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Attention and memory for threat in panic disorder
Behav. Res. The-r. Vol. 30, No. 6, pp. 619-629, Printed in Great Britain. All rights reserved
1992 Copyright
0005.7967/92 $5.00 + 0.00 Q 1992 Pergamon Press Ltd
ATTENTION AND MEMORY FOR THREAT IN PANIC DISORDER J. GAYLE BECK,‘* MELINDA A. STANLEY,’ PATRICIA M. AVERILL,’ LAURIE E. BALDWIN’ and EDWIN A. DEACLE III’ ‘University of Houston, 4800 Calhoun Street, Houston, TX 77204-5341 and *University of Texas Medical School, 1300 Moursund Street, Houston, TX 77030-3497, U.S.A. (Received 22 November 1991)
Summary-Recently, information processing paradigms have been utilized to explore the role of attentional and memory processes in the maintenance of clinical anxiety disorders. The present study extended these data using a dual-task paradigm to assess attentional vigilance and a cued recognition task to evaluate short-term memory effects in Panic Disorder (PD). Twenty PD patients and 20 normal controls completed a computerized task wherein they read aloud one of a pair of rapidly presented words (primary task) while simultaneously attempting to detect a small probe that appeared adjacent to one of the words (secondary task). Eighty stimulus words were chosen to represent four categories: physical panic-related threat, social threat, positive-emotional, and neutral. Reaction time and accuracy in detecting the probe were assessed, as well as psychophysiological responding (heart rate, skin conductance, EMG). Following task completion, a cued recognition task was administered to examine short-term memory of task stimuli. Results indicated that PD patients exhibited slower reaction times relative to normal controls during presentation of physical panic-related threat and positive-emotional stimuli. A similar trend emerged for social threat stimuli, although the PD and control samples responded similarly to neutral stimuli. No group differences were found on the cued recognition measure or psychophysiological responding during task performance. The data are discussed in terms of possible implications for cognitive models of PD.
Cognitive theories have been proposed to account for the origin and maintenance of fears in the anxiety disorders (e.g. Barlow, 1988; Beck, Emery & Greenwald, 1985; Lang, 1979). These models postulate that anxiety and specific fears arise from overactivity of the cognitive processes involved in detecting threat and personal danger. Each of these models proposes that anxiety disorders are maintained by the manner in which fear-relevant information is perceived, encoded, and recalled. For example, Beck et al. (1985) and Lang (1979) have postulated that patients with Panic Disorder (PD) are hypervigilant to information associated with feared stimuli, such as the sensations of increased heart rate, rapid respiration, and sweating. This extreme sensitivity theoretically arises from greater ease or automaticity in activating fear-relevant imagery (Lang, 1979) or related cognitive processes involving encoding and memory (Beck et al., 1985). Proponents of this approach have traditionally utilized self-report methods to support these models (e.g. Beck, Laude & Bohnert, 1974; Hibbert, 1984). For example, Hibbert (1984) noted that PD patients report worry about bodily harm when anxious, while patients with Generalized Anxiety Disorder (GAD) report worry about personal inadequacy. Although such data provide indirect support for cognitive models of the anxiety disorders, this method captures only those aspects of cognition which can be verbalized. More recent research has used information processing paradigms derived from experimental cognitive psychology to examine directly the influence of cognitive processing factors in the maintenance of anxiety and panic. To date, studies utilizing these paradigms have examined attentional allocation, memory processes, and the interpretation of ambiguous verbal stimuli in a variety of anxiety syndromes, including obsessive-compulsive disorder (e.g. Foa & McNally, 1986), post-traumatic stress disorder (e.g. Foa, Feske, Murdock, Kozak & McCarthy, 1991) GAD (e.g. Mathews & MacLeod, 1985), phobic disorders (e.g. Burgess, Jones, Robertson, Radcliffe & Emerson, 1981) and PD (e.g. Ehlers, Margraf, Davies & Roth, 1988). In general, two distinct types of paradigms have been used in these studies. First, encoding processes have been examined, with particular focus on the role of perceptual or sensory aspects of the stimulus and attentional vigilance. Second, semantic processes, in particular memory recall *Author for correspondence. 619
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and recognition of threat-related stimuli, have been measured. These paradigms assess different levels of cognitive processing and reflect the distinction between encoding, which is conceptualized as an index of processing capacity, and recall/recognition, which is determined by semantic memory and presumably guides the selection of stimuli for long-term encoding (e.g. Atkinson & Shiffrin, 1968). With reference to the anxiety disorders, this distinction implies that overactivity of semantic memory for threat information could effect the speed of perceiving stimuli involving harm, as well as enhancing recall or recognition of these cues. However, data derived from GAD patients have not been supportive of this hypothesis. For example, Mogg, Mathews and Weinman (1987) reported slightly poorer recall and recognition for threat information in GAD patients, relative to controls, suggesting that an inhibitory process interferes with memory storage of threatening information in anxious patients. This ‘cognitive avoidance’ process potentially could serve to maintain anxiety disorders, by preventing habituation or accurate evaluation of incoming stimuli. Thus, the distinction between encoding and memory becomes central in considering information processing models of anxiety. Of the identified anxiety disorders, PD with and without agoraphobia is the most prevalent, both in the community at large (Meyers, Weissman, Tischler, Holzer, Orvaschel, Anthony, Boyd, Burke, Kramer & Stoltzman, 1984) and in treatment clinics (Barlow, 1988). PD is characterized by an enduring fear of the physical sensations that occur during panic attacks (DSM-III-R, American Psychiatric Association, 1987). By definition, these fears involve beliefs that anxiety sensations are signs of serious underlying physical and/or psychological problems, such as a heart attack or serious mental illness (e.g. Clark, 1986; Goldstein & Chambless, 1978). Research is beginning to examine the role of information processing factors in PD. For example, Ehlers et al. (1988) addressed both attentional and memory processes in PD, using a modified Stroop color naming task involving flashcards containing threat words related to physical harm, separation, and social humiliation. In this study, slower reaction times for color naming threat words were noted in both PD patients and nonclinical panickers, relative to controls. However, no between-group differences were found for cued recognition of stimulus words after the task. Thus, these data suggest that interference in encoding, but not memory is salient in PD. Other studies have demonstrated similar Stroop interference effects for threat words in PD, relative to controls (McNally, Riemann & Kim, 1990) but data from memory paradigms have been inconsistent with the Ehlers et al. (1988) data. For example, at least two studies have demonstrated that PD patients (with and without agoraphobia) show enhanced free recall for threat-relevant stimuli (McNally, Foa & Donnell, 1989; Nunn, Stevenson & Whalan, 1984). Thus, saliency in short-term memory may operate to maintain PD, although the interaction between encoding and memory processes is uncertain. Further clarification of the role of encoding processes in PD may occur by utilizing alternative cognitive paradigms to document shifts in attentional allocation between threat and neutral stimuli. In particular, paradigms which simultaneously present two tasks, a primary threat-relevant task and a secondary neutral task, allow determination of the allocation of attention to each type of incoming stimulus (e.g. Posner & Boies, 1971; Navon & Margalit, 1983). If greater interference occurs on the secondary task only in the presence of threat stimuli on the primary task, attentional hypervigilence to threat cues is implicated. MacLeod, Mathews and Tata (1986) reported the use of such a task with GAD patients. In this study, the primary task involved rapid presentation of word pairs, some of which included threat-relevant words (e.g. criticized, injury). The secondary task required detection of a visual probe, in the form of a small dot which appeared in the spatial location of either word immediately after the word display terminated. Ss were required to read one word aloud and subsequently press a hand-held button if a visual probe was detected. The distribution of visual attention was assessed via probe detection latency, which has been shown to be a sensitive measure of visual attention allocation (Navon & Margalit, 1983). Results indicated that GAD patients shifted attention toward threat words, resulting in slower detection latencies of probes appearing in the vicinity of these stimuli (MacLeod et al., 1986). In the present study, a similar paradigm was employed to assess attentional allocation between threat and neutral stimuli. Stimuli were selected to represent four categories: physical panic-related threat words, social threat words, positive-valenced emotional words, and neutral words. Presumably, those stimuli which reflect physical threat would create significant attentional interference for PD patients, given current accounts of the nature of fear in PD. Social threat stimuli were expected
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to result in little to moderate interference, given that PD patients sometimes report secondary fears of doing something embarrassing while having a panic attack in public. Positive stimuli were included as a control for response biases resulting from presentation of emotionally-valenced words. In addition to attentional allocation, the present investigation assessed semantic memory via a cued recognition task presented immediately following the dot probe procedure. This task was modeled after that used by Ehlers et al. (1988) and required Ss to provide estimates of whether each of the series of word cues had been included in the preceding task. In addition, three measures of physiological responding were assessed: heart rate, skin conductance, and upper trapezious EMG. In previous research involving simultaneous assessment of physiological arousal during information processing, results are mixed and suggest that the activation of cognitive fear processes may not be accompanied by increases in autonomic and somatic arousal (Ehlers et al., 1988; McNally et af., 1989). If accurate, this finding implies that an intervening process is required to explain how the activation of fear-relevant cognitive processes instigates surges of physiological arousal that are the hallmark of panic attacks (e.g. Taylor, Sheikh, Agras, Roth, Margraf, Ehlers, Maddock & Gossard, 1986; Freedman, Ianni, Ettudgui & Puthezhath, 1985). Thus, the present study was undertaken to examine allocation of attention and cued recognition of threat-relevant stimuli in PD patients. Twenty PD patients and 20 normal controls, matched by ethnicity, gender, and age, were selected and screened using a semi-structured interview and questionnaire. The hypotheses under examination including the following: (1) PD patients, but not controls, would shift attention toward emotionally-threatening stimuli (physical threat, social threat), resulting in slower latencies in detection of the visual probe on these trials, relative to detection latencies for neutral and positively-valenced stimuli. These effects were expected to be most pronounced when the visual probe appeared in the vicinity of the threat stimulus; (2) PD patients would show enhanced recognition for threat-relevant words, relative to controls, although group differences in short-term memory were not hypothesized for neutral or positively-valenced stimuli; and (3) Activation of these cognitive fear processes would be accompanied by increases in heart rate, skin conductance, and muscle tension, as well as increased reports of anxious mood in the PD sample alone.
