Emotional Arousal Can Impair Feature Binding in Working Memory Mara Mather1, Karen J. Mitchell2, Carol L. Raye2, Deanna L. Novak1, Erich J. Greene2, and Marcia K. Johnson2 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/18/4/614/1756129/jocn.2006.18.4.614.pdf by guest on 18 May 2021 Abstract & To investigate whether emotional arousal affects memorial netic resonance imaging experiments showed that relative to Downloaded from http://direct.mit.edu/jocn/article-pdf/18/4/614/1935793/jocn.2006.18.4.614.pdf by guest on 26 September 2021 feature binding, we had participants complete a short-term low-arousal trials, high- and medium-arousal trials resulted in source-monitoring task—remembering the locations of four greater activity in areas associated with visual processing (fusi- different pictures over a brief delay. On each trial, the four form gyrus, middle temporal gyrus/middle occipital gyrus, lin- pictures were all either high arousal, medium arousal, or low gual gyrus) and less activity in superior precentral gyrus and arousal. Memory for picture–location conjunctions decreased the precentral–superior temporal intersect. These findings sug- as arousal increased. In addition, source memory for the loca- gest that arousal (and perhaps negative valence for depressed tion of negative pictures was worse among participants with people) recruits attention to items thereby disrupting working higher depression scores. Two subsequent functional mag- memory processes that help bind features together. & INTRODUCTION tional nature of an event may enhance memory for its In this study, we investigated the impact of emotion on emotionally arousing components but impair binding of the encoding of episodic memories. People often seem to other aspects of the event to the emotional elements remember shocking events particularly vividly (Pillemer, (Johnson, Nolde, & De Leonardis, 1996; but see MacKay Goldsmith, Panter, & White, 1988; Rubin & Kozin, 1984). & Ahmetzanov, 2005; Doerksen & Shimamura, 2001). People are also more likely to remember emotional To study feature binding during encoding of neutral than neutral stimuli (Charles, Mather, & Carstensen, events (line drawings of objects in various locations), 2003; Canli, Desmond, Zhao, & Gabrieli, 2002; Ochsner, Mitchell, Johnson, Raye, and D’Esposito (2000) used a 2000; Bradley, Greenwald, Petry, & Lang, 1992). Yet, emo- short-term source memory paradigm. In the present tional memories are often less accurate than we believe study, we used a similar working memory task (see Fig- they are (e.g., Schmolck, Buffalo, & Squire, 2000). ure 1) to examine how the emotional content of a In particular, although emotional events may result in picture affects people’s ability to remember where it ap- excellent memory for their central aspects, the ‘‘what’’ peared (a type of source memory, Johnson, Hashtroudi, of the event (Reisberg & Heuer, 2004), other elements & Lindsay, 1993). Our participants saw four pictures of the event are often either forgotten or confused with from the International Affective Picture System (IAPS; elements of other events (Christianson & Loftus, 1991). Lang, Bradley, & Cuthbert, 1999) presented sequentially For example, police officers recall fewer details from in different locations on a computer screen. After each scenarios in which a shooting occurred than those with- sequence of four pictures, there was a brief delay out a shooting (Stanny & Johnson, 2000), and memory followed by one of those pictures in one of the locations for contextual details is worse for emotionally arousing occupied on that trial. Participants indicated whether than nonemotional events (Kensinger, Piguet, Krendl, & the picture–location pairing was the same or different Corkin, 2005; Schmidt, 2002). Memories for shocking than at study. The critical manipulation was that all the events may import elements from other events, such as pictures on a given trial were either high, medium, or television footage seen later (Pezdek, 2003; Neisser & low in arousal, based on normative ratings (Lang et al., Harsch, 1992), and memory for peripheral details of such 1999). For generality, the high- and medium-arousal events is worst among people who find the event most pictures each included an equal number of negatively emotionally powerful (Schmidt, 2004). Thus, the emo- and positively valenced pictures; the low-arousal pic- tures were neutral in valence. Experiment 1 was a behavioral study in which we also examined the relationship between individual dif- 1University of California, Santa Cruz, 2Yale University ferences in levels of depression and source memory. D 2006 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 18:4, pp. 614–625 Figure 1. A schematic representation of one behavioral working memory trial with low-arousal, neutral pictures. Note that the picture to screen size proportion is not to scale. