Dissociative tendencies and right-hemisphere processing load: Effects on vigilance performance

Dissociative tendencies and right-hemisphere processing load: Effects on vigilance performance

Consciousness and Cognition 20 (2011) 696–702 Contents lists available at ScienceDirect Consciousness and Cognition journal homepage: www.elsevier.c...

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Consciousness and Cognition 20 (2011) 696–702

Contents lists available at ScienceDirect

Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog

Dissociative tendencies and right-hemisphere processing load: Effects on vigilance performance William S. Helton ⇑, Martin J. Dorahy, Paul N. Russell Department of Psychology, University of Canterbury, Christchurch, New Zealand

a r t i c l e

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Article history: Received 13 May 2010 Available online 16 October 2010 Keywords: Attention Dissociative tendencies Emotional processing Sustained attention Vigilance

a b s t r a c t The present study was designed to explore the relationship between self-reported dissociative experiences and performance in tasks eliciting right-hemisphere processing load. Thirty-four participants (10 men and 24 women) performed a vigilance task in two conditions: with task-irrelevant negative-arousing pictures and task-irrelevant neutral pictures. Dissociation was assessed with the Dissociative Experience Scale. Consistent with theories positing right-hemisphere deregulation in high non-clinical dissociators, dissociative experiences correlated with greater vigilance decrement only in the negative picture condition. As both the vigilance task and negative picture processing are right lateralized, this result provides support for a right-hemisphere dysfunction in high dissociators, at least in negative conditions. Ó 2010 Elsevier Inc. All rights reserved.

1. Introduction Dissociation is a complex psychobiological process that disrupts the integration of sensory, perceptual, conceptual, affective and behavioral information. In clinical cases this process may lead to structural divisions in the personality, for example, in the psychiatric condition dissociative identity disorder (Van der Hart, Nijenhuis, & Steele, 2006). Dissociation also gives rise to less severe manifestations, such as amnesia, ego-observing experience, and posttraumatic flashbacks. It is related to more mundane experiences such as trance states and absorption. Dissociation has been associated with alterations in memory, attentional, psychophysiological and neurobiological functioning in experimental studies (e.g., DePrince & Freyd, 1999, 2001; Dorahy, McCusker, Loewenstein, Colbert, & Mulholland, 2006; Griffin, Resick, & Mechanic, 1997; Lanius et al., 2002). Although research on the neurophysiology of dissociation is not extensive, studies on hemispheric lateralization have pointed to right-hemisphere dysfunction in high non-clinical dissociators. For example, Spitzer et al. (2004), using Transcranial Magnetic Stimulation, found that student participants with a Dissociative Experiences Scale (DES) score above 30, showed right-hemisphere dysfunction relative to the left hemisphere in comparison to participants with a DES score below 30. The authors concluded that ‘‘dissociation may involve a functional superiority of the left hemisphere over the right hemisphere or, alternatively, a lack of integration in the right hemisphere” (p. 167). Enriquez and Bernabeu (2008) gave high (n = 50) and low (n = 50) dissociators from the college student population a dichotic listening task (i.e., stimuli simultaneously presented to both ears) and asked participants to respond to a target word and target emotional tone. The presentation of emotional stimuli is typically associated with dominant right hemispheric functioning, while the presentation of word or language-based stimuli is associated with dominant left hemisphere functioning (e.g., Bryden, Free, Gagne, & Groff, 1991). Both high and low dissociators showed the expected left hemisphere dominance when responding to target words, but only the low dissociators demonstrated the expected right hemisphere dominance ⇑ Corresponding author. Address: Department of Psychology, University of Canterbury, Private Bag 4800, Christchurch, New Zealand. Fax: +64 3 3642181. E-mail address: [email protected] (W.S. Helton). 1053-8100/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.concog.2010.09.019