METHOD
Subjects Fifty-nine patients with a primary diagnosis of PD (PD sample) were recruited via media announcements and screened initially by phone. If panic appeared to be a primary problem, the Anxiety Disorders Interview Schedule-Revised (DiNardo, Barlow, Cerny, Vermilyea, Vermilyea, Himadi & Waddell, 1985) was administered. All patients with severe agoraphobia were excluded, based on requirements of a subsequent treatment protocol. Diagnostic reliability was established by a second clinician for 17 cases (28.8% of the entire patient sample). 100% diagnostic agreement was noted, most likely due to extensive prescreening of potential Ss. All patients reported being medication-free and were not enrolled in psychotherapy at the time of evaluation. A subset of 20 PD patients was selected randomly for this investigation. This sample included 16 females and 4 males, with a mean age of 38.3 (SD 11.76). The average duration of panic was 4.4 yr with 95% reporting mild (n = 14) or moderate (n = 5) agoraphobia. Clinical severity of PD, based on the degree of impairment and distress was rated on an 8-point Likert scale. Average severity was 3.9 (SD 1.32, range 2-7). The control sample (NC sample) included 20 normals, matched by ethnicity, gender, and age with the PD sample (average age = 36.8; SD = 12.74). All control Ss were screened for psychiatric disorders via the ADIS-R and none reported ever having experienced a panic attack. Control Ss received payment for participation and were recruited from local civic organizations, friendship networks, and the undergraduate population of the University of Houston.
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Table I. Questionnaire
State-Trait Anxiety Inventory State anxiety score Trait anxiety score Beck Depression Inventory Shipley Institute of Living Scale Fear Questionnaire Agoraphobia subscale Blood/injury subscale Social subscale Total Anxiety Sensitivity Inventory
scores for PD and NC samples
45.85 41.75 9.85 100.4
30. IO 32.35 3.85 109.7
16.92 4.10 8.43 3.30
0.0001 0.05 0.006 0.002
10.95 13.47 13.68 38.1 I 33.95
2.25 5.20 5.25 12.70 9.65
16.21 16.59 16.61 30.36 54.02
0.0001 0.0001 0.0001 0.0001 0.0001
All Ss completed the Spielberger State-Trait Anxiety Inventory (STAI; Spielberger, Gorsuch & Lushene, 1970), the Beck Depression Inventory (BDI: Beck, Ward, Mendelsohn, Mock & Erbaugh, 1961), Shipley Institute of Living Scale (SH; Zachary, 1986), the Fear Questionnaire (FQ; Marks & Mathews, 1979), and the Anxiety Sensitivity Inventory (ASI; Reiss, Peterson, Gursky & McNally, 1986). Mean scores are provided in Table 1. As expected, the PD sample exhibited higher levels of state and trait anxiety, depression, anxiety sensitivity, and specific fears on the FQ. Both samples scored within the normal range of IQ on the SH, although a statistically significant difference was noted, with the PD sample scoring slightly lower than the NC sample. Materials
Eighty stimulus words were drawn from previous research by Mathews and colleagues (Mathews, pers. comm., May 1989) and modified for the current study. Twenty of these words were related to physical panic-related threat (e.g. collapse) and 20 to social threat (e.g. humiliated). Additionally, 20 words were positive-valenced emotional words (e.g. confident), and 20 pertained to household activities (e.g. furnished). Physical threat, social threat, and positive stimulus words were matched by independent raters for level of emotionality. Stimulus words are listed in Table 2. Each stimulus word was paired with a neutral word matched for both length and usage frequency to make 80 critical word pairs. Another 250 neutral word pairs matched for word length were generated randomly, to serve as filler items. Word pairs were presented using an IBM-PC microcomputer and a 12-in VGA monitor. Relying on a Scientific Solutions A-D processor and LabPac software, each word pair was presented for 500 msec duration, with words separated on the vertical axis by a distance of 3 cm. Each stimulus word could appear with equal probability in either the top or bottom position. Dot probes occurred on 50% of the total trials, including 100% of the stimulus trials. Dot probes were presented simultaneously with the word pairs and were positioned to the left of either the top or bottom Table 2. Stimulus
words used in the dot probe procedure
Physicalpanic
Social
Positive
Household (neutral)
Collapse Tremble Disease Emergency Attack Illness Tumor Cancer Coronary Ambulance. Paralysis Fatal Tingling Pain Suffocated Death Faint Choking Sweat Dizzv
Persecuted Offended Inept Worthless Hated US&SS Humiliated Indecisive Inferior Hostile Unsuccessful Slle.X Neglected Stupid Hopeless Ridicule Foolish Lonely Unfriendly Snub
Devoted Applause Helpful Superb Achievement Excellent Charm Terrific Delight Comfort Merry Serene Romance Miracle Sensual Confident Enthusiasm Celebration Praise Generous
Lounge Bleach Cushion Domestic Furnished Groceries Ornament Shower Staircase Lamp Mantlepiece Shelves Vase BKXm Towel Switch Wardrobe Chimney Shampoo Upstairs
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words.* The dot probe could appear with equal probability in either position. On each trial, a 1 set intertrial interval followed offset of the word pair. The program recorded reaction time to 1 msec accuracy. Given the design of this study, only the data from the 80 stimulus word pairs are of interest. Thus, two factors were independently varied on stimulus trials: the position of the stimulus word (top/bottom) and the position of the dot probe (top/bottom). The combination of these two factors produced four possible orders. For each S, 20 of the 80 stimulus trials appeared in each order. Specific word pairs were balanced to match order of presentation between groups. Measures Cognitive measures. Two information-processing measures were included: (1) reaction time, measured in milliseconds, collected during the dot probe task, and (2) recognition memory, taken after the completion of the task. For the latter, Ss were administered a 60-item word list and instructed to rate each on a l-4 scale (1 = word was definitely not included in the task; 4 = word was definitely included in the task). Of the 60 items, 20 were derived from the task and 40 were novel filler items. Word order was randomized. Psychophysiological measures. Skin conductance (SC), heart rate (HR), and upper trapezious EMG were measured for each S. SC was assessed from the medial phalanx of the first two fingers of the left hand, using Beckman Ag-AgCl electrodes and a Grass 7Pl preamplifier. The skin surface was cleansed with soap and water immediately prior to sensor attachment, to control for intersubject variation. SC was transformed from mms pen deflection to micromhos conductance based on pre-session calibration (constant voltage of 0.5 V). HR was measured with two Ag-AgCl electrodes placed bilaterally on the chest 5 cm below the midpoint of each clavicle, using a Grass 7P3 preamplifier. HR was converted from a raw EKG signal to a beats-per-minute expression using a Grass 7P44B tachograph. EMG was assessed using three Ag-AgCl electrodes placed in a standard triangular configuration on the upper trapezious muscle, halfway between the C7 vertebrae and the angle of the acromion. A Grass 7P3 preamplifier was used, with a low frequency amplifier setting of 0.3 Hz and a high frequency amplifier setting of 35 Hz. The raw EMG signal was integrated with a time constant of 0.2 sec. The skin surface was cleansed with mildly abrasive soap, to reduce resistance below 10,000 Q. K-Y jelly was used as the conducting medium for all Ag-AgCl electrodes. Afictive measures. Ss completed the Profile of Mood States (POMS; McNair, Lorr & Droppleman, 1971). The POMS is an adjective rating scale which includes six subscales: tension-anxiety, depression-dejection, anger-hostility, vigor-activity, fatigue-inertia, and confusionbewilderment. Ss were instructed to rate each of 65 adjectives on a 5-point Likert scale to indicate their current mood. Apparatus Psychophysiological measures were recorded on a Grass 7D polygraph, interfaced to an AT computer via an A-D converter. The dot probe task was administered via a PC computer, equipped with a second A-D converter. In order to synchronize the psychophysiological data with the dot probe task, the two A-D converters were interfaced so that reaction time data were paired with the appropriate SC, HR, and EMG values. Psychophysiological data were sampled at a rate of 10 samples/set and stored for later compilation. Procedure Following determination of suitability for inclusion, Ss provided informed consent and were assessed individually in a sound- and light-controlled laboratory. Upon arrival at the laboratory, psychophysiological sensors were placed by a trained assistant and a 10 min habituation interval occurred.
