coronal cross-sections of BOLD activation for p b 0.001. BA = Brodmann area. Low dis. = low dissociators, high dis. = high dissociators. (a) Deeply encoded neutral words (hits) compared to new neutral words (correct rejections), (b) deeply encoded negative words (hits) compared to new negative words (correct rejections), (c) deeply encoded words compared to shallowly encoded words (hits pooled for affective valence).

information about brain regions involved in memory retrieval, there are several drawbacks. One of them is that it entails comparing a ‘yes’ to a ‘no’ response, which will differentially activate brain areas that involve taxation of stimulus relevance. That is, ‘yes’ responses elicit brain areas that respond to stimulus relevance, irrespective of the fact if a stimulus is old or new. To obtain a pure estimate of brain activity associated with conscious recollection, a direct comparison was made between correctly recognized deeply and shallowly encoded stimuli (that both involve a ‘yes’ response), hypothesizing that the former category is associated with higher levels of recollection than the latter category (e.g., see Rugg et al., 1998). In agreement with this view, mainly posterior parietal activity could be discerned in the fMRI data (thought to be related to conscious recollection), whereas hardly any prefrontal activity was found (thought to index control processes such as taxation of stimulus relevance). High dissociators showed much more posterior parietal activity than low dissociators (amongst other cortical areas), and in addition, left amygdala and right posterior hippocampus activity was found,

again adding support to the notion that high dissociators are characterized by high levels of conscious recollection. From a completely different point of entry, one might reason that the large differential processing of neutral and negative stimuli in high dissociators is due to dysfunctional, instead of enhanced cognitive abilities in the high dissociators. It might be argued that the high-dissociative group was more depressive or anxious which would result in a preferential processing of the affectively negative stimuli (i.e., mood-congruent processing, Bower, 1981). Three arguments can be raised against this view. Firstly, we found no differences in subjective distress (as measured by SUD-S) between groups. Secondly, our experiment was conducted with healthy, young college students instead of psychiatric patients. Thirdly, we found that the proportion of words that was classified as ‘negative’ during affective evaluation was similar for both groups. Another alternative explanation for our results might be that the highdissociative group was not well concentrated, leaving no processing resources for elaboration of neutral stimuli (e.g., McNally et al., 1998). If this would have been the case, however, high

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dissociators should have shown lower memory performance for the neutral stimuli than the low dissociators, which they did not. As mentioned in the Introduction, we propose that high dissociators are characterized by high levels of elaboration learning (Mandler, 1980, 2002). Elaboration may take place during both encoding and retrieval and can best be characterized as a constructive process. A higher tendency to elaboratively encode and retrieve (‘reconstruct’) information may lead to a higher conscious memory performance but may at the same time be associated with an enhanced sensitivity for false memories. In line with this view, a higher prevalence of false memories in high dissociators has been found in several experimental paradigms (e.g., Cann and Katz, 2005; Ost et al., 2005; Bremner et al., 2000; Clancy et al., 2000). Also, the positive correlations between dissociation and fantasy proneness need mentioning in this respect (Elzinga et al., 2002; Merckelbach et al., 2000, 2002). It is likely, that when overwhelming emotional experiences are involved, dissociative abilities are invoked to cope with these circumstances and that exposure to severe or chronic traumatic experience puts these individuals at risk for developing a dissociative disorder. To explore the elaborative encoding hypothesis further, future studies could incorporate stimulus material that is attention capturing, but not affectively negative, or not salient by virtue of its emotional nature at all. Simultaneous EEG and fMRI recordings would provide highly complementary neural information about temporal en spatial aspects of dissociative abilities. Finally, more extensive determination of psychiatric comorbidity and state and trait measures would rule out alternative explanations for effects of trait dissociation to a higher degree of certainty. To conclude, the results of the present study suggest that high dissociators from a nonclinical population are characterized by higher levels of elaborative encoding of affectively negative stimulus material, and lower levels of elaborative encoding of affectively neutral stimulus material, than low dissociators. This is demonstrated by the greater differential recruitment of the inferior frontal gyrus and areas in the medial temporal lobe, including the hippocampus, according to stimulus valence. This higher ability to elaborate results in higher levels of conscious recollection, as indicated by higher memory performance and more activity in hippocampus and posterior parietal areas at retrieval. No indications for avoidant encoding in high dissociators were found. We suggest that dissociation in healthy individuals may reflect a powerful individual difference that is closely linked to enhanced attentional and working memory capacity, resulting in elaborative encoding and high levels of conscious recollection. Acknowledgments The study was supported by a grant from the Board for Behavioral and Educational Sciences (No. 575-29-003) and from the Board for Medical Sciences (No. 970-10-030) of The Netherlands Organization of Scientific Research (NWO). We thank Geertje Hagedoorn for her assistance in data collection and analysis. References Addis, D.R., McAndrews, M.P., 2006. Prefrontal and hippocampal contributions to the generation and binding of semantic associations during successful encoding. NeuroImage 33, 1194–1206. Becker-Blease, K.A., Deater-Deckard, K., Eley, T., Freyd, J.F., Stevenson,