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when responding to emotional (e.g., happy, angry) tones. The high dissociators showed no difference in hemisphere dominance for emotional tones, supporting the view of right-hemisphere dysfunction associated with dissociation. Spitzer et al. (2004) suggest that right-hemisphere dysfunction in the form of lack of integration is linked to dissociative encoding during threat processing. Specifically, normal right hemisphere functioning during negative emotional exposure allows the discrete aspects of the experience to be bound together or integrated. Right hemisphere dysregulation in high dissociators impedes this integration process in the presence of emotionally distressing or threatening stimuli. The current study was designed to determine if lateral asymmetry in the form of right-hemisphere dysfunction for emotional stimuli, could be replicated in high dissociators using visual threat stimuli in a sustained attention task. Vigilance or sustained attention tasks require participants to monitor visual displays or auditory streams for prolonged periods of time and detect the occurrence of relatively rare target stimuli (Davies & Parasuraman, 1982; Warm, 1984; Warm & Jerison, 1984). Researchers have demonstrated using a wide variety of imaging techniques, including functional magnetic resonance imaging (fMRI), positron emission tomography (PET), transcranial doppler sonography (TCD), and functional near-infrared spectroscopy (fNRIS), increased blood flow and greater metabolic activity in the right as compared to the left hemisphere during sustained attention tasks (Helton et al., 2007; Parasuraman, Warm, & See, 1998; Pardo, Fox, & Raichle, 1991). Typically, in sustained vigilance tasks participants cannot maintain their performance level with time on task, but instead have a noticeable decline in performance efficiency over the watch-keeping period. This decline in performance with time on watch is known as the vigilance decrement (Davies & Parasuraman, 1982; Helton & Warm, 2008; Mackworth, 1948, 1950; Matthews, Davies, Westerman, & Stammers, 2000; See, Howe, Warm, & Dember, 1995; Warm 1984). The vigilance decrement is accompanied by a parallel decline in right hemispheric cerebral blood flow velocity, suggesting a coupling between right hemisphere activity and performance with time on task; that is, the right hemisphere shows greater activation during vigilance than the left hemisphere and the vigilance decrement is matched by a reduction of activity in the right hemisphere (Hitchcock et al., 2003; Schnittger, Johannes, Arnavaz, & Munte, 1997; Shaw et al., 2009). Given the association between right hemispheric functioning and emotional stimuli, the inclusion of non-task relevant negative emotional (threatening) and neutral pictures into the vigilance task provides a useful mechanism to explore the relationship between self-reported dissociative experience and right-hemisphere processing. In the present experiment, participants performed a vigilance task in two conditions: a neutral picture vigilance condition and a negative picture vigilance condition. Picture stimuli were task-irrelevant and briefly presented (250 ms) at random intervals. The inclusion of both a neutral and a negative picture stimuli condition was employed to further delineate the role of the right hemisphere. Exposure to negative picture stimuli elicits greater right hemisphere activation than neutral picture stimuli (Helton, Kern, & Walker, 2009b). Emotional processing, and negative emotional processing in particular, are right lateralized (Balconi & Lucchiari, 2008; Foster et al., 2008). Since the vigilance task is itself right lateralized and negative emotional processing is also right lateralized, if high dissociators have right hemisphere functional difficulties (e.g. difficulties integrating information within the right hemisphere), then they should have a greater decrement in the vigilance task with negative pictures than should low dissociators. This difference should not be as great in the vigilance task without additional right processing load (i.e., neutral picture task), as this condition will require less intra-hemispheric coordination in the right hemisphere. A vigilance decrement with the negative but not neutral pictures on the part of high dissociators compared to low dissociators would provide additional evidence that high dissociators have difficulty regulating information within the right hemisphere. In line with Enriquez and Bernabeu’s (2008) results, it was hypothesized that high non-clinical dissociators would show a relative increase in reaction time to targets over time and relative decrease in perceptual sensitivity over time in comparison to low dissociators, in the negative condition. 2. Method 2.1. Participants Thirty-four students (10 male; 24 female) from upper undergraduate psychology courses served as participants for course credit. Participants ranged in age between 20 and 39 years (M = 22.7 years, SD = 3.7). All had normal or corrected-to-normal vision and were right-handed based on self-report responses to interview questions given prior to the experimental session. The students were recruited as part of a larger set of studies ongoing at the University of Canterbury in which the role dissociative experiences have during vigilance tasks is being investigated. It was a sample of convenience. 2.2. Procedure The participants were tested in a small laboratory room. They surrendered wristwatches, pagers, and/or cell phones at the outset of the experimental session and commenced by signing an informed consent form and then completing the DES. The DES (Carlson & Putnam, 1993) is a 28-item self-report instrument that measures a wide variety of dissociative phenomena (e.g., absorption, imaginative involvement, depersonalization, derealization, amnesia). Responses are made along a 0–100 scale based on the frequency of experience. It has been widely used in clinical and non-clinical populations and has demonstrated good psychometric properties (Van Ijzendoorn & Schuengel, 1996).