*This procedure represents a slight modification of that used by MacLeod ef al. (1986), where dot probes were presented 25 msec after word pair offset. Our modification permitted interpretation of the results in terms of a ‘true’ dual task procedure, given that Ss were asked to read the top word aloud and to indicate simultaneously whether or not a dot probe had been detected (see Procedure).
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Two test phases were included. Phase 1 involved a 3 min resting baseline, during which Ss sat quietly. At the end of Phase 1, Ss completed the POMS and then were informed that they would be presented with word pairs, arranged with one word above the other (Phase 2). They were told to read the top word aloud and informed that on some trials, a small dot would appear to the left of one of the words. Ss were instructed to press one of two keys as quickly as possible, to indicate whether or not a dot had been detected. Irrespective of the dot’s position, Ss were informed that their response time would be recorded by the computer. Following a short practice session, consisting of 50 filler word pairs, the procedure was completed. At the end of Phase 2, Ss completed the POMS and the verbal recognition task. Statistical
methods
Cognitive measures. Dot probe detection latency data were analyzed in two fashions. First, in order to compare the results with those of MacLeod et al. (1986), a Group (PD, NC) x stimulus type (physical, social, positive, household) x stimulus position (top, bottom) x probe position (top, bottom) MANOVA was conducted. Second, the two position variables were combined to yield one factor (e.g. Stimulus top/probe top = 1; stimulus top/probe bottom = 2, etc.) and separate Group (PD, NC) x stimulus-probe position MANOVAs were conducted for each Stimulus type. Bonferroni-type adjustment of the nominal x was employed to control experiment-wise error rate; thus, these tests were conducted at c1 = 0.0125, given the inclusion of four separate analyses. This second approach was selected to provide a closer examination ‘of attentional processes in anxiety via enhancement of statistical power. In each case, significant effects were followed with Tukey’s procedure. Data from the recognition task were scored and converted to d’ values, using signal detection methodology (Egan, 1975; Green & Swets, 1966)* and analyzed using a Group (PD, NC) x Stimulus type (physical, social, positive, household) MANOVA. Psychophysiological measures. Psychophysiological data were analyzed in two fashions. First, data from the initial baseline were compiled into I-min epochs. A Group (PD, NC) x Epoch (min. 1,2,3) MANOVA was conducted for SC, HR, and EMG. Significant effects were followed using univariate procedures and Tukey’s follow-up procedure, with comparison-specific error terms.? Second, data collected during the dot probe procedure were analyzed using a Group (PD, NC) x Stimulus type (physical, social, positive, household) x Epoch (ten 0.1 set samples) MANOVA. The use of 0.1 set epochs was selected to assess momentary reactions in SC, EMG, and HR to rapid presentation of threat stimuli. The first five 0.1 set samples occurred before word presentation, while the latter five samples were taken after presentation of stimulus word pairs. Significant effects were followed as above. Afictive measure. The POMS was scored according to protocol and subscale scores were converted into t scores. These values were submitted to a Group (PD, NC) x Time (initial baseline, dot probe task) MANOVA. Significant effects were followed using Tukey’s procedure, with comparison-specific error terms.
RESULTS Cognitive measures. Examination of the Group x Stimulus type by Stimulus position by Probe position MANOVA indicated a significant Group effect [F(6,3193) = 11.10, P < O.OOOl], which revealed that the PD sample was significantly slower in reaction times than the NC sample. When these data were examined by stimulus type with separate MANOVAs, significant effects were noted for Physical-panic stimuli [P(7,792) = 3.57, P < 0.0009] and Positive stimuli [F(7,792) = 3.15, P < 0.0031. For Physical-panic words, a significant Group effect was noted [F(1,792) = 21.99,
*For each stimulus cue, a ‘hit’ was scored when the S correctly indicated familiarity with the cue (a rating of 3 or 4). A ‘false alarm’ was scored when the S incorrectly indicated familiarity. These values were converted into probability scores and a value of d’ (a measure of observer sensitivity) was derived by determining the normalized ratio of these two probabilities, thus controlling for bias effects. Higher values of d’ indicate more accurate recognition memory. tThe use of comparison-specific error terms in conducting follow-up testing controls for inflation of the nominal G(that results from violation of the sphericity assumption in repeated measures designs (Rogan, Keselman & Mendoza, 1979; Vasey & Thayer, 1987).
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processing
P < O.OOOl], indicating that the PD sample showed significantly slower reaction times (3 = 1114.3 msec) relative to the NC sample (8 = 931.5 msec). Similarly, for Positive stimuli, a significant Group effect was noted [F(l,792) = 17.56, P < O.OOOOl] again indicating that the PD sample showed slower reaction times (2 = 1088.2 msec), relative to the NC sample (p = 937.2 msec). Additionally, a nonsignificant trend was noted for Social threat stimuli [F(7,792) = 3.15, P < 0.021. Examination of this trend revealed a Group effect [F(l,792) = 14.30, P -C0.0002] indicating that the PD sample again showed slower reaction time (2 = 1111.9 msec) relative to the NC sample (8 = 967.4 msec). No significant effects were noted for household (P < 0.07) stimuli. Examination of the d’ data indicated a significant effect for Stimulus type [1;(3,36) = 3.30, P(O.031, indicating greater recognition memory for Social threat stimuli, relative to the three other stimulus types. No group differences were noted in d’. Recognition memory was moderately good for both groups across stimulus types. Psychophysiological measures. Examination of the initial baseline data indicated no effects for EMG or HR. The SC data indicated a Group x Time effect [F(2,36) = 3.50, P < 0.051, which indicated that the PD sample showed significantly higher SC responding (J? = 3.83) during the final minute of the resting baseline, relative to the NC sample (8 = 2.99). During the dot probe procedure, SC and EMG did not reveal significant effects. For HR, a significant Time effect was noted [F(9,28) = 3.17, P < 0.0091 indicating that HR following presentation of word pairs (epochs &lo) decreased relative to HR prior to word presentation (epochs l-5, P -C 0.05). Aflectiue measure. Examination of the POMS data indicated significant effects on the tensionanxiety [F(3,71) = 9.03, P < O.OOOl] and the vigor-activity subscales [F(3,72) = 3.24, P < 0.031. Follow-up of these effects indicated that the PD sample reported significantly more tension-anxiety relative to the NC sample (P < 0.05) and that the dot probe procedure elevated tension for both samples (P < 0.05). On the vigor subscale, a significant Group effect was noted (P < 0.03), which indicated that the PD sample scored significantly lower than the NC sample throughout the procedure. POMS subscale scores are shown in Table 3 for both the PD and NC groups. DISCUSSION In this study, PD patients demonstrated slower reaction time to physical threat and positivevalenced verbal stimuli in a dual-task dot probe paradigm, relative to normal controls. A trend in the same direction emerged for the social threat stimuli, although the two samples showed equivalent reaction times to emotionally neutral stimuli. Unlike previous research using a similar paradigm (MacLeod et al., 1986), no position effects were noted in reaction time in either group, indicating that the relative positions of the dot probe and stimulus target did not influence the speed of encoding. Contrary to prediction, no differences between PD patients and normal controls emerged on a measure of stimulus recognition, regardless of word type. Attentional processing effects were not accompanied by increases in heart rate, skin conductance, or muscle tension, although presentation of verbal stimuli was accompanied by a slight but significant decrease in heart rate for both groups. Although the procedure evoked anxiety for both groups, the PD sample reported greater levels of anxiety throughout. In the present study, as in studies employing the modified Stroop color-naming paradigm (Ehlers et al., 1988; McNally et al., 1990), PD patients demonstrated selective interference in encoding threat-relevant verbal stimuli. Of particular interest is the finding that this interference also Table 3. POMS scores, by group (PD, NC) and assessment point CiNXlp PD
Tension-anxiety Depression-dejection Anger-hostility Vigor-activity Fatigue-inertia Confusion-bewilderment Row means sharing
common
NC
Baseline
Task
Baseline
Task
38.2’ 36.0” 38.3’ 52.1” 42.8’ 36.9’
39.2b 35.4’ 39.4” 52.1” 41.8” 39.1’
30.7’ 33.58 37.9” 60.0b 40.8” 35.4”
36.8d 34.5a 38.4” 61.2b 39.9” 37.1s
superscripts
are not statistically
different (P > 0.05)
