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Journal of Abnormal Psychology February 1999 Vol. 108, No. 1, 153-163
© 1999 by the American Psychological Association For personal use only--not for distribution.
Explicit Memory in Anxiety Disorders Eni S. Becker Department of Clinical Psychology and Psychotherapy Dresden University of Technology Walton T. Roth Psychiatric Consultation Service Veterans Affairs Palo Alto Health Care System Matthias Andrich Department of Psychology Jürgen Margraf Department of Clinical Psychology and Psychotherapy Dresden University of Technology ABSTRACT Two experiments were conducted to study selective memory bias favoring anxiety-relevant materials in patients with anxiety disorders. In the 1st experiment, 32 patients with generalized anxiety disorder (GAD), 30 with social phobia (speaking anxiety), and 31 control participants incidentally learned GAD-relevant words, speech anxiety-relevant words, strongly pleasant words, and words with a neutral valence. Participants did not show any explicit memory bias for threatening materials. Thirty patients suffering from panic disorder (PD) with agoraphobia and 30 controls took part in the 2nd experiment. The design was similar to the 1st experiment. This time a highly specific selective memory bias for threatening words was found. Words describing symptoms of anxiety were better recalled by PD patients. Results are consistent with previous findings but are inexplicable by existing theories.
Preparation of this article was supported by a fellowship from the German Academic Exchange Service (DAAD), a grant from the Christoph-Dornier Stiftung, and the support of the Veterans Administration. We thank Cassandra Lehmann for recruiting and diagnosing the generalized anxiety disorder patients and Cheryl Post for her help in conducting the first experiment. We also thank the Christoph-Dornier Center for their invaluable help in recruiting and diagnosing the agoraphobic patients. Special thanks go to Mike Rinck for helpful comments on an earlier version of the article and to Ulrich Glowalla, Joachim Hasebrook, and Gilbert Fezzardi for supplying the software used to conduct Experiment 1. Correspondence may be addressed to Eni S. Becker, Department of Clinical Psychology and Psychotherapy, Dresden University of Technology, Dresden, Germany, D-01062. Electronic mail may be sent to
[email protected] Received: February 4, 1998 Revised: August 30, 1998 Accepted: August 30, 1998
Cognitive processes have attracted considerable interest in research on anxiety disorders. Most psychological models of anxiety disorders ( Barlow, 1988 ; Beck, Emery, & Greenberg, 1985 ; Eysenck, 1992 ; Foa & Kozak, 1986 ) postulate that cognitive processes are crucial for the origin of these disorders. In addition to selective attentional and interpretational biases, interest has focused on a possible selective memory bias in anxious individuals, that is, improved retention of threat-related
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materials. Two theories have been influential: Bower's network theory of mood and memory ( Bower, 1981 , 1987 ) and Beck's schema theory ( Beck et al., 1985 ). Both predict that anxious individuals will show enhanced memory for anxiety-relevant information. Surprisingly, the predicted selective memory for threat-related materials has rarely been found ( Williams, Watts, MacLeod, & Mathews, 1988 , 1997 ). Instead, such memory biases have been documented almost exclusively in depressed patients, who, on the other hand, rarely have shown the attentional biases observed fairly regularly in anxiety patients. Based on these findings, Williams et al. (1988) concluded that anxiety leads to an attentional bias, whereas depression leads to a memory bias. Depressed patients are assumed to elaborate sad themes and thus show a good memory for them. Apparently, anxiety patients attend to threatening stimuli to avoid feared situations and objects but do not elaborate on these stimuli because that would be too frightening. Thus they show no disordercongruent memory bias. In addition, they may avoid searching their memory for threatening stimuli, causing a disorder-incongruent memory bias. The above explanation for good memory in depression is somewhat less convincing when applied to major depression, however, because patients suffering from major depression are almost always anxious as well. To test the Williams et al. theory, implicit memory tests were introduced. Mathews, Mogg, May, and Eysenck (1989) conducted one of the first studies that used an implicit as well as an explicit memory test, namely word stem completion and cued recall. They found that generalized anxiety disorder (GAD) patients showed no explicit memory bias for threat-related words but did show enhanced retention of these words on the implicit memory test. Subsequent studies testing anxiety patients of various kinds used the same paradigm, and their results often have been interpreted as confirmation of the theory proposed by Williams et al. (1988 , 1997 ). However, in some anxiety disorders, selective memory was found for both explicit and implicit tests. In general, studies of memory biases have given different results in different disorders, as Table 1 illustrates. Patients with panic disorder (PD) or agoraphobia have had enhanced memory for threat-related materials in explicit memory tests ( Becker, Rinck, & Margraf, 1994 ; Cloitre, Cancienne, Heimberg, Holt, & Liebowitz, 1995 ; Cloitre & Liebowitz, 1991 ; McNally, Foa, & Donnell, 1989 ; Nunn, Stevenson, & Whalan, 1984 ). Only two studies failed to find an explicit memory bias in panic patients ( Otto, McNally, Pollack, Chen, & Rosenbaum, 1994 ; Pickles & van den Broek, 1988 ). These exceptions could be due to small sample sizes or, in the case of Otto et al. (1994) , to the use of a cued recall test, which is suboptimal for showing effects of mood on memory. In fact, in a later article ( Mathews & MacLeod, 1994 ), two of the authors of the Williams et al. theory acknowledge that PD patients might indeed differ from other anxiety patients in showing an explicit memory bias for threat-related materials. A different picture emerges for GAD. Most studies did not find an explicit memory bias in these patients ( Bradley, Mogg, & Williams, 1995 ; MacLeod & McLaughlin, 1995 ; Mathews et al., 1989 ; Mogg, Mathews, & Weinman, 1987 ), but they often found an implicit bias ( MacLeod & McLaughlin, 1995 ; Mathews et al., 1989 ). Only one experiment using an explicit test showed better memory for anxietyrelated words in GAD patients ( Mogg & Mathews, 1990 ). Hardly any studies address specific phobias, except for an early study of spider phobics ( Watts, Trezise, & Sharrock, 1986 ), the results of which are not easily interpreted. Spider phobics recognized fewer large spiders than did controls, but they recognized more small spiders than did controls. None of the several studies on patients with social phobia (SP) found enhanced memory for words denoting social threat ( Cloitre et al., 1995 ; Lundh & Öst, 1997 ; Rapee, McCallum, Melville, Ravenscroft, & Rodney, 1994 ), although one identified a subgroup of patients (those with specific social fears) who did show selective memory in an implicit memory test ( Lundh & Öst, 1997 ).