333

J., Plomin, R., 2004. A genetic analysis of individual differences in dissociative behaviours in childhood and adolescence. J. Child Psychol. Psychiatry 45, 522–532. Bernstein, E.M., Putnam, F.W., 1986. Development, reliability, and validity of a dissociation scale. J. Nerv. Ment. Dis. 174, 727–735. Bower, G., 1981. Mood and memory. Am. Psychol. 36, 129–148. Bremner, J.D., Shobe, K.K., Kihlstrom, J.F., 2000. False memories in women with self-reported childhood sexual abuse: an empirical study. Psychol. Sci. 11, 333–337. Bush, G., Luu, P., Posner, M.I., 2000. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222. Cann, D.R., Katz, A.N., 2005. Habitual acceptance of misinformation: examination of individual differences and source attributions. Mem. Cogn. 33, 405–417. Clancy, S., Schacter, D., McNally, R., Pitman, R.K., 2000. False recognition in women reporting recovered memories of sexual abuse. Psychol. Sci. 11, 26–31. Cloitre, M., 1992. Avoidance of emotional processing: a cognitive perspective. In: Stein, D.J., Young, J.E. (Eds.), Cognitive Science and Clinical Disorders. Academic Press, San Diego, pp. 19–41. Cloitre, M., Cancienne, J., Brodsky, B., Dulit, R., Perry, S.W., 1996. Memory performance among women with parental abuse histories: enhanced directed forgetting or directed remembering? J. Abnorm. Psychol. 105, 204–211. Conway, A.R.A., Cowan, N., Bunting, M.F., 2001. The cocktail party phenomenon revisited: the importance of working memory capacity. Psychon. Bull. Rev. 8, 331–335. Craik, F., Lockhart, R., 1972. Levels of processing: a framework for memory research. J. Verbal Learn. Verbal Behav. 11, 671–684. Daselaar, S.M., Veltman, D.J., Witter, M.P., 2004. Common pathway in the medial temporal lobe for storage and recovery of words as revealed by event-related functional MRI. Hippocampus 14, 163–169. Davidson, R.J., Irwin, W., 1999. The functional neuroanatomy of affective style. Trends Cogn. Sci. 3, 11–21. DePrince, A.P., Freyd, J.J., 1999. Dissociative tendencies, attention, and memory. Psychol. Sci. 10, 449–452. DePrince, A.P., Freyd, J.J., 2004. Forgetting trauma stimuli. Psychol. Sci. 15, 488–492. de Ruiter, M.B., Phaf, R.H., Veltman, D.J., Kok, A., van Dyck, R., 2003. Attention as a characteristic of nonclinical dissociation: an ERP study. NeuroImage 19, 376–390. de Ruiter, M.B., Phaf, R.H., Elzinga, B.M., van Dyck, R., 2004. Dissociative style and individual differences in verbal working memory span. Conscious. Cogn. 13, 821–828. de Ruiter, M.B., Elzinga, B.M., Phaf, R.H., 2006. Dissociation: capacity or dysfunction? J. Trauma Dissociation 7, 115–134. Elzinga, B.M., de Beurs, E., Sergeant, J.A., Van Dyck, R., Phaf, R.H., 2000. Dissociative style and directed forgetting. Cogn. Ther. Res. 24, 279–295. Elzinga, B.M., Bermond, B., van Dyck, R., 2002. The relationship between dissociative proneness and alexithymia. Psychother. Psychosom. 71, 104–111. Elzinga, B.M., Ardon, A.M., Heijnis, M.K., de Ruiter, M.B., van Dyck, R., Veltman, D.J., 2007. Neural correlates of enhanced working-memory performance in dissociative disorder: a functional MRI study. Psychol. Med. 37, 235–245. Feldman Barrett, L., Tugade, M.M., Engle, R.W., 2004. Individual differences in working memory capacity and dual-process theories of the mind. Psychol. Bull. 130, 553–573. Genovese, C.R., Lazar, N.A., Nichols, T., 2002. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15, 870–878. Jang, K.L., Paris, J., Zweig-Frank, H., Livesley, W.J., 1998. Twin study of dissociative experience. J. Nerv. Ment. Dis. 186, 345–351. Jobard, G., Crivello, F., Tzourio-Mazoyer, N., 2003. Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. NeuroImage 20, 693–712.