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/18/4/614/1756129/jocn.2006.18.4.614.pdf by guest on 18 May 2021 Downloaded from http://direct.mit.edu/jocn/article-pdf/18/4/614/1935793/jocn.2006.18.4.614.pdf by guest on 26 September 2021 Negative stimuli are especially likely to capture the of four pictures from the same emotion category (e.g., attention of depressed people (Gotlib & Neubauer, high arousal negative). 2000), and this selective attention might negatively affect memory-binding processes. That is, depressed people may be especially likely to process the content of Procedure negative stimuli at the expense of binding the con- On each trial (see Figure 1), participants first saw the tent with location. To further clarify the cognitive pro- cue ‘‘STUDY’’ for 500 msec, followed by four pictures cesses associated with the arousal-induced deficits in shown sequentially for 750 msec each. Each picture source memory revealed in Experiment 1, in Experi- appeared in a different one of eight possible locations. ments 2A and 2B we used functional magnetic reso- After a 7000 msec delay a ‘‘TEST’’ cue appeared for nance imaging (fMRI) to identify brain regions where 500 msec, followed by one of the four pictures from activity differed depending on the arousal level of the the trial for 500 msec in one of the locations used pictures. during that trial. Participants pressed one key to indi- cate the picture–location conjunction was the ‘‘same’’ as during study and another to indicate it was ‘‘differ- EXPERIMENT 1 ent.’’ The intertrial interval (ITI) was 2000 msec, during Methods which the screen was blank. Participants were given three practice trials with pictures not used during the Participants experiment. Twenty undergraduates (15 women, mean age = 18 years) We were interested in people’s memory for picture– participated for course credit. location pairings (source memory). Half of the test pictures of each emotion type were presented in their correct location (‘‘same’’ trials) and half in a different Materials location (these ‘‘different’’ test probes were a picture We compiled five categories of 16 pictures each from the and a location from the current trial, but they were re- IAPS (Lang et al., 1999):1 (1) high arousal negative paired). Each set of four pictures appeared in four (Marousal = 6.38 on a scale of 1–9), (2) high arousal different trials (picture location and ordinal position positive (Marousal = 6.38), (3) medium arousal negative within trial was different across repetitions); each pic- (Marousal = 4.56), (4) medium arousal positive (Marousal = ture was tested once during the session (for a total of 4.53), and (5) low arousal/neutral (Marousal = 3.24). Each 80 trials). Whether a picture was tested in its correct of the 80 pictures was randomly assigned to one set location was counterbalanced across participants. Two Mather et al. 615 different versions of the sets varied which pictures ap- a 2 (valence: negative, positive) Â 2 (arousal: high, me- peared in the same set across participants. Thus, there dium) repeated measures analysis of variance (ANOVA) were four versions of the session. The presentation showed only a main effect of arousal, F(1,19) = 9.32, 2 order of picture sets was random. MSE = .28, p < .01, hp = .33. There was no main effect Participants completed four 5-min blocks of the task. of valence and no interaction of valence and arousal Between blocks, they completed various questionnaires (both F < 1). Thus, unlike arousal, valence did not for 5 min. In the last break, they completed a depression influence source accuracy. scale (Sheikh & Yesavage, 1986). Correlations with Depression Scale Scores Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/18/4/614/1756129/jocn.2006.18.4.614.pdf by guest on 18 May 2021 Results and Discussion Scores on the depression scale ranged from 0 to 8 out Short-term Source Memory Data of a possible 15 (M = 2.9, SD = 3.36). Scores of six or higher indicate probable depression (Ferraro & Participants’ source accuracy when responding to the 0 Chelminski, 1996). Participants’ depression scores were Downloaded from http://direct.mit.edu/jocn/article-pdf/18/4/614/1935793/jocn.2006.18.4.614.pdf by guest on 26 September 2021 picture–location conjunctions is expressed as d scores. negatively correlated with source accuracy for negative Proportions of hits (H) and false alarms (FA) were pictures (r = À.52, p < .05); participants with higher adjusted as follows: p(H) = 1 was recalculated as 1 À depression scores were less likely to remember the 1/(2N), p(FA) = 0 was recalculated as 1/(2N), where N is negative picture–location conjunctions correctly, but de- the maximum number of hits or false alarms possible pression scores were not correlated with source accuracy (Macmillan & Creelman, 1991). A linear contrast showed for neutral (r =.07,p =.80)orpositive(r =.14,p =.50) that the more arousing the pictures were, the less likely pictures. people were to remember where they had occurred, 2 F(1,19) = 10.16, MSE = .42, p < .01, hp = .35 (see Fig- ure 2).