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The one study with posttraumatic stress disorder (PTSD) patients that used a free recall test found better retention for emotional words in veterans with PTSD, although not a specific bias for trauma-related stimuli ( Vrana, Roodman, & Beckham, 1995 ). With respect to implicit memory in PTSD, the results are sparse and ambiguous: One study failed to demonstrate enhanced retention of PTSD-relevant words in an implicit perceptual memory test ( McNally & Amir, 1996 ); a second found a better implicit memory for combat-relevant sentences in PTSD patients compared with veterans without PTSD ( Amir, McNally, & Wiegartz, 1996 ). Several studies have been done with nonpatients, for example, people with panic attacks ( Norton, Schaefer, Cox, Dorward, & Wozney, 1988 ) or high trait anxiety (e.g., Bradley, Mogg, & Williams, 1994 ; Reidy & Richards, 1997 ) or with socially anxious students ( Foa, McNally, & Murdock, 1989 ; Sanz, 1996 ). These studies show patterns of results very similar to those of patient populations. In summary, panic patients show enhanced retention of relevant materials whether or not an implicit or explicit memory test is given; GAD patients show no such memory bias in explicit tests but tend to remember threatening material in implicit tests; SP patients show no bias for social threat words. What uncontrolled factors might explain such inconclusive results? First, it may be easier to construct appropriate materials for PD patients than for GAD patients because the former fear a few topics but the latter fear a wide range of topics. Second, disorder relevance and emotionality may have been confounded, at least in the experiments of Martin, Williams, and Clark (1991) , in which anxiety patients were partial to all words with high emotionality, not just to threat words. Studies by other researchers ( Becker et al., 1994 ; Cloitre & Liebowitz, 1991 ; Cloitre, Shear, Cancienne, & Zeitlin, 1994 ), however, did not always give this result. In these studies, specific biases toward threat words were found. Third, statistical power may have been insufficient. Mood congruency or schema congruency effects are typically not very large (e.g., Cohen's f = .21, Becker et al., 1994 ), so samples must contain at least 20, or better 30 participants per group in order to have a realistic chance of finding memory biases. However, power does not explain all the observed differences between disorders because the sample sizes for GAD patients were often adequate. Fourth, the kind of encoding task, the kind of explicit test, and the nature of their combination seem important. Several studies have found that incidental learning tasks and free recall tests optimize the chances of finding mood effects. Free recall has been extensively and successfully used in research on mood and memory (e.g., Bower & Cohen, 1982 ; Eich, 1980 ; Eich, Weingartner, Stillman, & Gillin, 1975 ; Fiedler & Ströhm, 1986 ). Explicit learning tasks and cued recall tests, on the other hand, seem to involve too many cues, which may override any effect mood has. Only two studies of GAD used a free recall test ( Bradley, Mogg, & Williams, 1995 ; Mogg & Mathews, 1990 ), and one of them did find an explicit disorder-congruent memory bias ( Mogg & Mathews, 1990 ). On the other hand, both SP studies that used free recall failed to show selective memory ( Cloitre et al., 1995 ; Rapee et al., 1994 ). In addition, suboptimal encoding tasks were sometimes chosen, for example, a modified Stroop test ( MacLeod & McLaughlin, 1995 ). Finally, the congruency of encoding task and retrieval task seems to be of major importance; that is, both should be either conceptual or perceptual ( Eysenck & Byrne, 1994 ). Fifth, the high comorbidity between anxiety and depression ( Sanderson & Wetzler, 1991 ) needs to be taken into account. Sometimes, in the studies cited, significant correlations of anxiety scores and depression scores were recorded ( Bradley, Mogg, & Williams, 1994 , 1995 ), and in others depression was excluded ( Eysenck & Byrne, 1994 ; Reidy & Richards, 1997 ). Overall, one can conclude that memory effects are indeed due to anxiety, although it is still unclear whether state or trait anxiety is more important and whether depression has an additional effect. The two experiments reported in this article were an attempt to overcome some of the uncontrolled
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factors listed above. Patients with three different anxiety disorders (GAD, SP, and PD) participated. Memory biases in all three patient groups were tested using almost identical methods. In addition, the materials and procedures used in the two experiments were chosen to maximize the chances of observing memory biases: Incidental learning tasks and free recall tests were used, sample sizes were adequate, the verbal stimuli were specific to the disorders, and patient groups rather than analog populations were tested. In both experiments, the participants learned each word incidentally by generating an imaginary scene that combined the word with themselves. This conceptual learning task was combined with a conceptual memory test–a free recall test that followed a distractor task. We chose verbal materials that were rated by experts as especially relevant to the disorders, trying to match the threat schemata inherent in the disorders. The disorder-relevant words were matched to highly positive and neutral words, thereby controlling for emotionality effects. Thus we hoped to maximize the chance of finding an explicit memory bias for disorder-relevant words in all three patient groups.