334

M.B. de Ruiter et al. / NeuroImage 37 (2007) 323–334

Kihlstrom, J.F., Glisky, M.L., Angiulo, M.J., 1994. Dissociative tendencies and dissociative disorders. J. Abnorm. Psychol. 103, 117–124. Kirchhoff, B.A., Buckner, R.L., 2006. Functional–anatomic correlates of individual differences in memory. Neuron 51, 263–274. Korfine, L., Hooley, J.M., 2000. Directed forgetting of emotional stimuli in borderline personality disorder. J. Abnorm. Psychol. 109, 214–221. Mandler, G., 1980. Recognizing: the judgement of previous occurrence. Psychol. Rev. 87, 252–271. Mandler, G., 2002. Consciousness Recovered. John Benjamins, Amsterdam. Maratos, E.J., Allan, K., Rugg, M.D., 2000. Recognition memory for emotionally negative and neutral words: an ERP study. Neuropsychologia 38, 1452–1465. McNally, R.J., Metzger, L.J., Lasko, N.B., Clancy, S.A., Pitman, R.K., 1998. Directed forgetting of trauma cues in adult survivors of childhood sexual abuse with and without posttraumatic stress disorder. J. Abnorm. Psychol. 107, 596–601. McNally, R.J., Clancy, S.A., Schacter, D.L., 2001. Directed forgetting of trauma cues in adults reporting repressed or recovered memories of childhood sexual abuse. J. Abnorm. Psychol. 110, 151–156. McNally, R.J., Ristuccia, C.S., Perlman, C.A., 2005. Forgetting of trauma cues in adults reporting continuous or recovered memories of childhood sexual abuse. Psychol. Sci. 16, 336–340. Merckelbach, H., Muris, P., Horselenberg, R., Stougie, S., 2000. Dissociative experiences, response bias, and fantasy proneness in college students. Pers. Individ. Differ. 28, 49–58. Merckelbach, H., Horselenberg, R., Schmidt, H., 2002. Modeling the connection between self-reported trauma and dissociation in a student sample. Pers. Individ. Differ. 32, 695–705. Morris, J.S., Öhman, A., Dolan, R.J., 1998. Conscious and unconscious emotional learning in the human amygdala. Nature 393, 467–470. Moulds, M.L., Bryant, R.A., 2002. Directed forgetting in acute stress disorder. J. Abnorm. Psychol. 111, 175–179. Moulds, M.L., Bryant, R.A., 2005. An investigation of retrieval inhibition in acute stress disorder. J. Trauma. Stress 18, 233–236. Ost, J., Foster, S., Costall, A., Bull, R., 2005. False reports of childhood events in appropriate interviews. Memory 13, 700–710. Putnam, F.W., Carlson, E.B., Ross, C.A., Anderson, G., Clark, P., Torem, M., Bowman, E.S., Coons, P., Chu, J.A., Dill, D.L., Loewenstein, R.J., Braun, B.G., 1996. Patterns of dissociation in clinical and nonclinical samples. J. Nerv. Ment. Dis. 184, 673–679. Raaijmakers, J.G.W., Shiffrin, R.M., 1981. Search of associative memory. Psychol. Rev. 88, 552–572. Ranganath, C., Cohen, M.X., Brozinsky, C.J., 2005. Working memory maintenance contributes to long-term memory formation: neural and behavioral evidence. J. Cogn. Neurosci. 17, 994–1010.