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The participants performed two vigilance tasks in a counterbalanced order. They were unaware of the time length for each task. The tasks were both 8-min vigils divided into four continuous 2-min periods of watch. These tasks were based on the abbreviated vigilance task developed by Temple and his associates (Temple et al., 2000). This abbreviated vigilance task exhibits many of the same effects as do longer duration vigilance tasks, including a decline in signal detections over time and right cerebral dominance (Helton & Warm, 2008; Helton et al., 2007). During the vigilance tasks, participants inspected the repetitive presentation of 8  6 mm light gray capital letters consisting of either an O, a D, or a backwards D, centered on a video display terminal (VDT). The 270 mm  340 mm VDT was mounted at eye-level approximately 40 cm from the seated participant and head movements were not restrained. The letter stimuli appeared in 24-point Avante Garde font. The letters were presented for 40 ms against a visual mask consisting of unfilled circles on a white background. See Fig. 1 for an example of a stimulus display. The mask remained visible during a 1000 ms interstimulus interval during which the participant could respond. The circular elements of the mask were 1 mm in diameter and were outlined by black lines (0.25 mm thick). The contrast between the black outlines of the circles and the white background of the screen was 92%, as indexed by the Michaelson equation for spatial modulation ([maximum luminance  minimum luminance/maximum luminance + minimum luminance]  100; Coren, Ward, & Enns, 1999). Mask elements were separated by 3 mm in the horizontal and vertical directions and by 2.5 mm diagonally. Critical signals for detection were the appearance of the letter O. As indexed by the Michaelson equation, the contrast ratio between the letter stimuli and the background was 45%. The order of presentation of the three letter stimuli was varied randomly within each period of watch for each observer in all experimental conditions with the restriction that the critical signal (i.e., O) occurred with a probability p = .20 and each of the two non-signal letters (D and backwards D) occurred with a probability of p = .40. Participants signified their detection of critical signals by pressing a key on an electronic keyboard located in front of them. No response was required for the non-signal letters. Responses occurring within 1000 ms after the onset of the critical signal were recorded as correct detections (hits). All other key presses were recorded as errors of commission (false alarms). The two vigilance tasks differed with reference to the presentation of negative or neutral picture stimuli. Following the first 2-min period of watch (picture free), participants were randomly shown five pictures within each of the remaining three 2-min watch periods. These were displayed in the centre of the screen for 250 ms and randomly interspersed within the vigilance trial sequence. During the picture stimuli presentation the vigilance task was not presented. The picture stimuli sets consisted of either neutral or negative pictures, such that one whole vigilance task was conducted solely with neutral pictures and the other solely with negative pictures. The pictures were selected from the International Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 2001). The IAPS contains normative ratings based on a 9-point scale for arousal and valence. The pictures for each set (neutral and negative) were chosen based on these normative ratings. The neutral set contained pictures that were low in arousal with neutral valence (mean rating of 3.0; e.g. a chair and a spoon). The negative set contained slides that were high in arousal and negative valence (mean rating of 6.0 or greater; e.g. a gun pointing at the participant and a snarling dog). These picture stimuli have been employed in a previous sustained attention study (Helton, Kern, & Walker, 2009a). All participants were given a 2-min practice period to familiarize themselves with the vigilance task. During the practice period, they were provided with guidance via a computer-controlled voice that announced ‘‘hit” after a correct detection and ‘‘miss” after a missed signal. They were instructed that detection responses unaccompanied by voice-feedback were errors of commission (false alarms). In order to be retained in the study, participants were required to detect 80% of the critical signals during practice, with no more than 10% false alarms. All observers met these criteria. Feedback was not provided during the main portion of the study. The main experimental trials commenced immediately after the practice period. There were no rest breaks during the vigil. Between the two vigilance tasks participants were given a 6-min unstructured rest break. 2.3. Analysis 2.3.1. Performance For each period of the vigilance task reaction times to the target stimuli (e.g. O), percent hits (correct detections), and percent false alarms were recorded for each participant. From the percent hits and false alarms, we calculated A0 which is