Experiment 1 Method Participants. The participants in this experiment were recruited by advertisements in local newspapers in Palo Alto, California. The sample comprised 32 GAD patients, 30 SP patients, and 31 control participants. Patients were offered treatment after taking part in the experiment, and control participants were paid. All candidates were interviewed using the Structural Clinical Interview for DSM—III—R, Upjohn version (SCID-UP; Spitzer, Williams, & Gibbon, 1987 ) by a master's level psychologist and a graduate student in psychology who were extensively trained before the study. Unfortunately, the improved DSM—IV diagnoses were not available at the time of this study. However, a major problem with the DSM—III—R diagnosis of GAD, namely its separation from depression, was avoided by excluding all participants who suffered from a current episode of major depression or dysthymia. Still, it is possible that some patients were included in the GAD sample who would have been excluded according to the improved criteria of DSM—IV. Several other potential participants were excluded for a variety of reasons, such as medical illness, substance abuse, and past or current psychotic episodes. Four GAD patients had a major depression in remission, and 4 had a simple phobia. Eight of the SP patients had an additional simple phobia. Patients with both GAD and SP were excluded, as were those with both GAD and PD. No participant was taking psychoactive medication. Control participants had to be free of psychological disorders except mild specific phobias (no significant impairment or avoidance). The three groups did not differ in age (mean age in years: GAD, 44.3; SP, 46.2; controls, 45.2), gender (female: GAD, 43%; SP, 40%; controls, 44%), or education (mean years of education: GAD, 16.4; SP, 16.4; controls, 16.6). Questionnaires. Participants filled out a battery of questionnaires. Only the results of the Symptom Checklist—90 (SCL90; Derogatis, Lipman, & Covi, 1977 ), the State-Trait Anxiety Inventory (STAI) Trait subscale (STAIT; Spielberger, Gorsuch, & Lushene, 1970 ), and the Beck Depression Inventory (BDI; Beck, Ward, Mendelsohn, Mock, & Erbaugh, 1961 ) are reported here. These questionnaires were completed at the diagnostic interview, about a week before the day of the experiments. In addition, before and after the experiment, participants were asked to fill out the STAI State subscale (STAI-S; Spielberger et al., 1970 ). Stimulus words. Experimental stimuli were drawn from a word pool provided by seven experts on anxiety disorders. These words fall into four classes: GAD-related words, speech phobia-related words (also called speech-
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related), words with a neutral valence, and words with a positive valence. The seven experts were asked to name words that were especially relevant for the two disorders. We chose the words that were named by most experts and that were typical for one disorder but not for the other one. Afterward, the positive and neutral words were selected from the norms given by Francis and Kučera (1982) . The stimulus material consisted of 24 words, 6 words per word type. Table 2 shows the words used. At the end of Experiment 1, all words were rated by all participants on the three dimensions of personal relevance, excitingness, and pleasantness on a scale ranging from 1 ( not at all ) to 7 ( extremely ). An analysis of these ratings confirmed that appropriate words were chosen (all differences reported in this paragraph were significant at the .05 level). For all participants, the emotional words (GAD-related, speech-related, and positive) were more relevant and more exciting than the neutral words. For positive and neutral words, the ratings of the three groups did not differ with regard to relevance, excitement, or emotional valence. The GAD-related words were as relevant to the GAD patients as they were to the social phobics, although the means seemed to show slightly higher ratings by GAD patients ( M = 4.7, SD = 2.0 vs. M = 4.2, SD = 2.1). The GAD-relevant words were more relevant to the GAD patients than to the control participants ( M = 4.7, SD = 2.0 vs. M = 3.5, SD = 2.0). The speech-relevant words were significantly more relevant to the social phobics ( M = 4.7, SD = 1.9) than to the GAD patients ( M = 4.1, SD = 1.9), who again found them more relevant than did the control participants ( M = 3.1, SD = 2.0). The same pattern evolved with regard to the excitement ratings. The GAD patients found the GADrelevant words more unpleasant ( M = 2.3, SD = 1.7) than did the control group ( M = 2.8, SD = 1.7). The SP patients rated the speech-relevant words as more unpleasant ( M = 2.7, SD = 1.5) than did the GAD patients ( M = 3.3, SD = 1.6) or the control participants ( M = 3.7, SD = 1.7). Moreover, the disorder-related words were judged to be as unpleasant as the positive words were pleasant. All experimental words were chosen to be easy to image. Taken together, these results indicate that the chosen experimental words were suited for the experiment sufficiently well. Incidental learning task. Participants were asked to create a visual scene combining a presented word with themselves, for example, a scene in which they received a gift (a positive word, see Table 2 ). Creating visual images generally results in good retention in both clinical ( Becker et al., 1994 ) and nonclinical participants (e.g., Bower, 1970 , 1972 ; Paivio, 1971 ), even for incidental learning. The words were presented one by one on a computer screen in capitalized letters at a fixed position. After each word, participants were asked to rate how well they had been able to imagine the scene. The rating was given on the computer on a scale ranging from 1 ( very difficult ) to 5 ( very easy ). The first five words were practice words. Order of the experimental words was randomized with the restriction that no more than two words of the same group followed each other. Each word was presented for 10 s, followed by a sound to signal participants to give the rating. After the rating, the next word was presented. Emotional state ratings. After finishing the learning task, participants gave four retrospective ratings of their emotional state during the task. On scales ranging from 0 ( not at all ) to 10 ( extremely ), they rated their levels of excitement, tension, and anxiety and how much they would have liked to leave the experimental situation (avoidance). Free recall test. Participants were instructed to write down all words they had imagined during the learning task. They were told to also include any words they were unsure about. They had 5 min for this test.
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Procedure. On the day of the experiment, participants first completed the state subscale of the STAI. Then they received instructions for the incidental learning task. They were told that we were interested in their ability to create visual images. After six practice words, the experimental words were presented. The computer recorded the ratings given to each word. After the learning task, participants rated their emotional state. This was followed by a distractor task lasting for 5 min. In this task, participants were asked to rate how funny cartoons were. Then the free recall test was given. Upon completion, participants were asked to fill out the STAI-S questionnaire. Then they rated the word materials. After this participants were debriefed. The complete experiment lasted between 30 and 40 min. Design. Full combination of the independent variables group (patients with GAD, SP patients, and control participants) and word type (GAD-relevant, speech-relevant, positive, and neutral words) yielded a 3 × 4 design. Word type was a within-subjects factor and experimental group a between-subjects factor. As the dependent variables, the number of correctly recalled words and the number of intrusions in the free recall test were recorded. Effect sizes were computed according to Cohen (1988) and are given as f values below. Results Questionnaires. As the p levels indicate, the three groups differed significantly in most questionnaires scores (see Table 3 ). Additional tests following Scheffé revealed that the following differences between pairs of groups were significant at the .05 level: GAD patients scored higher than social phobics and control participants on all three trait measures (i.e., the SCL-90, the BDI, and the STAI-T). The SCL-90 scores indicated a higher level of general psychopathology in the group of GAD patients, although even in that group the