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occurred with stimuli of equal, but positive emotional valence. Although previous studies with PD patients have not employed positive stimuli, our results suggest that the emotional significance, or salience, of stimuli which produce encoding interference in these patients is not mediated solely by the association of these words with anxiety. The lack of observed differences between the PD and control samples in responding to neutral stimuli suggests that the present results cannot be explained by slower reaction time responses or overall slower encoding processes in the PD sample. As evidenced by the affective ratings, the dot probe task used in the present study created significant increases in anxiety for both PD and NC samples. Possibly, this increase in anxiety in the PD patient sample affected encoding processes for all emotionally-valenced stimuli. If accurate, this interpretation suggests necessary modifications to existing cognitive theories of the anxiety disorders. In particular, PD may be maintained by hypervigilance in encoding emotionally-toned stimuli of all forms, rather than simply fear-relevant stimuli per se. Related studies with patients who meet criteria for other anxiety disorders have included positively-valenced words in the modified Stroop paradigm, with inconsistent results. For example, Martin, Williams and Clark (1988) reported that GAD patients demonstrated as much interference to positive stimuli as to threat words. However, McNally, Kaspi, Riemann and Zeitlin (1990) noted that Vietnam veterans with PTSD exhibited Stroop interference only to Vietnam-related words and not to positive affective words. This pattern of mixed results strongly suggests the need for inclusion of positive emotional stimuli in future investigations of information processing in the anxiety disorders. Despite the observed encoding interference in the PD sample, no between-group differences were noted on the cued recognition task, suggesting that semantic memory processes may not play a significant role in the maintenance of PD. As elucidated by Atkinson and Shiffrin (1968) recognition is a product of short-term memory storage, which can be influenced at the discretion of the S. Although a stronger test of semantic memory in PD patients would involve a free recall paradigm, which makes greater requirements on semantic memory, the present data suggest that selective memory processes may not constitute a key cognitive process which contributes to the maintenance of PD. It is important to note that those studies which have relied on free recall tasks have noted both enhanced (McNally et al., 1989; Nunn et al., 1984) and impaired (Mogg et al., 1987) recall of threat-relevant words, while the one study which used a cued recognition paradigm (Ehlers et al., 1988) failed to note differences between PD patients and controls. In light of this mixed pattern of results, it is difficult to ascribe a central role to short-term memory processes in the anxiety disorders. As discussed by Rapee (1991), it is possible that delayed retrieval tasks or implicit memory assessment strategies are better tests of the role of semantic memory in maintenance of the anxiety disorders. To interpret these results, it is important to highlight two key features of the dot probe paradigm which differ from previous research. First, unlike the paradigm employed by MacLeod et al. (1986) which presented dot probes 25 msec after word pair offset, the paradigm used in this investigation was a ‘true’ dual task procedure, given that probes were presented simultaneously with word pairs. Although this procedural modification appears slight, in this type of paradigm even a small delay between primary (e.g. threat-relevant words) and secondary (e.g. dot probe detection) tasks can influence reaction times (e.g. Posner & Boies, 1971; Johnson, Greenberg, Fisher & Martin, 1970). In order to assess attentional allocation as an index of cognitive processing, both primary and secondary tasks need to be presented simultaneously; under these circumstances, when interference on the secondary task occurs in the presence of threat-relevant stimuli on the primary task, attentional bias is inferred. With this procedural modification, no relative position effects were noted in reaction time for either sample, suggesting that the attentional interference noted in the PD sample on physical-panic threat and positive stimuli reflects a global attentional process. A second difference between the current paradigm and past research involves the response procedure utilized. In this study, Ss were required to respond via key pressing to indicate both the presence and absence of detection probes, unlike the procedure used by MacLeod et al. (1986), where Ss responded only when a dot probe was perceived. This modification ensured equal task requirements across conditions and reduced the possibility of a motor response bias as an explanation for reaction time differences. No between-group differences in physiological arousal (heart rate, skin conductance, and muscle tension) accompanied attentional interference effects. Rather, a small but significant heart rate
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decrease occurred following presentation of word pairs. This pattern is consistent with observations derived from Lacey’s ‘intake-rejection’ hypothesis. Specifically, Lacey (1959) and Lacey, Kagan, Lacy and Moss (1963) have demonstrated that heart rate deceleration occurs during perceptual functions (e.g. attention to visual stimuli), presumably to facilitate intake of environmental stimuli. In contrast, higher cognitive activities (e.g. mental arithmetic) are accompanied by heart rate acceleration, presumably to ‘reject’ unrelated stimuli which could disrupt cognitive performance. Although Lacey’s theory concerning the neurophysiological bases for these effects has been criticized (Elliott, 1972; Hahn, 1973), the observation of heart rate deceleration during perceptual tasks is robust across a variety of paradigms and supports conceptualization of the dot probe task as a measure of perceptual attention. The absence of between-group differences suggests that attentional hypervigilance in PD patients is not accompanied by increases in autonomic and somatic arousal. Based on these data, it would appear that an additional mediating process is required to account for the role of cognitive processes in initiating panic attacks. In particular, a model is needed to explain how stimulus encoding triggers the surges in physiological arousal which occur during panic attacks. A feature of the present study which deserves comment is the relative lack of group differences in resting levels of physiological arousal. With the exception of skin conductance, the PD patients and control Ss did not differ in resting arousal and in fact, the differences noted on skin conductance occurred only at one timepoint during the 3 min resting baseline. Other investigators have reported that PD patients show tonic elevation in autonomic arousal (cf. Barlow, 1988). Our failure to observe this phenomenon may have resulted from several procedural controls. First, the assessment protocol and instrumentation were explained thoroughly to each S prior to beginning the procedure, in order to reduce intergroup variation in psychophysiological response. Farha and Sher (1989) have demonstrated that informing Ss completely about experimental procedures prior to beginning psychophysiological measurement can significantly affect tonic arousal. Additionally, the use of a 10 min laboratory habituation interval could have served an important function, as shorter habituation intervals do not control fully for adaptation to the laboratory and the orienting reflex (Sallis & Lichstein, 1979). It is notable that Clark, Taylor, Hayward, King, Margraf, Ehlers, Roth and Agras (1990) also failed to observe higher levels of tonic heart rate in PD patients relative to controls using ambulatory monitoring, suggesting that previous reports may have been influenced by laboratory procedures. As noted in the description of Ss, the PD patients in this study obtained IQ scores which were slightly, but significantly lower than that obtained by the control Ss. In considering whether these IQ differences could account for the cognitive-attentional differences noted between PD patients and controls, it is notable that attentional interference effects were specific to emotionallysalient stimuli. Presumably, if reaction time differences on the dot probe task were attributable to IQ, the PD sample would have shown slower responding to neutral words as well as physical-panic threat, positive, and social threat terms. In light of the specificity of attentional interference, as well as the fact that the dot probe task appears to assess perceptual processes, rather than higher cognitive processes, the observed IQ differences between the PD and control samples do not appear relevant in interpreting these results. Additionally, the lack of group differences in semantic memory further suggests that IQ differences, while statistically different, did not influence these data. In sum, these data support the role of attentional processes in the maintenance of PD, although semantic memory appeared relatively unimportant in the context of these findings. Of particular note is the finding that PD patients demonstrate selective encoding effects with both threat-relevant stimuli and positive-valenced stimuli. This finding suggests that attentional vigilance in PD is not specific to anxiety-relevant cues, but rather, may reflect a more generalized process of encoding emotionally-toned stimuli. These effects were not accompanied by increases in physiological responding in the PD sample, suggesting that elaboration of existing theoretical models is necessary to account for the role of cognitive processes in initiating panic attacks. Clearly, future research would benefit by the inclusion of alternative strategies for assessment of semantic memory, given the inconsistent pattern of results obtained in studies to date. In many respects, the usefulness of information processing paradigms for refining available cognitive models of the anxiety disorders appears clear and necessary.
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Acknowledgements -This research was supported in part by grants from the Higher Education Coordinating Boards (Nos 0116181-061 and 003652-I 18), awarded to the first and second authors. We gratefully acknowledge the help of A. Marie Barron for assisting with structured interviews and Tom Chase and Joy Breckenridge for help with data collection.
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J., Riemann, B. C. & Kim, E. (1990). Selective processing of threat cues in panic disorder. Behaviour Research and Therapy, 5, 407-412. McNallv, R. J.. Kaspi, S. P., Riemann, B. C. & Zeitlin, S. B. (1990). Selective processing of threat cues in post-traumatic stress disorder. journal of Abnormal Psychology, 99, 398-402. Mevers. J. K.. Weissman. M. M.. Tischler, C. E., Holzer. C. E. III, Orvaschel. H., Anthony, J. C., Boyd, J. H., Burke, J, D. Jr, Kramer, M. & Stoltzman, R. (1984). Six-month prevalence of psychiatric disorders in three communities. Archives of General Psychiatry, 41, 959-967.