Fig. 1. The abbreviated vigilance task display.

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a signal detection metric of perceptual sensitivity (i.e., sensitivity of correctly and exclusively identifying targets from non-targets, see Macmillan & Creelman, 2005). High-event rate abbreviated vigilance tasks, like the one employed in this experiment, have been shown to lead to changes in perceptual sensitivity, not response bias (see Helton, Dember, Warms, & Matthews, 2000; Helton & Warm, 2008; Parasuraman, 1979; Temple et al., 2000). A0 was chosen, as the abbreviated vigilance task typically has blocks with 100% detections and/or 0% false alarms, thus making d0 an inappropriate measure of perceptual sensitivity (Macmillan & Creelman, 2005). 2.3.2. Performance and dissociation In order to test specific predictions regarding the relationship between the DES and performance, we calculated two derived indices for A0 and RT for each individual: the intercept and slope. Within each vigilance task, lines of best fit using least squares estimation were calculated for each participant for both A0 and RT. The three periods of watch within the vigilance task were centered before calculating the lines of best fit. This was achieved by coding the three watch intervals sequentially as 1, 0, and 1 instead of 1, 2, and 3 when computing the lines of best fit for each participant. Using this procedure, the intercept of the fitted line for a participant equals the mean A0 or RT over the entire three intervals of their watch. The slope of the line indicates the linear trend or the change in magnitude of A0 or RT of the participant over the three watch intervals (Keppel & Zedeck, 2001). This strategy enabled us to specifically look at average task performance (the intercept) and, more importantly, linear change in performance over the task (the slope) (see Helton, Shaw, Warm, Matthews, & Hancock, 2008; Helton & Warm, 2008; Langer, Wukknesm, Chatterjee, Eickhoff, & Sturm, in press). A relationship between the intercept of A0 or RT and DES scores would suggest a difference in absolute level of vigilance performance between participants having higher and lower DES scores. A relationship between the slope of A0 or RT and DES score would suggest a difference in performance with time on task between those participants higher or lower DES scores. For example, a negative relationship between DES score and A0 slope would indicate that those with higher DES scores displayed a greater A0 decrement with time on task (i.e., were getting less able to accurately detect targets over time), than those with lower scores on the DES. A positive relationship between DES score and RT slope would indicate that those with higher DES scores had a greater RT increment with time on task (i.e., were getting slower over time), than those with lower DES scores. This technique enabled us to examine the relationship between the DES score and the vigilance decrement directly. Finally, we also analyzed the data by grouping the participants into low and high dissociation groups based on a median split. Although statisticians and methodologists are often critical of this data analysis approach (see Pedhazur, 1997), it is used extensively in the dissociation literature and may aid the interpretation or visualization of results. Two mixed or split-plot ANOVAs were conducted, one for A0 and one for RT, and these results were used in combination with the more powerful correlational results (regarding the relationship between the intercept and slope) for interpretation. 3. Results The DES scores ranged in our sample from 5.9 to 53.2 (M = 19.0, SD = 10.1). In order to test the hypothesis of steeper vigilance decrement with higher DES scores in the negative but not neutral picture condition Pearson correlation coefficients were computed between DES scores and the performance metrics separately for negative and neutral conditions. Consistent with prediction a significant negative correlation between A0 slope, r = .34, p < .05 was found in the negative picture condition but not neutral picture condition, r = .03, p > .10. Thus, the decrease in sensitivity with time on task was greater for higher dissociators but only in the negative picture condition. Similarly RT slope increased significantly with DES score, r = .37, p < .05, but only in the negative picture condition. Rate of increase in RT with time on task was greater for higher dissociators but only in the negative picture condition. These results are presented in Table 1, with the negative picture condition above the main diagonal and the neutral picture condition below the main diagonal. Another way to test the hypothesis is to classify participants as high and low dissociators based on a median split of the DES scores (DESmedian = 16.6; 17 low dissociators and 17 high dissociators) and then treat the A0 and RT scores with separate 2 (low vs. high dissociators)  2 (picture condition: negative vs. neutral)  3 (periods of watch) mixed analyses of variance. The DES mean in the high group was 26.5 (SD = 9.1) and in the low group 11.4 (SD = 3.0). The analysis of A0 revealed a significant main effect for picture condition, F(1, 32) = 7.54, p = .01, g2p = .19. The negative picture condition resulted in significantly lower sensitivity (M = .96) than the neutral picture condition (M = .97). There was also a non-significant trend regarding the picture condition by DES level interaction, F(1, 32) = 3.39, p = .07, g2p = .10. This later trend is displayed in Table 1 Correlations between variables (negative above main diagonal; neutral below). DES DES A0 intercept A0 slope RT intercept RT slope Note: p < .05 bold.