score of 0.92 was low. The BDI scores indicate mild levels of depression in the GAD group, with the other two groups reporting fewer symptoms of depression. As expected, GAD patients' scores on the STAI-T indicated substantial levels of anxiety, whereas SP patients and control participants scored lower. On the STAI-S, GAD patients reported significantly more anxiety than the two other groups both before and after the experiment. After the experiment, the difference between social phobics and control participants was significant as well. In addition, a joint analysis of the STAI-S scores observed before and after the experiment showed that, in all three participant groups, STAI-S scores changed very little during the course of the experiment. Accordingly, a two-way analysis of variance (ANOVA) of these scores yielded a strong effect of participant group, F (2, 78) = 35.71, p < .001, f = .82, whereas the time of measurement (before vs. after the experiment) did not reach significance, F (1, 78) = 1.35, ns , f = .06. The interaction was marginally significant, F (2, 78) = 2.99, p < .06, f = .12. Emotional state during the task. F tests indicated differences between the three groups for reported tension, anxiety, and excitement, but not avoidance. As expected, Scheffé tests confirmed that both GAD and SP patients rated themselves as significantly more tense (GAD M = 2.3, SD = 2.5 vs. SP M = 1.7, SD = 2.0) and anxious (GAD M = 2.4, SD = 2.4 vs. SP M = 1.6, SD = 1.8) than the control participants (tense M = 0.6, SD = 1.0 vs. anxiety M = 0.7, SD = 1.0) did (both p s < .05), but they did not differ from each other significantly. With regard to excitement and anxiety, only GAD patients (excitement M = 2.9, SD = 2.7 vs. anxiety M = 2.4, SD = 12.4) gave higher ratings than did the control participants (excitement M = 1.8, SD = 2.0 vs. anxiety M = 0.7, SD = 1.0, p < .05). The avoidance ratings of the three participant groups did not differ significantly from one another (GAD M = 1.4, SD = 2.3 vs. SP M = 0.8, SD = 1.4 vs. control participants M = 0.4, SD
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= 0.8). Thus, these results indicate that the emotional state of the two patient groups during the memory test was comparable. Free recall. Participants' performance in the free recall test was analyzed with the number of words each participant remembered correctly from each word type as the dependent variable. This number could vary between zero and six. To facilitate comparison of these results with those of the second experiment, mean percentages of words recalled and corresponding standard deviations of correctly recalled words broken down by group and word type are shown in Table 4 . A two-way ANOVA of the free recall data showed no significant difference in memory performance between the three groups: Overall, both GAD and SP patients recalled as many words as did the control participants, F (2, 90) < 1, ns , f = .06. Word type had a significant effect, F (3, 270) = 7.21, p < .001, f = .22, in that positive words were better recalled than the other word types. Most important, however, the interaction of group and word type was not significant, F (6, 270) = 1.25, ns , f = .13. Therefore, in this experiment no patient group exhibited a selective memory bias in free recall. Furthermore, free recall did not correlate significantly with ease of imaging ( r = .09), probably because of a ceiling effect, because all stimulus words had been selected to be easy to imagine. Intrusions in the free recall test. To check for response biases, we also analyzed the intrusions in the memory test, that is, the words that were "recalled" but in fact were not presented. The overall number of intrusions was very low (on average, 0.15), despite the fact that the instructions encouraged guessing. The few words produced were classified into the four word types described above. The ANOVA of these data did not reveal any significant effects (all F s < 1.35, ns ). These results indicate that no response bias occurred in this experiment. Taken together, the results of Experiment 1 indicate that no memory bias occurred in either GAD patients or SP patients. Contrary to dominant theoretical conceptions (e.g., Beck et al., 1985 ; Bower, 1981 , 1987 ), but in accordance with other empirical studies, neither a specific bias toward anxietyrelated information nor a bias favoring the retention of emotional information in general was observed.
Experiment 2 Experiment 2 was conducted to find out if a memory bias for anxiety-related information would occur in PD patients, with the same experimental procedures as in Experiment 1. If a memory bias for anxietyrelated information occurred in this experiment, methodological explanations for the observed differences between PD versus GAD and SP would be rendered unlikely. In addition, Experiment 2 delineated in more detail the nature of the expected memory bias in PD patients by using three different types of panic-related words: frightening situations, physical symptoms of anxiety, and catastrophic cognitions. In previous studies with PD patients, no distinction was made between different types of panic-related words, so it was impossible to tell whether the PD memory bias generalizes to relevant situations, symptoms, and cognitions. Method Participants. We recruited 30 PD with agoraphobia patients from the Christoph-Dornier inpatient treatment center in Münster, Germany and 30 control participants in Dresden, Germany. The agoraphobic avoidance had to be at least moderate for the patients to be included in this study. All participants were interviewed with
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the DIPS (Diagnostisches Interview bei psychischen Störungen; Margraf, Schneider, & Ehlers, 1991 ), a German version of the Anxiety Disorders Interview Schedule (ADIS—R; DiNardo & Barlow, 1988 ). Interviews were conducted by trained psychologists. Control participants had no diagnosis. None of the participants were taking psychoactive medication. For patients, the experiment took place during the diagnostic phase, before treatment. Control participants were paid. The groups did not differ in age (agoraphobia M = 39.9; controls M = 39.9), gender (agoraphobia, 63% female; controls, 63% female) or education. Questionnaires and emotional state ratings. Participants received a battery comparable to the questionnaires used in Experiment 1, except for the SCL-90. As in Experiment 1, participants gave four retrospective ratings of their emotional state during the experiment. Stimulus words. Experts on anxiety disorders were asked to judge words for their relevance to patients suffering from agoraphobia. From this word pool, those with the highest relevance ratings were chosen as experimental stimuli. They comprise three classes of agoraphobia-relevant words: situational words, symptom words, and catastrophic cognitions. Then neutral words and positive words were selected from the norms of Hager and Hasselhorn (1994) to be comparable in valence, ease of visual imaging, word length, and the type of word (noun, verb, adjective). Altogether, there were 21 agoraphobia-relevant words (7 situational words, 7 symptom words, and 7 catastrophic cognitions), 7 neutral words, and 14 positive words. The number of positive words was doubled to avoid a negative mood induction caused by the incidental learning task. Table 5 shows the stimulus material. As in Experiment 1, participants rated the words after the experiment on the dimensions of relevance, excitement, and emotional valence, this time on a scale ranging from 0 ( not at all ) to 6 ( extremely ). The agoraphobia-related words were significantly more relevant to the PD patients than to the control participants (3.67 vs. 1.97), whereas the neutral words (0.94 vs. 1.47) and positive words (4.38 vs. 4.96) were comparably relevant to both groups. All three types of agoraphobia-related words were significantly more relevant to the patients. Furthermore, anxiety symptoms (3.69), agoraphobic situations (3.44), and anxiety cognitions (3.87) did not differ in relevance to the PD patients. Similar patterns emerged for excitement and valence: Agoraphobia-related words were rated as more exciting and more negative by PD patients. The positive words were rated as positive and the anxiety-related words as negative. Thus the words were relatively well chosen. Incidental learning task, free recall test, and procedure. The learning task and the recall test were identical to the ones used in Experiment 1. Procedural differences were minor; that is, only three practice words were shown and the distractor task lasted 4.5 min. In this experiment, the distractor task was the d2 test ( Brickenkamp, 1962 ), a concentration test. Design. Full combination of the independent variables experimental group (patients with agoraphobia and control participants) and word type (agoraphobia-relevant words: situational, symptoms and cognitions, neutral words and positive words) yielded a 2 × 5 design. Word type was a within-subjects factor and experimental group a between-subjects factor. Percentage of correctly recalled words and the number of intrusions in the free recall test were the dependent variables. Effect sizes were computed according to