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Mogg, K., Mathews, A. S. & Weinman, J. (1987). Memory bias in clinical anxiety. Journal of Abnormal Psychology, 96, 94-98. Navon, D. & Margalit, B. (1983). Allocation of attention according to informativeness in visual recognition. Quarterly Journal of Experimental Psychology, 35, 497-512. Nunn, J. D., Stevenson, R. J. & Whalan, G. (1984). Selective memory effects in agoraphobic patients. British Journal of Clinical Psychology, 23, 195-20 1. Posner, M. 1. & Boies, S. J. (1971). Components of attention. Psychological Reoiew, 78, 391-408. Rapee, R. M. (1991). Generalized Anxiety Disorder: A review of clinical features and theoretical concepts. Clinical Psychology Review, II, 419-440. Reiss, S., Peterson, R. A., Gursky, D. M. & McNally, R. J. (1986). Anxiety sensitivity, anxiety frequency, and the prediction of fearfulness. Behaviour Research and Therapy, 24, 1-8. Rogan, J. C., Keselman, H. J. & Mendoza, J. L. (1979). Analysis of repeated measurements. British Journal ofMathematics and Statistics in Psychology, 32, 269-286. Sallis, J. F. & Lichstein, K. L. (1979). The frontal electromyographic adaptation response: A potential source of confounding. Biofeedback and Self-Regulation, 4, 337-339. Spielberger, C. D., Gorsuch, R. L. & Lushene, R. E. (1970). Manualfor the State-Trait Anxiefy Invenfory, Palo Alto, Calif.: Consulting Psychologists Press. Taylor, C. B., Sheikh, J., Agras, W. S., Roth, W. T., Margraf, J., Ehlers, A., Maddock, R. J. & Gossard, D. (1986). Ambulatory heart rate changes in patients with panic attacks. American Journal of Psychiatry, 143, 478-482. Vasey, M. W. & Thayer, J. F. (1987). The continuing problem of false positives in repeated measures ANOVA in psychophysiology: A multivariate solution. Psychophysiology, 24, 479-486. Zachary, R. A. (1986). Shipley institute of living scale: Revised manual. Los Angeles, Calif.: Western Psychological Services.
1992 Copyright
0005.7967/92 $5.00 + 0.00 Q 1992 Pergamon Press Ltd
ATTENTION AND MEMORY FOR THREAT IN PANIC DISORDER J. GAYLE BECK,‘* MELINDA A. STANLEY,’ PATRICIA M. AVERILL,’ LAURIE E. BALDWIN’ and EDWIN A. DEACLE III’ ‘University of Houston, 4800 Calhoun Street, Houston, TX 77204-5341 and *University of Texas Medical School, 1300 Moursund Street, Houston, TX 77030-3497, U.S.A. (Received 22 November 1991)
Summary-Recently, information processing paradigms have been utilized to explore the role of attentional and memory processes in the maintenance of clinical anxiety disorders. The present study extended these data using a dual-task paradigm to assess attentional vigilance and a cued recognition task to evaluate short-term memory effects in Panic Disorder (PD). Twenty PD patients and 20 normal controls completed a computerized task wherein they read aloud one of a pair of rapidly presented words (primary task) while simultaneously attempting to detect a small probe that appeared adjacent to one of the words (secondary task). Eighty stimulus words were chosen to represent four categories: physical panic-related threat, social threat, positive-emotional, and neutral. Reaction time and accuracy in detecting the probe were assessed, as well as psychophysiological responding (heart rate, skin conductance, EMG). Following task completion, a cued recognition task was administered to examine short-term memory of task stimuli. Results indicated that PD patients exhibited slower reaction times relative to normal controls during presentation of physical panic-related threat and positive-emotional stimuli. A similar trend emerged for social threat stimuli, although the PD and control samples responded similarly to neutral stimuli. No group differences were found on the cued recognition measure or psychophysiological responding during task performance. The data are discussed in terms of possible implications for cognitive models of PD.
Cognitive theories have been proposed to account for the origin and maintenance of fears in the anxiety disorders (e.g. Barlow, 1988; Beck, Emery & Greenwald, 1985; Lang, 1979). These models postulate that anxiety and specific fears arise from overactivity of the cognitive processes involved in detecting threat and personal danger. Each of these models proposes that anxiety disorders are maintained by the manner in which fear-relevant information is perceived, encoded, and recalled. For example, Beck et al. (1985) and Lang (1979) have postulated that patients with Panic Disorder (PD) are hypervigilant to information associated with feared stimuli, such as the sensations of increased heart rate, rapid respiration, and sweating. This extreme sensitivity theoretically arises from greater ease or automaticity in activating fear-relevant imagery (Lang, 1979) or related cognitive processes involving encoding and memory (Beck et al., 1985). Proponents of this approach have traditionally utilized self-report methods to support these models (e.g. Beck, Laude & Bohnert, 1974; Hibbert, 1984). For example, Hibbert (1984) noted that PD patients report worry about bodily harm when anxious, while patients with Generalized Anxiety Disorder (GAD) report worry about personal inadequacy. Although such data provide indirect support for cognitive models of the anxiety disorders, this method captures only those aspects of cognition which can be verbalized. More recent research has used information processing paradigms derived from experimental cognitive psychology to examine directly the influence of cognitive processing factors in the maintenance of anxiety and panic. To date, studies utilizing these paradigms have examined attentional allocation, memory processes, and the interpretation of ambiguous verbal stimuli in a variety of anxiety syndromes, including obsessive-compulsive disorder (e.g. Foa & McNally, 1986), post-traumatic stress disorder (e.g. Foa, Feske, Murdock, Kozak & McCarthy, 1991) GAD (e.g. Mathews & MacLeod, 1985), phobic disorders (e.g. Burgess, Jones, Robertson, Radcliffe & Emerson, 1981) and PD (e.g. Ehlers, Margraf, Davies & Roth, 1988). In general, two distinct types of paradigms have been used in these studies. First, encoding processes have been examined, with particular focus on the role of perceptual or sensory aspects of the stimulus and attentional vigilance. Second, semantic processes, in particular memory recall *Author for correspondence. 619
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and recognition of threat-related stimuli, have been measured. These paradigms assess different levels of cognitive processing and reflect the distinction between encoding, which is conceptualized as an index of processing capacity, and recall/recognition, which is determined by semantic memory and presumably guides the selection of stimuli for long-term encoding (e.g. Atkinson & Shiffrin, 1968). With reference to the anxiety disorders, this distinction implies that overactivity of semantic memory for threat information could effect the speed of perceiving stimuli involving harm, as well as enhancing recall or recognition of these cues. However, data derived from GAD patients have not been supportive of this hypothesis. For example, Mogg, Mathews and Weinman (1987) reported slightly poorer recall and recognition for threat information in GAD patients, relative to controls, suggesting that an inhibitory process interferes with memory storage of threatening information in anxious patients. This ‘cognitive avoidance’ process potentially could serve to maintain anxiety disorders, by preventing habituation or accurate evaluation of incoming stimuli. Thus, the distinction between encoding and memory becomes central in considering information processing models of anxiety. Of the identified anxiety disorders, PD with and without agoraphobia is the most prevalent, both in the community at large (Meyers, Weissman, Tischler, Holzer, Orvaschel, Anthony, Boyd, Burke, Kramer & Stoltzman, 1984) and in treatment clinics (Barlow, 1988). PD is characterized by an enduring fear of the physical sensations that occur during panic attacks (DSM-III-R, American Psychiatric Association, 1987). By definition, these fears involve beliefs that anxiety sensations are signs of serious underlying physical and/or psychological problems, such as a heart attack or serious mental illness (e.g. Clark, 1986; Goldstein & Chambless, 1978). Research is beginning to examine the role of information processing factors in PD. For example, Ehlers et al. (1988) addressed both attentional and memory processes in PD, using a modified Stroop color naming task involving flashcards containing threat words related to physical harm, separation, and social humiliation. In this study, slower reaction times for color naming threat words were noted in both PD patients and nonclinical panickers, relative to controls. However, no between-group differences were found for cued recognition of stimulus words after the task. Thus, these data suggest that interference in encoding, but not memory is salient in PD. Other studies have demonstrated similar Stroop interference effects for threat words in PD, relative to controls (McNally, Riemann & Kim, 1990) but data from memory paradigms have been inconsistent with the Ehlers et al. (1988) data. For example, at least two studies have demonstrated that PD patients (with and without agoraphobia) show enhanced free recall for threat-relevant stimuli (McNally, Foa & Donnell, 1989; Nunn, Stevenson & Whalan, 1984). Thus, saliency in short-term memory may operate to maintain PD, although the interaction between encoding and memory processes is uncertain. Further clarification of the role of encoding processes in PD may occur by utilizing alternative cognitive paradigms to document shifts in attentional allocation between threat and neutral stimuli. In particular, paradigms which simultaneously present two tasks, a primary threat-relevant task and a secondary neutral task, allow determination of the allocation of attention to each type of incoming stimulus (e.g. Posner & Boies, 1971; Navon & Margalit, 1983). If greater interference occurs on the secondary task only in the presence of threat stimuli on the primary task, attentional hypervigilence to threat cues is implicated. MacLeod, Mathews and Tata (1986) reported the use of such a task with GAD patients. In this study, the primary task involved rapid presentation of word pairs, some of which included threat-relevant words (e.g. criticized, injury). The secondary task required detection of a visual probe, in the form of a small dot which appeared in the spatial location of either word immediately after the word display terminated. Ss were required to read one word aloud and subsequently press a hand-held button if a visual probe was detected. The distribution of visual attention was assessed via probe detection latency, which has been shown to be a sensitive measure of visual attention allocation (Navon & Margalit, 1983). Results indicated that GAD patients shifted attention toward threat words, resulting in slower detection latencies of probes appearing in the vicinity of these stimuli (MacLeod et al., 1986). In the present study, a similar paradigm was employed to assess attentional allocation between threat and neutral stimuli. Stimuli were selected to represent four categories: physical panic-related threat words, social threat words, positive-valenced emotional words, and neutral words. Presumably, those stimuli which reflect physical threat would create significant attentional interference for PD patients, given current accounts of the nature of fear in PD. Social threat stimuli were expected