0.03 0.03 0.20 0.19

A0 intercept

A0 slope

RT intercept

RT slope

0.15

0.34 0.59

0.10 0.55 0.30

0.37 0.39 0.61 0.02

0.19 0.64 0.05

0.17 0.06

0.04

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Fig. 2. All other results of this analysis were not statistically significant nor where there any other trends (all p > .10). The analysis of RTs yielded a significant three way interaction between picture condition, DES level, and periods, F(2, 64) = 3.15, p = .05, g2p = .09. No other results of this analysis were statistically significant nor where there any trends (all p > .10). In order to further investigate this interaction, two 2 (low vs. high dissociators)  3 (periods of watch) mixed analyses of variance were conducted each for the neutral and negative conditions. In the neutral condition, all results were not statistically significant nor where there any trends (all p > .10). In the negative picture condition, there was a statistically significant DES level by periods interaction, F(2, 64) = 3.15, p = .05, g2p = .09. This interaction is displayed in Fig. 3. As predicted the increase in RT with watch interval was greater for high than low dissociators. With continued sustained attention in the negative condition, high dissociators showed slower RTs compared to low dissociators. 4. Discussion Overall, results show that performing a sustained attention task with negative picture stimuli has detrimental impact on performance that was not present with neutral picture stimuli. However, in support of the hypothesis, that high non-clinical dissociators are particularly prone to problems with right hemisphere intra-activity, the present study demonstrated that high dissociators had more difficulty performing the target detection task over time with the addition of negative pictures than low dissociators. Based on a median split of the DES, compared to low dissociators, high dissociators showed an increment in reaction time over the course of the experiment in the negative condition. There was no difference in the neutral condition. The correlation between RT slope and the DES was both statistically significant (p < .05) and positive in the negative picture condition, suggesting a greater slowing over time in those with higher DES scores. In the neutral condition the relationship was statistically insignificant (p > .05) and actually slightly negative. The interaction between high dissociation and reduced performance (A0 ) fell marginally short of significance in the median split ANOVA analysis. However, the correlation between A0 slope and the DES was both statistically significant (p < .05) and negative in the negative picture condition, suggesting a greater reduction in detection sensitivity over time in those with higher DES scores. In the neutral condition the relationship was both statistically insignificant (p > .05) and near zero. Those higher on the DES generally (both in RT and A0 ) did worse with time on task in the negative condition, ruling out a speed-accuracy tradeoff in that condition. This did not occur in the neutral picture condition. Thus, increases in dissociation scores were significantly related to decreases in perceptual sensitivity (A0 ) over time for target stimuli and slower RTs over time in the negative condition only. In sum, the current findings support the perspective that high non-clinical dissociators have more difficulty coordinating activity within the right hemisphere, such that deficits in cognitive functioning become evident when the right hemispheres of high dissociators become loaded with the combined effects of a sustained attention task and negative emotional stimuli. The current findings are consistent with previous work on hemispheric lateralization in non-clinical dissociators (Enriquez & Bernabeu, 2008; Spitzer et al., 2004). Previous research does indicate that sustained attention generally, and in particular performance on the abbreviated task utilized in this experiment is right-lateralized (see Helton et al., 2007). Emotional, particularly negative, picture processing is also right-lateralized (Balconi & Lucchiari, 2008; Foster et al., 2008). Our results would therefore be consistent with the possibility of high dissociators having a reduced ability to coordinate activity within the right hemisphere. Thus, the integration of experiences, which rely heavily on right hemisphere activation (e.g., negative emotion, sense of self with reference to the experience) may be compromised in high dissociators, leading to dissociative (non-integrated) memory encoding, and therefore later intrusive dissociative phenomena. One limitation of this study is that we did not actually measure cerebral activity. We could only infer greater righthemisphere load based on previous studies using the abbreviated vigilance task and negative pictures used here. Future studies should combine both sophisticated behavioral measures and brain-imaging to better elucidate the hemispheric processing differences amongst individuals low and high in self-reported dissociative experience. A vexing issue is whether