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Cohen (1988) and are given as f values. Results Questionnaires. As expected, the PD patients scored significantly higher than the control participants on all questionnaires used (see the p levels shown in Table 6 ). The BDI scores indicate moderate to severe levels of depression in the patient group. As expected, patients' scores on the STAI-T indicated substantial levels of anxiety. The PD patients reported significantly more anxiety on the STAI-S than the control participants did, both before and after the experiment. Again, a joint analysis of the STAI-S scores observed before and after the experiment was computed as well. This two-way ANOVA of the STAI-S scores gave a strong effect of participant group, F (1, 58) = 44.05, p < .001, f = .79, while the time of measurement (before vs. after the experiment) did not reach significance, F (1, 58) < 1, f = .05. The interaction was significant as well, F (1, 58) = 6.97, p < .05, f = .13, indicating that the PD patients calmed down more during the experiment than did the control participants. Emotional state during the task. As in Experiment 1, participants rated their emotional state on the four rating scales for excitement, tension, anxiety, and avoidance after they had finished the incidental learning task. Surprisingly, there were no statistically significant differences between the PD patients and the control participants. On all four scales both groups gave comparable ratings, although patient means were slightly higher (PD: anxiety M = 1.8, SD = 1.8, excited M = 3.3, SD = 2.6, tense M = 5.4, SD = 2.8, avoidance M = 1.1, SD = 2.2 vs. control participants: anxiety M = 1.1, SD = 1.9, excited M = 2.6, SD = 1.9, tense M = 4.9, SD = 2.4, avoidance M = 0.9, SD = 2.1). Free recall. The mean percentage of words correctly recalled in the free recall test broken down by experimental group and word type is shown in Table 7 . Because of the unequal number of words in the different word types, participants' performance in the free recall test was analyzed in percentages. To adjust for the abnormal distribution of percentages, the arcsine-transformed percentage of words each participant remembered correctly from each word type was used as the dependent variable (see Winer, 1971 ). The two-way ANOVA of these data showed no significant difference in the overall performance of the two groups: Overall, the PD patients recalled as many words as the control participants did, F (1, 58) = 2.82, ns , f = .11. Word type had a significant effect, F (4, 232) = 10.86, p < .001, f = .36, in that positive words and agoraphobic situations were recalled better by both groups than were the other three word types. Most important, there was a significant interaction of group and word type, F (4, 232) = 2.42, p < .05, f = .17. Table 7 shows that the patients suffering from PD with agoraphobia recalled significantly more anxiety symptoms than the control participants did. A similar difference was observed for agoraphobic situations, which, however, missed statistical significance. Interestingly, there was no difference between the two groups for catastrophic cognitions. Also, both groups recalled comparative numbers of positive and neutral words. Therefore, in this experiment a selective memory bias for anxiety-related words in patients suffering from PD with agoraphobia did occur. Anxiety symptoms were particularly salient for these patients. As in the previous experiment, free recall did not correlate significantly with ease of imaging. Furthermore, the two participant groups did not differ regarding their ability to create visual images of the stimulus words, F (1, 58) = 1.20, ns . Intrusions. Each falsely recalled word was classified by two independent raters as either an agoraphobic situation,
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an anxiety symptom, an anxiety cognition, a positive word, or a neutral word. The overall number of intrusions was very low and averaged 0.43 words. In the ANOVA of these data neither the main effect of group nor the interaction of experimental group and word type reached statistical significance (all F s < 1.66, ns ). The main effect of word type was significant, F (4, 232) = 2.46, p < .05, indicating that most intrusions were classified as neutral or positive. Thus, there was no indication of a response bias that could explain the pattern of results found in the free recall data. Influence of anxiety and depression on the memory bias. As mentioned before, PD patients had higher scores than control participants on both the anxiety questionnaires and the depression questionnaire (the BDI). This is a frequent result in studies of anxiety disorders, and it raises the question whether differences in depression contributed to the memory bias observed in this experiment in addition to differences in anxiety. This is a plausible assumption with regard to memory biases, given that Williams et al. (1988 , 1997 ) concluded from earlier research that depressed patients are particularly likely to exhibit memory biases. To determine the effect of depression independent of anxiety effects, we correlated questionnaire scores with a memory bias score. In a first analysis, the bias score was computed by subtracting each participant's arcsine-transformed percentage of correctly recalled neutral words from his or her arcsine-transformed percentage of correctly recalled anxiety words. Thus, the three different types of anxiety words were analyzed together. The higher the resulting bias score, the stronger the participant's tendency to favor anxietyrelated words in free recall. Correlations and partial correlations between the bias score and the scores of the BDI, STAI-T, and the STAI-S before and after the experiment were computed. In this analysis, all questionnaire scores correlated with the memory bias score to a similar, low degree: r = .25, ( p < .10) for the STAI-T; r = .28, ( p < .05) for the STAI-S before the experiment; r = .26 ( p < .05) for the STAIS after the experiment; and r = .35 ( p < .01) for the BDI. The BDI score correlated with the bias score if the STAI scores were partialled out ( r = .24, p < .05). Thus, these results suggest that there was indeed a weak, but independent, correlation between depression and memory bias in the free recall test. In contrast, the STAI-T scores did not correlate significantly with the bias score if the BDI scores were partialled out ( r = − .09, ns ). The same was true for the STAI-S scores both before ( r = .06, ns ) and after the experiment ( r = .04, ns ). Thus, state and trait anxiety did not seem to have an independent relation to the memory bias. In a second analysis, the bias score was computed by subtracting each participant's arcsine-transformed percentage of correctly recalled neutral words from his or her arcsine-transformed percentage of correctly recalled anxiety symptom words. Because the symptom words were associated most strongly with the PD patients' memory bias, one might expect a stronger correlation with the STAI scores and a weaker correlation with the BDI scores. However, the observed correlations of this symptom memory bias score did not differ significantly from those observed for the combined score reported above: r = .28 ( p < .05) for the STAI-T; r = .36 ( p < .01) for the STAI-S before the experiment; r = .25 ( p < .05) for the STAI-S after the experiment; and r = .34 ( p < .01) for the BDI. The STAI-T scores did not correlate significantly with the symptom bias score if the BDI scores were partialled out ( r = − .02, ns ). Similar results were found for the STAI-S scores both before ( r = .19, p < .10) and after the experiment ( r = .05, ns ). Also, the BDI score did not correlate significantly with the bias score if the STAI scores were partialled out ( r = .15, ns ). Thus, these results suggest that depression and anxiety had an interdependent relation to symptom memory bias.