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to result in little to moderate interference, given that PD patients sometimes report secondary fears of doing something embarrassing while having a panic attack in public. Positive stimuli were included as a control for response biases resulting from presentation of emotionally-valenced words. In addition to attentional allocation, the present investigation assessed semantic memory via a cued recognition task presented immediately following the dot probe procedure. This task was modeled after that used by Ehlers et al. (1988) and required Ss to provide estimates of whether each of the series of word cues had been included in the preceding task. In addition, three measures of physiological responding were assessed: heart rate, skin conductance, and upper trapezious EMG. In previous research involving simultaneous assessment of physiological arousal during information processing, results are mixed and suggest that the activation of cognitive fear processes may not be accompanied by increases in autonomic and somatic arousal (Ehlers et al., 1988; McNally et af., 1989). If accurate, this finding implies that an intervening process is required to explain how the activation of fear-relevant cognitive processes instigates surges of physiological arousal that are the hallmark of panic attacks (e.g. Taylor, Sheikh, Agras, Roth, Margraf, Ehlers, Maddock & Gossard, 1986; Freedman, Ianni, Ettudgui & Puthezhath, 1985). Thus, the present study was undertaken to examine allocation of attention and cued recognition of threat-relevant stimuli in PD patients. Twenty PD patients and 20 normal controls, matched by ethnicity, gender, and age, were selected and screened using a semi-structured interview and questionnaire. The hypotheses under examination including the following: (1) PD patients, but not controls, would shift attention toward emotionally-threatening stimuli (physical threat, social threat), resulting in slower latencies in detection of the visual probe on these trials, relative to detection latencies for neutral and positively-valenced stimuli. These effects were expected to be most pronounced when the visual probe appeared in the vicinity of the threat stimulus; (2) PD patients would show enhanced recognition for threat-relevant words, relative to controls, although group differences in short-term memory were not hypothesized for neutral or positively-valenced stimuli; and (3) Activation of these cognitive fear processes would be accompanied by increases in heart rate, skin conductance, and muscle tension, as well as increased reports of anxious mood in the PD sample alone.
METHOD
Subjects Fifty-nine patients with a primary diagnosis of PD (PD sample) were recruited via media announcements and screened initially by phone. If panic appeared to be a primary problem, the Anxiety Disorders Interview Schedule-Revised (DiNardo, Barlow, Cerny, Vermilyea, Vermilyea, Himadi & Waddell, 1985) was administered. All patients with severe agoraphobia were excluded, based on requirements of a subsequent treatment protocol. Diagnostic reliability was established by a second clinician for 17 cases (28.8% of the entire patient sample). 100% diagnostic agreement was noted, most likely due to extensive prescreening of potential Ss. All patients reported being medication-free and were not enrolled in psychotherapy at the time of evaluation. A subset of 20 PD patients was selected randomly for this investigation. This sample included 16 females and 4 males, with a mean age of 38.3 (SD 11.76). The average duration of panic was 4.4 yr with 95% reporting mild (n = 14) or moderate (n = 5) agoraphobia. Clinical severity of PD, based on the degree of impairment and distress was rated on an 8-point Likert scale. Average severity was 3.9 (SD 1.32, range 2-7). The control sample (NC sample) included 20 normals, matched by ethnicity, gender, and age with the PD sample (average age = 36.8; SD = 12.74). All control Ss were screened for psychiatric disorders via the ADIS-R and none reported ever having experienced a panic attack. Control Ss received payment for participation and were recruited from local civic organizations, friendship networks, and the undergraduate population of the University of Houston.
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Table I. Questionnaire
State-Trait Anxiety Inventory State anxiety score Trait anxiety score Beck Depression Inventory Shipley Institute of Living Scale Fear Questionnaire Agoraphobia subscale Blood/injury subscale Social subscale Total Anxiety Sensitivity Inventory
scores for PD and NC samples
45.85 41.75 9.85 100.4
30. IO 32.35 3.85 109.7
16.92 4.10 8.43 3.30
0.0001 0.05 0.006 0.002
10.95 13.47 13.68 38.1 I 33.95
2.25 5.20 5.25 12.70 9.65
16.21 16.59 16.61 30.36 54.02
0.0001 0.0001 0.0001 0.0001 0.0001
All Ss completed the Spielberger State-Trait Anxiety Inventory (STAI; Spielberger, Gorsuch & Lushene, 1970), the Beck Depression Inventory (BDI: Beck, Ward, Mendelsohn, Mock & Erbaugh, 1961), Shipley Institute of Living Scale (SH; Zachary, 1986), the Fear Questionnaire (FQ; Marks & Mathews, 1979), and the Anxiety Sensitivity Inventory (ASI; Reiss, Peterson, Gursky & McNally, 1986). Mean scores are provided in Table 1. As expected, the PD sample exhibited higher levels of state and trait anxiety, depression, anxiety sensitivity, and specific fears on the FQ. Both samples scored within the normal range of IQ on the SH, although a statistically significant difference was noted, with the PD sample scoring slightly lower than the NC sample. Materials
Eighty stimulus words were drawn from previous research by Mathews and colleagues (Mathews, pers. comm., May 1989) and modified for the current study. Twenty of these words were related to physical panic-related threat (e.g. collapse) and 20 to social threat (e.g. humiliated). Additionally, 20 words were positive-valenced emotional words (e.g. confident), and 20 pertained to household activities (e.g. furnished). Physical threat, social threat, and positive stimulus words were matched by independent raters for level of emotionality. Stimulus words are listed in Table 2. Each stimulus word was paired with a neutral word matched for both length and usage frequency to make 80 critical word pairs. Another 250 neutral word pairs matched for word length were generated randomly, to serve as filler items. Word pairs were presented using an IBM-PC microcomputer and a 12-in VGA monitor. Relying on a Scientific Solutions A-D processor and LabPac software, each word pair was presented for 500 msec duration, with words separated on the vertical axis by a distance of 3 cm. Each stimulus word could appear with equal probability in either the top or bottom position. Dot probes occurred on 50% of the total trials, including 100% of the stimulus trials. Dot probes were presented simultaneously with the word pairs and were positioned to the left of either the top or bottom Table 2. Stimulus
words used in the dot probe procedure
Physicalpanic
Social
Positive
Household (neutral)
Collapse Tremble Disease Emergency Attack Illness Tumor Cancer Coronary Ambulance. Paralysis Fatal Tingling Pain Suffocated Death Faint Choking Sweat Dizzv
Persecuted Offended Inept Worthless Hated US&SS Humiliated Indecisive Inferior Hostile Unsuccessful Slle.X Neglected Stupid Hopeless Ridicule Foolish Lonely Unfriendly Snub
Devoted Applause Helpful Superb Achievement Excellent Charm Terrific Delight Comfort Merry Serene Romance Miracle Sensual Confident Enthusiasm Celebration Praise Generous
Lounge Bleach Cushion Domestic Furnished Groceries Ornament Shower Staircase Lamp Mantlepiece Shelves Vase BKXm Towel Switch Wardrobe Chimney Shampoo Upstairs
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words.* The dot probe could appear with equal probability in either position. On each trial, a 1 set intertrial interval followed offset of the word pair. The program recorded reaction time to 1 msec accuracy. Given the design of this study, only the data from the 80 stimulus word pairs are of interest. Thus, two factors were independently varied on stimulus trials: the position of the stimulus word (top/bottom) and the position of the dot probe (top/bottom). The combination of these two factors produced four possible orders. For each S, 20 of the 80 stimulus trials appeared in each order. Specific word pairs were balanced to match order of presentation between groups. Measures Cognitive measures. Two information-processing measures were included: (1) reaction time, measured in milliseconds, collected during the dot probe task, and (2) recognition memory, taken after the completion of the task. For the latter, Ss were administered a 60-item word list and instructed to rate each on a l-4 scale (1 = word was definitely not included in the task; 4 = word was definitely included in the task). Of the 60 items, 20 were derived from the task and 40 were novel filler items. Word order was randomized. Psychophysiological measures. Skin conductance (SC), heart rate (HR), and upper trapezious EMG were measured for each S. SC was assessed from the medial phalanx of the first two fingers of the left hand, using Beckman Ag-AgCl electrodes and a Grass 7Pl preamplifier. The skin surface was cleansed with soap and water immediately prior to sensor attachment, to control for intersubject variation. SC was transformed from mms pen deflection to micromhos conductance based on pre-session calibration (constant voltage of 0.5 V). HR was measured with two Ag-AgCl electrodes placed bilaterally on the chest 5 cm below the midpoint of each clavicle, using a Grass 7P3 preamplifier. HR was converted from a raw EKG signal to a beats-per-minute expression using a Grass 7P44B tachograph. EMG was assessed using three Ag-AgCl electrodes placed in a standard triangular configuration on the upper trapezious muscle, halfway between the C7 vertebrae and the angle of the acromion. A Grass 7P3 preamplifier was used, with a low frequency amplifier setting of 0.3 Hz and a high frequency amplifier setting of 35 Hz. The raw EMG signal was integrated with a time constant of 0.2 sec. The skin surface was cleansed with mildly abrasive soap, to reduce resistance below 10,000 Q. K-Y jelly was used as the conducting medium for all Ag-AgCl electrodes. Afictive measures. Ss completed the Profile of Mood States (POMS; McNair, Lorr & Droppleman, 1971). The POMS is an adjective rating scale which includes six subscales: tension-anxiety, depression-dejection, anger-hostility, vigor-activity, fatigue-inertia, and confusionbewilderment. Ss were instructed to rate each of 65 adjectives on a 5-point Likert scale to indicate their current mood. Apparatus Psychophysiological measures were recorded on a Grass 7D polygraph, interfaced to an AT computer via an A-D converter. The dot probe task was administered via a PC computer, equipped with a second A-D converter. In order to synchronize the psychophysiological data with the dot probe task, the two A-D converters were interfaced so that reaction time data were paired with the appropriate SC, HR, and EMG values. Psychophysiological data were sampled at a rate of 10 samples/set and stored for later compilation. Procedure Following determination of suitability for inclusion, Ss provided informed consent and were assessed individually in a sound- and light-controlled laboratory. Upon arrival at the laboratory, psychophysiological sensors were placed by a trained assistant and a 10 min habituation interval occurred.