High Dissociators Low Dissociators

1.00 0.98 0.96

Mean A'

0.94 0.92 0.90 0.88 0.86 0.84 0.82 0.80

Negative

Neutral

Picture Condition Fig. 2. Mean percentage correct detections for the dissociation level by picture condition trend (error bars are standard errors of the mean).

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701

Low Dissociators

480

High Dissociators

Mean RT (msec)

470 460 450 440 430 420 410 400 1

2

3

Periods of Watch (2 min) Fig. 3. Mean percent reaction times (ms) for the three periods for the low and high dissociators in the negative picture condition (error bars are standard error of the mean).

high dissociators have a general right-hemisphere dysfunction or only problems integrating and processing negative emotional information. Both the majority of previous studies and the present study have employed negative emotional stimuli in combination with another task (DePrince & Freyd, 1999, 2001). This is rational given the relationship between clinical dissociation and previous traumatic experiences (see Vermetten, Dorahy, & Spiegel, 2007). However, it is often undefined whether the non-affect tasks used in previous studies of dissociation require predominantly left or right hemisphere activation and whether tasks and emotional stimuli either cancel each other out in terms of hemispheric load or combine to provide greater strain on one hemisphere. Oathes and Ray (2008), for example, found that high non-clinical dissociators demonstrated superior performance identifying emotional stimuli compared to low dissociators. High dissociators may process emotional information differently than low dissociators or high dissociators may simply deploy more cognitive resources to processing emotional information. It is unclear at this point whether high dissociators have a general righthemisphere dysfunction, or if emotional processing is special. While Amrhein and colleagues (2008) did find that high dissociators had lower spatial memory spans than low dissociators, also implicating a right-hemisphere dysfunction, this remains a relatively unexplored issue. Future research should separate out emotion from known lateralized cognitive and perceptual tasks to see if dissociation relates to lateral differences generally, or if affect, especially negative, is required to demonstrate right-hemisphere dysfunction. With reference to affect, it needs to be determined if the current results are isolated to negative affective stimuli or whether positive affective stimuli produce similar findings. Sustained attention or vigilance performance is notoriously hard to predict from personality measures (Shaw et al., in press). Previous research has suggested that high non-clinical dissociators have superior selective and/or divided attention abilities (e.g., De Ruiter, Phaf, Elzinga, & Van Dyck, 2004; De Ruiter, Phaf, Veltman, Kok, & Van Dyck, 2003; DePrince & Freyd, 2001). The present findings, however, suggest that individuals with high self-reported dissociation experiences may have an increased vigilance decrement in situations where they may also be exposed to negative emotional stimuli during the task. There are, of course, a number of settings that require vigilance and possibly exposure to negative emotional stimuli, these would include military-law enforcement surveillance, post-disaster search and rescue, and medical monitoring during surgical procedures. Aside from any clinical implications, the results of the present study indicate further research of dissociation and its relationship to performance is warranted.

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