General Discussion The first experiment compared GAD patients, social phobics, and control participants to each other and
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did not find a memory bias toward disorder-relevant materials. Neither GAD patients nor social phobics remembered words relevant to their fears better than control participants did. Because the sample sizes used in this experiment should have been sufficient to find any existing memory bias, lack of experimental power is not a sufficient explanation for the lack of findings. Also, the incidental learning task and the free recall test are considered to be well suited for showing explicit memory effects ( Bower & Cohen, 1982 ; Fiedler & Ströhm, 1986 ). In addition, they match each other by both being conceptually driven tests ( Eysenck & Byrne, 1994 ). For observing selective memory biases, it is crucial to use materials that are relevant to the disorders and part of the patients' threat schemata. As mentioned before ( Reidy & Richards, 1997 ), it is not easy to find suitable materials for patients with GAD. This patient group is worried about a rather wide and diverse selection of threatening stimuli, and therefore, it is difficult to find words that are relevant to each individual patient. The ratings of the materials used in Experiment 1 showed that the GAD-relevant words were rated as highly relevant and unpleasant by GAD patients. However, these words were not more relevant or unpleasant than they were for the SP patients. This shows that the GAD-relevant words were meaningful and threatening, although they might not have been the most salient words for each individual patient, as reflected by the rather large standard deviation (2.25) observed for the GAD patients' relevance ratings of GAD-related words. Therefore, future studies might choose individual words for each participant, thereby sacrificing counterbalancing of materials for higher relevance of the materials. The speech-relevant words in this experiment, on the other hand, were well chosen according to the ratings given by the SP patients. This group rated the speech-relevant words as significantly more relevant and unpleasant than both other groups. Still, they did not show enhanced memory for these words. Thus, it seems that the lack of effects in Experiment 1 cannot be easily explained by inadequate materials. The second experiment compared patients suffering from PD with agoraphobia to control participants, and in contrast to the first experiment, the patient group did show selective memory for disorder-relevant words. There were three groups of words of theoretical importance to the patients: agoraphobic situations, catastrophic cognitions, and physical anxiety symptoms. Physical anxiety symptoms were the disorder-relevant words that revealed the strongest memory bias in the PD patient group. The PD patients remembered more words referring to bodily symptoms than did the control participants, whereas both groups remembered about the same number of neutral and positive words. The memory bias shown by the anxiety patients was therefore highly selective and cannot be explained by a general bias toward emotional words. The preference for bodily symptom words also demonstrates their special relevance for the anxiety schema in PD with agoraphobia. Furthermore, this finding supports the hypothesis that "fear of fear" is a central issue in PD and that treatments which focus on this problem (e.g., interoceptive exposure) are on the mark. Surprisingly, agoraphobic situations were not as important to these patients, and catastrophic cognitions even less. The relation of anxiety and depression measures to memory biases was complex. Depression scores correlated with the general memory bias, even after anxiety scores were partialled out. This correlation, however, was weak and not replicated when depression was correlated with the specific memory bias for physical symptom words. Partial correlations of anxiety with the two memory bias scores showed a more consistent pattern of results, namely, that the correlation of anxiety with the memory biases disappeared when depression was partialled out, perhaps because symptoms experienced by anxious and depressed patients overlap. In any case, neither anxiety nor depression was strongly related to the memory bias observed in Experiment 2, and so other factors must be considered. Some of our results may have depended on the degree of categorization inherent in the experimental materials. Words that form a coherent category are more easily learned and recalled than unrelated words ( Klein & Kihlstrom, 1986 ). Moreover, anxiety-related words may be grouped into a category
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more easily by anxiety patients. Thus, as Mogg, Kentish, and Bradley (1993) suggested, their memory bias for threat-related words might be due to better categorization of these words rather than to their relation to the patients' fear schema. However, this hypothesis does not explain our results very well. First, in both experiments, the positive words might easily be grouped into a category of "pleasant things"; nevertheless, anxiety patients did not show a memory bias for these words. Second, and more important, the speech-related words used in Experiment 1 as well as the situations and cognitions used in Experiment 2 form very coherent categories for SP patients and PD patients, respectively. Nonetheless, no memory bias was observed for these words. Another, rather unlikely, explanation of the memory bias is that it occurs because threat-related words are more familiar to PD patients than to control participants. However, if that were true, why did not the SP patients of Experiment 1 show a memory bias for speech-related words and the PD patients of Experiment 2 for panic-related situations and cognitions? Moreover, prior studies testing patients before and after successful therapy ( Mathews et al., 1989 ; Mathews, May, Mogg, & Eysenck, 1990 ) or testing anxiety therapists as a control group ( Cloitre et al., 1994 ; McNally, Riemann, & Kim, 1990 ) speak against familiarity as an explanation of the memory bias. The relevance ratings collected in both experiments did not offer an explanation either: Anxiety symptoms were not rated as more relevant to PD patients than situations or cognitions, and they were not more relevant to the PD patients than the GAD-related words were to the GAD patients. Furthermore, it seems difficult to explain the observed results as differences in imagery. In both experiments, all stimulus words were