*This procedure represents a slight modification of that used by MacLeod ef al. (1986), where dot probes were presented 25 msec after word pair offset. Our modification permitted interpretation of the results in terms of a ‘true’ dual task procedure, given that Ss were asked to read the top word aloud and to indicate simultaneously whether or not a dot probe had been detected (see Procedure).
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Two test phases were included. Phase 1 involved a 3 min resting baseline, during which Ss sat quietly. At the end of Phase 1, Ss completed the POMS and then were informed that they would be presented with word pairs, arranged with one word above the other (Phase 2). They were told to read the top word aloud and informed that on some trials, a small dot would appear to the left of one of the words. Ss were instructed to press one of two keys as quickly as possible, to indicate whether or not a dot had been detected. Irrespective of the dot’s position, Ss were informed that their response time would be recorded by the computer. Following a short practice session, consisting of 50 filler word pairs, the procedure was completed. At the end of Phase 2, Ss completed the POMS and the verbal recognition task. Statistical
methods
Cognitive measures. Dot probe detection latency data were analyzed in two fashions. First, in order to compare the results with those of MacLeod et al. (1986), a Group (PD, NC) x stimulus type (physical, social, positive, household) x stimulus position (top, bottom) x probe position (top, bottom) MANOVA was conducted. Second, the two position variables were combined to yield one factor (e.g. Stimulus top/probe top = 1; stimulus top/probe bottom = 2, etc.) and separate Group (PD, NC) x stimulus-probe position MANOVAs were conducted for each Stimulus type. Bonferroni-type adjustment of the nominal x was employed to control experiment-wise error rate; thus, these tests were conducted at c1 = 0.0125, given the inclusion of four separate analyses. This second approach was selected to provide a closer examination ‘of attentional processes in anxiety via enhancement of statistical power. In each case, significant effects were followed with Tukey’s procedure. Data from the recognition task were scored and converted to d’ values, using signal detection methodology (Egan, 1975; Green & Swets, 1966)* and analyzed using a Group (PD, NC) x Stimulus type (physical, social, positive, household) MANOVA. Psychophysiological measures. Psychophysiological data were analyzed in two fashions. First, data from the initial baseline were compiled into I-min epochs. A Group (PD, NC) x Epoch (min. 1,2,3) MANOVA was conducted for SC, HR, and EMG. Significant effects were followed using univariate procedures and Tukey’s follow-up procedure, with comparison-specific error terms.? Second, data collected during the dot probe procedure were analyzed using a Group (PD, NC) x Stimulus type (physical, social, positive, household) x Epoch (ten 0.1 set samples) MANOVA. The use of 0.1 set epochs was selected to assess momentary reactions in SC, EMG, and HR to rapid presentation of threat stimuli. The first five 0.1 set samples occurred before word presentation, while the latter five samples were taken after presentation of stimulus word pairs. Significant effects were followed as above. Afictive measure. The POMS was scored according to protocol and subscale scores were converted into t scores. These values were submitted to a Group (PD, NC) x Time (initial baseline, dot probe task) MANOVA. Significant effects were followed using Tukey’s procedure, with comparison-specific error terms.
RESULTS Cognitive measures. Examination of the Group x Stimulus type by Stimulus position by Probe position MANOVA indicated a significant Group effect [F(6,3193) = 11.10, P < O.OOOl], which revealed that the PD sample was significantly slower in reaction times than the NC sample. When these data were examined by stimulus type with separate MANOVAs, significant effects were noted for Physical-panic stimuli [P(7,792) = 3.57, P < 0.0009] and Positive stimuli [F(7,792) = 3.15, P < 0.0031. For Physical-panic words, a significant Group effect was noted [F(1,792) = 21.99,
*For each stimulus cue, a ‘hit’ was scored when the S correctly indicated familiarity with the cue (a rating of 3 or 4). A ‘false alarm’ was scored when the S incorrectly indicated familiarity. These values were converted into probability scores and a value of d’ (a measure of observer sensitivity) was derived by determining the normalized ratio of these two probabilities, thus controlling for bias effects. Higher values of d’ indicate more accurate recognition memory. tThe use of comparison-specific error terms in conducting follow-up testing controls for inflation of the nominal G(that results from violation of the sphericity assumption in repeated measures designs (Rogan, Keselman & Mendoza, 1979; Vasey & Thayer, 1987).