Ross, C.A., Joshi, S., Currie, R., 1990. Dissociative experiences in the general population. Am. J. Psychiatry 147, 1547–1552. Rugg, M.D., 2002. Functional neuroimaging of memory, In: Baddeley, A., Wilson, B., Kopelman, M. (Eds.), Handbook of Memory Disorders, 2nd ed. Wiley, Hoboken, NJ. Rugg, M.D., Walla, P., Schloerscheidt, A.M., Fletcher, P.C., Frith, C.D., Dolan, R.J., 1998. Neural correlates of depth of processing effects on recollection: evidence from brain potentials and positron emission tomography. Exp. Brain Res. 123, 18–23. Rugg, M.D., Otten, L.J., Henson, R.N.A., 2002. The neural basis of episodic memory: evidence from functional neuroimaging. Philos. Trans. R. Soc. Lond., B Biol. Sci. 57, 1097–1110. Shannon, B.J., Buckner, R.L., 2004. Functional–anatomic correlates of memory retrieval that suggest nontraditional processing roles for multiple distinct regions within posterior parietal cortex. J. Neurosci. 24, 10084–10092. Snodgrass, J.G., Corwin, J., 1988. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J. Exp. Psychol. 117, 34–50. Spiegel, D., Cardeña, E., 1991. Disintegrated experience: the dissociative disorders revisited. J. Abnorm. Psychol. 100, 366–378. Squire, L.R., Knowlton, B.J., 2000. The medial temporal lobe, the hippocampus, and the memory systems of the brain. In: Gazzaniga, M.S. (Ed.), The New Cognitive Neurosciences. The MIT Press, Cambridge MA, pp. 765–779. Vanderlinden, J., Van Dyck, R., Vandereycken, W., Vertommen, H., 1991. Dissociative experiences in the general population in Belgium and The Netherlands. An exploratory study with the Dissociation Questionnaire (Dis-Q). Dissociation 4, 180–184. Vanderlinden, J., Van Dyck, R., Vandereycken, W., Vertommen, H., Verkes, R.J., 1993. The Dissociation Questionnaire (Dis-Q): development and characteristics of a new self-report questionnaire. Clin. Psychol. Psychother. 1, 21–28. Veltman, D.J., de Ruiter, M.B., Rombouts, S.A.R.B., Lazeron, R.H.C., Barkhof, F., Van Dyck, R., Dolan, R.J., Phaf, R.H., 2005. Neurophysiological correlates of increased verbal working memory in highdissociative subjects: a functional MRI study. Psychol. Med. 35, 175–185. Wagner, A.D., Shannon, B.J., Kahn, I., Buckner, R.L., 2005. Parietal lobe contributions to episodic memory retrieval. Trends. Cogn. Sci. 9, 445–453. Wolf, O.T., 2003. HPA axis and memory. Best. Pract. Res. Clin. Endocrinol. Metab. 17, 287–299. Wright, C.I., Fischer, H., Whalen, P.J., McInerney, S.C., Shin, L.M., Rauch, S.L., 2001. Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli. NeuroReport 12, 379–383.