selected to be easily imaged. This was confirmed by the ease of imagery ratings that the participants gave in both experiments. Finally, the number of relevant words presented to participants does not explain the memory bias either: It is true that the PD patients in Experiment 2 were exposed to more relevant words than GAD or social phobia patients were in Experiment 1. However, there are at least two studies ( MacLeod & McLaughlin, 1995 ; Mathews et al., 1989 ) in which the GAD patients encountered 50% relevant words, which is just as many as the PD patients encountered in Experiment 2. Nonetheless, the GAD patients in these studies did not show a memory bias. Moreover, there are several studies in which PD patients encountered fewer relevant words than in Experiment 2, that is, 33% ( Becker et al., 1994 ; Cloitre & Liebowitz, 1991 ; Cloitre et al., 1994 ). Yet the PD patients showed a memory bias in all of these studies. Thus, the ratio of relevant to irrelevant words does not explain the occurrence of the memory bias. The same is true for the absolute number of relevant words: The studies with GAD patients listed in Table 1 used between 16 and 36 relevant words, and the studies with PD patients between 9 and 30 words. Despite these similar numbers, an explicit memory bias was observed solely with PD patients. Although the results of our experiments fit in well with previous findings reported in the literature, they are hard to explain on the basis of current theories ( Beck et al., 1985 ; Bower, 1981 , 1987 ; Williams et al., 1988 , 1997 ). As a first attempt to accommodate the empirical findings, Mathews and MacLeod (1994) acknowledged that panic patients may be an exception to the rule that memory biases are restricted to depression. But one could also conclude that GAD patients should be an exception. GAD patients ruminate and worry most of the time ( Craske, Rapee, Jackel, & Barlow, 1989 ), thereby having the opportunity to elaborate their fears at least as much as PD patients. Yet GAD patients do not show a memory bias. Although some results indicate that the GAD patients' thought processes might prevent deeper processing and physiological arousal ( Borkovec & Hu, 1990 ; Borkovec & Inz, 1990 ; Borkovec, Lyonfields, Wiser, & Deihl, 1993 ), it is hard to believe that these patients would not have extensive threat schemas. In addition, SP patients are known to exhibit an attentional bias toward threatening materials, for example, both words and pictures of faces ( Byrne & Eysenck, 1995 ), without having an explicit memory bias for these materials ( Cloitre et al., 1995 ; Lundh & Öst, 1997 ; Rapee et al., 1994 ).
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Of course, methodological problems might be responsible for the lack of findings for GAD and SP patients in Experiment 1. However, using almost identical procedures in Experiment 2, disordercongruent stimuli in panic patients resulted in an explicit memory bias. The only major difference between both experiments is the nationality and language of the participants: Experiment 1 was conducted with American participants and English materials, and the participants and materials of Experiment 2 were German. We cannot imagine how this difference might explain the different results observed in the two experiments, particularly because other studies have given consistent results independent of nationality and language. One speculative explanation of the memory differences in anxiety disorders, particularly GAD versus PD, might be deduced from the results reported by Borkovec and his colleagues ( Borkovec & Hu, 1990 ; Borkovec et al., 1993 ). These authors observed that GAD patients' ruminations serve to reduce the amount of physiological arousal associated with processing of threat-related stimuli. Physiological arousal can affect memory storage (for reviews see Revelle & Loftus, 1992 , or McGaugh, 1992 ), and there is some evidence that the memory bias for threat-related information increases with heightened physiological arousal ( McNally et al., 1989 ). Thus, if the PD patients' physiological arousal during processing of threat-related words was higher than the GAD patients' arousal, the occurrence of a memory bias in PD, and not in GAD, might be explained. Unfortunately, the excitement ratings collected in this study are less than optimal for measuring the hypothesized differences in arousal because they were subjective and collected after the experiment. In order to assess arousal appropriately, physiological variables (e.g., skin conductance or heart rate) would have to be measured during learning. This was not done in the experiments reported here but should be done in future experiments, which also need to distinguish between effects of tonic activation and phasic activation to individual disorderrelevant stimuli. It remains to be determined how social phobia fits into this argument. SP patients may indeed show less physiological arousal than PD patients, as they have, for example, in challenge tests ( Caldirola, Perna, Arancio, Bertani, & Bellodi, 1997 ). In a behavior assessment test (giving a speech), only about half of the SP patients were more aroused than control participants ( Hofmann, Newman, Ehlers, & Roth, 1995 ). Thus, the lack of a memory bias in social phobia is possibly a consequence of less physiological arousal in these patients in the testing situation. To summarize, we have obtained a pattern of results that is consistent with findings in the literature but that is inexplicable by existing theories: Panic disorder patients show an explicit memory bias for disorder-relevant material, whereas GAD and SP patients do not. Furthermore, our two experiments indicate that this pattern of results cannot be attributed to methodological differences or shortcomings of the empirical studies. Further research is needed to determine whether the same is true for other anxiety disorders such as specific phobia, PTSD, or obsessive-compulsive disorder, and for major depression. Memory biases in these disorders should also be investigated systematically and compared with each other directly. The most sensitive procedures should be applied identically to multiple disorders, with sufficiently large sample sizes, disorder-specific stimuli, and an incidental learning task paired with a free recall test. Should the current pattern of results turn out to be reliable, new theoretical explanations will be urgently needed. Current theories (e.g., Beck et al., 1985 ; Bower, 1981 , 1987 ; Williams et al., 1997 ) may have to be extended, revised, or replaced.
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retrieval cues in the retention of categorized lists. Journal of VerbalLearning and Verbal Behavior, 14, 408-417. Eysenck, M. W. (1992). Anxiety: The cognitive perspective. (Hove, England: Erlbaum) Eysenck, M. W. & Byrne, A. (1994). Implicit memory, explicit memory bias, and anxiety. Cognition and Emotion, 8, 415-431. Fiedler, K. & Ströhm, W. (1986). What kind of mood influences what kind of memory: The role of arousal and information structure. Memory & Cognition, 14, 181-188. Foa, E. & Kozak, M. J. (1986). Emotional processing of fear: Exposure to correcting information. PsychologicalBulletin, 99, 20-35. Foa, E. B., McNally, R. & Murdock, T. (1989). Anxious mood and memory. Behaviour Research and Therapy, 27, 141-147. Francis, W. N. & Kučera, H. (1982). Frequency analysis of English usage. (Boston: HoughtonMifflin.) Hager, W. & Hasselhorn, M. (1994). Handbuch deutschsprachiger Wortnormen. (Göttingen, Germany: Hogrefe) Hofmann, S. G., Newman, M. G., Ehlers, A. & Roth, W. T. (1995). Psychophysiological differences between subgroups of social phobia. Journal of Abnormal Psychology, 104, 224-231. Klein, S. B. & Kihlstrom, J. F. (1986). Elaboration, organization, and the self-reference effect in memory. Journal of Experimental Psychology: General, 115, 26-38. Lundh, L.—G. & Öst, L.—G. (1997). Explicit and implicit memory bias in social phobia: The role of subdiagnostic type. Behaviour Research and Therapy, 35, 305-317. MacLeod, C. & McLaughlin, K. (1995). Implicit and explicit memory bias in anxiety: A conceptual replication. BehaviourResearch and Therapy, 33, 1-14. Margraf, J., Schneider, S. & Ehlers, A. (1991). DIPS: Diagnostisches Interview bei psychischen Störungen. (Berlin:Springer.) Martin, M., Williams, R. M. & Clark, D. M. (1991). Does anxiety lead to selective processing of threatrelated information? Behaviour Research and Therapy, 29, 147-160. Mathews, A. & MacLeod, C. (1994). Cognitive approaches to emotion and emotional disorders. Annual Review ofPsychology, 45, 25-50. Mathews, A., May, J., Mogg, K. & Eysenck, M. (1990). Attentional bias in anxiety: Selective search or defective filtering? Journal of Abnormal Psychology, 99, 166-173. Mathews, A., Mogg, K., May, J. & Eysenck, M. (1989). Implicit and explicit memory bias in anxiety. Journal of AbnormalPsychology, 96, 236-240. McGaugh, J. L. (1992). Affect, neuromodulatory systems, and memory storage.(In S.-A. Christianson (Ed.), Handbook of emotion and memory: Research and theory (pp. 245—268). Hillsdale, NJ: Erlbaum.) McNally, R. J. & Amir, N. (1996). Perceptual implicit memory for trauma-related information in posttraumatic stress disorder. Cognition and Emotion, 10, 551-556. McNally, R. J., Foa, E. B. & Donnell, C. D. (1989). Memory bias for anxiety information in patients with panic disorder. Cognition and Emotion, 3, 27-44. McNally, R. J., Riemann, B. C. & Kim, E. (1990). Selective processing of threat cues in panic disorder. BehaviourResearch and Therapy, 28, 407-412. Mogg, K., Kentish, J. & Bradley, B. P. (1993). Effects of anxiety and awareness on colour-identification latencies for emotional words. Behaviour Research and Therapy, 31, 559-567. Mogg, K. & Mathews, A. (1990). Is there a self-referent mood-congruent recall bias in anxiety? Behaviour Research andTherapy, 28, 91-92. Mogg, K., Mathews, A. & Weinman, J. (1987). Memory bias in clinical anxiety. Journal of Abnormal Psychology, 96, 94-98. Norton, G., Schaefer, E., Cox, B., Dorward, J. & Wozney, K. (1988). Selective memory effects in nonclinical panickers. Journal of Anxiety Disorders, 2, 196-177. Nunn, J., Stevenson, R. & Whalan, G. (1984). Selective memory effects in agoraphobic patients. British
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Journal ofClinical Psychology, 23, 195-201. Otto, M. W., McNally, R. J., Pollack, M. H., Chen, E. & Rosenbaum, J. F. (1994). Hemispheric laterality and memory bias for threat in anxiety disorders. Journal of AbnormalPsychology, 103, 828831. Paivio, A. (1971). Imagery and verbal processes. (New York: Holt, Rinehart, & Winston) Pickles, A. J. & van den Broek, M. D. (1988). Failure to replicate evidence for phobic schemata in agoraphobic patients. British Journal of Clinical Psychology, 27, 271-272. Rapee, R. M., McCallum, S. L., Melville, L. F., Ravenscroft, H. & Rodney, J. M. (1994). Memory bias in social phobia. Behaviour Research and Therapy, 32, 89-99. Reidy, J. & Richards, A. (1997). Anxiety and memory: A recall bias for threatening words in high anxiety. BehaviourResearch and Therapy, 35, 531-542. Revelle, W. & Loftus, D. A. (1992). The implications of arousal effects for the study of affect and memory.(In S.-A.Christianson (Ed.), Handbook of emotion and memory: Research and theory (pp. 113—149). Hillsdale, NJ: Erlbaum.) Sanderson, W. C. & Wetzler, S. (1991). Chronic anxiety and generalized anxiety disorder: Issues in comorbidity.(In R. M.Rapee & D. Barlow (Eds.), Chronic anxiety: Generalized anxiety disorder and mixed anxiety-depression. New York: Guilford Press.) Sanz, J. (1996). Memory bias in social anxiety and depression. Cognition and Emotion, 10, 87-105. Spielberger, C. D., Gorsuch, R. L. & Lushene, R. E. (1970). Manual for the State-Trait Anxiety Inventory. (Palo Alto, CA: Consulting Psychologists Press) Spitzer, R. L., Williams, J. B. & Gibbon, M. (1987). Structured clinical interview for DSM—III—R. (NewYork: New York State Psychiatric Institute.) Vrana, S. R., Roodman, A. & Beckham, J. C. (1995). Selective processing of trauma-relevant words in posttraumatic stress disorder. Journal of Anxiety Disorders, 9, 515-530. Watts, F. N., Trezise, L. & Sharrock, R. (1986). Processing of phobic stimuli. British Journal of ClinicalPsychology, 77, 97-108. Williams, J. M. G., Watts, F. N., MacLeod, C. & Mathews, A. (1988). Cognitive psychology and emotional disorders. (Chichester, England: Wiley) Williams, J. M. G., Watts, F. N., MacLeod, C. & Mathews, A. (1997). Cognitive psychology and emotional disorders ((2nd ed.). Chichester, England: Wiley) Winer, B. J. (1971). Statistical principles in experimental design. (New York: McGraw-Hill) Table 1. Overview of Studies on Memory Biases in Anxiety Disorders
Table 2. Stimulus Words Used in Experiment 1
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Table 3. Participant Characteristics in Experiment 1
Table 4. Mean Percentage of Words (With Standard Deviations) Reproduced in the Free Recall Test of Experiment 1
Table 5. Stimulus Words Used in Experiment 2
Table 6. Participant Characteristics in Experiment 2
Table 7. Mean Percentage of Words (With Standard Deviations) Reproduced in the Free Recall Test of Experiment 2
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