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processing
P < O.OOOl], indicating that the PD sample showed significantly slower reaction times (3 = 1114.3 msec) relative to the NC sample (8 = 931.5 msec). Similarly, for Positive stimuli, a significant Group effect was noted [F(l,792) = 17.56, P < O.OOOOl] again indicating that the PD sample showed slower reaction times (2 = 1088.2 msec), relative to the NC sample (p = 937.2 msec). Additionally, a nonsignificant trend was noted for Social threat stimuli [F(7,792) = 3.15, P < 0.021. Examination of this trend revealed a Group effect [F(l,792) = 14.30, P -C0.0002] indicating that the PD sample again showed slower reaction time (2 = 1111.9 msec) relative to the NC sample (8 = 967.4 msec). No significant effects were noted for household (P < 0.07) stimuli. Examination of the d’ data indicated a significant effect for Stimulus type [1;(3,36) = 3.30, P(O.031, indicating greater recognition memory for Social threat stimuli, relative to the three other stimulus types. No group differences were noted in d’. Recognition memory was moderately good for both groups across stimulus types. Psychophysiological measures. Examination of the initial baseline data indicated no effects for EMG or HR. The SC data indicated a Group x Time effect [F(2,36) = 3.50, P < 0.051, which indicated that the PD sample showed significantly higher SC responding (J? = 3.83) during the final minute of the resting baseline, relative to the NC sample (8 = 2.99). During the dot probe procedure, SC and EMG did not reveal significant effects. For HR, a significant Time effect was noted [F(9,28) = 3.17, P < 0.0091 indicating that HR following presentation of word pairs (epochs &lo) decreased relative to HR prior to word presentation (epochs l-5, P -C 0.05). Aflectiue measure. Examination of the POMS data indicated significant effects on the tensionanxiety [F(3,71) = 9.03, P < O.OOOl] and the vigor-activity subscales [F(3,72) = 3.24, P < 0.031. Follow-up of these effects indicated that the PD sample reported significantly more tension-anxiety relative to the NC sample (P < 0.05) and that the dot probe procedure elevated tension for both samples (P < 0.05). On the vigor subscale, a significant Group effect was noted (P < 0.03), which indicated that the PD sample scored significantly lower than the NC sample throughout the procedure. POMS subscale scores are shown in Table 3 for both the PD and NC groups. DISCUSSION In this study, PD patients demonstrated slower reaction time to physical threat and positivevalenced verbal stimuli in a dual-task dot probe paradigm, relative to normal controls. A trend in the same direction emerged for the social threat stimuli, although the two samples showed equivalent reaction times to emotionally neutral stimuli. Unlike previous research using a similar paradigm (MacLeod et al., 1986), no position effects were noted in reaction time in either group, indicating that the relative positions of the dot probe and stimulus target did not influence the speed of encoding. Contrary to prediction, no differences between PD patients and normal controls emerged on a measure of stimulus recognition, regardless of word type. Attentional processing effects were not accompanied by increases in heart rate, skin conductance, or muscle tension, although presentation of verbal stimuli was accompanied by a slight but significant decrease in heart rate for both groups. Although the procedure evoked anxiety for both groups, the PD sample reported greater levels of anxiety throughout. In the present study, as in studies employing the modified Stroop color-naming paradigm (Ehlers et al., 1988; McNally et al., 1990), PD patients demonstrated selective interference in encoding threat-relevant verbal stimuli. Of particular interest is the finding that this interference also Table 3. POMS scores, by group (PD, NC) and assessment point CiNXlp PD
Tension-anxiety Depression-dejection Anger-hostility Vigor-activity Fatigue-inertia Confusion-bewilderment Row means sharing
common
NC
Baseline
Task
Baseline
Task
38.2’ 36.0” 38.3’ 52.1” 42.8’ 36.9’
39.2b 35.4’ 39.4” 52.1” 41.8” 39.1’
30.7’ 33.58 37.9” 60.0b 40.8” 35.4”
36.8d 34.5a 38.4” 61.2b 39.9” 37.1s
superscripts
are not statistically
different (P > 0.05)
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occurred with stimuli of equal, but positive emotional valence. Although previous studies with PD patients have not employed positive stimuli, our results suggest that the emotional significance, or salience, of stimuli which produce encoding interference in these patients is not mediated solely by the association of these words with anxiety. The lack of observed differences between the PD and control samples in responding to neutral stimuli suggests that the present results cannot be explained by slower reaction time responses or overall slower encoding processes in the PD sample. As evidenced by the affective ratings, the dot probe task used in the present study created significant increases in anxiety for both PD and NC samples. Possibly, this increase in anxiety in the PD patient sample affected encoding processes for all emotionally-valenced stimuli. If accurate, this interpretation suggests necessary modifications to existing cognitive theories of the anxiety disorders. In particular, PD may be maintained by hypervigilance in encoding emotionally-toned stimuli of all forms, rather than simply fear-relevant stimuli per se. Related studies with patients who meet criteria for other anxiety disorders have included positively-valenced words in the modified Stroop paradigm, with inconsistent results. For example, Martin, Williams and Clark (1988) reported that GAD patients demonstrated as much interference to positive stimuli as to threat words. However, McNally, Kaspi, Riemann and Zeitlin (1990) noted that Vietnam veterans with PTSD exhibited Stroop interference only to Vietnam-related words and not to positive affective words. This pattern of mixed results strongly suggests the need for inclusion of positive emotional stimuli in future investigations of information processing in the anxiety disorders. Despite the observed encoding interference in the PD sample, no between-group differences were noted on the cued recognition task, suggesting that semantic memory processes may not play a significant role in the maintenance of PD. As elucidated by Atkinson and Shiffrin (1968) recognition is a product of short-term memory storage, which can be influenced at the discretion of the S. Although a stronger test of semantic memory in PD patients would involve a free recall paradigm, which makes greater requirements on semantic memory, the present data suggest that selective memory processes may not constitute a key cognitive process which contributes to the maintenance of PD. It is important to note that those studies which have relied on free recall tasks have noted both enhanced (McNally et al., 1989; Nunn et al., 1984) and impaired (Mogg et al., 1987) recall of threat-relevant words, while the one study which used a cued recognition paradigm (Ehlers et al., 1988) failed to note differences between PD patients and controls. In light of this mixed pattern of results, it is difficult to ascribe a central role to short-term memory processes in the anxiety disorders. As discussed by Rapee (1991), it is possible that delayed retrieval tasks or implicit memory assessment strategies are better tests of the role of semantic memory in maintenance of the anxiety disorders. To interpret these results, it is important to highlight two key features of the dot probe paradigm which differ from previous research. First, unlike the paradigm employed by MacLeod et al. (1986) which presented dot probes 25 msec after word pair offset, the paradigm used in this investigation was a ‘true’ dual task procedure, given that probes were presented simultaneously with word pairs. Although this procedural modification appears slight, in this type of paradigm even a small delay between primary (e.g. threat-relevant words) and secondary (e.g. dot probe detection) tasks can influence reaction times (e.g. Posner & Boies, 1971; Johnson, Greenberg, Fisher & Martin, 1970). In order to assess attentional allocation as an index of cognitive processing, both primary and secondary tasks need to be presented simultaneously; under these circumstances, when interference on the secondary task occurs in the presence of threat-relevant stimuli on the primary task, attentional bias is inferred. With this procedural modification, no relative position effects were noted in reaction time for either sample, suggesting that the attentional interference noted in the PD sample on physical-panic threat and positive stimuli reflects a global attentional process. A second difference between the current paradigm and past research involves the response procedure utilized. In this study, Ss were required to respond via key pressing to indicate both the presence and absence of detection probes, unlike the procedure used by MacLeod et al. (1986), where Ss responded only when a dot probe was perceived. This modification ensured equal task requirements across conditions and reduced the possibility of a motor response bias as an explanation for reaction time differences. No between-group differences in physiological arousal (heart rate, skin conductance, and muscle tension) accompanied attentional interference effects. Rather, a small but significant heart rate
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decrease occurred following presentation of word pairs. This pattern is consistent with observations derived from Lacey’s ‘intake-rejection’ hypothesis. Specifically, Lacey (1959) and Lacey, Kagan, Lacy and Moss (1963) have demonstrated that heart rate deceleration occurs during perceptual functions (e.g. attention to visual stimuli), presumably to facilitate intake of environmental stimuli. In contrast, higher cognitive activities (e.g. mental arithmetic) are accompanied by heart rate acceleration, presumably to ‘reject’ unrelated stimuli which could disrupt cognitive performance. Although Lacey’s theory concerning the neurophysiological bases for these effects has been criticized (Elliott, 1972; Hahn, 1973), the observation of heart rate deceleration during perceptual tasks is robust across a variety of paradigms and supports conceptualization of the dot probe task as a measure of perceptual attention. The absence of between-group differences suggests that attentional hypervigilance in PD patients is not accompanied by increases in autonomic and somatic arousal. Based on these data, it would appear that an additional mediating process is required to account for the role of cognitive processes in initiating panic attacks. In particular, a model is needed to explain how stimulus encoding triggers the surges in physiological arousal which occur during panic attacks. A feature of the present study which deserves comment is the relative lack of group differences in resting levels of physiological arousal. With the exception of skin conductance, the PD patients and control Ss did not differ in resting arousal and in fact, the differences noted on skin conductance occurred only at one timepoint during the 3 min resting baseline. Other investigators have reported that PD patients show tonic elevation in autonomic arousal (cf. Barlow, 1988). Our failure to observe this phenomenon may have resulted from several procedural controls. First, the assessment protocol and instrumentation were explained thoroughly to each S prior to beginning the procedure, in order to reduce intergroup variation in psychophysiological response. Farha and Sher (1989) have demonstrated that informing Ss completely about experimental procedures prior to beginning psychophysiological measurement can significantly affect tonic arousal. Additionally, the use of a 10 min laboratory habituation interval could have served an important function, as shorter habituation intervals do not control fully for adaptation to the laboratory and the orienting reflex (Sallis & Lichstein, 1979). It is notable that Clark, Taylor, Hayward, King, Margraf, Ehlers, Roth and Agras (1990) also failed to observe higher levels of tonic heart rate in PD patients relative to controls using ambulatory monitoring, suggesting that previous reports may have been influenced by laboratory procedures. As noted in the description of Ss, the PD patients in this study obtained IQ scores which were slightly, but significantly lower than that obtained by the control Ss. In considering whether these IQ differences could account for the cognitive-attentional differences noted between PD patients and controls, it is notable that attentional interference effects were specific to emotionallysalient stimuli. Presumably, if reaction time differences on the dot probe task were attributable to IQ, the PD sample would have shown slower responding to neutral words as well as physical-panic threat, positive, and social threat terms. In light of the specificity of attentional interference, as well as the fact that the dot probe task appears to assess perceptual processes, rather than higher cognitive processes, the observed IQ differences between the PD and control samples do not appear relevant in interpreting these results. Additionally, the lack of group differences in semantic memory further suggests that IQ differences, while statistically different, did not influence these data. In sum, these data support the role of attentional processes in the maintenance of PD, although semantic memory appeared relatively unimportant in the context of these findings. Of particular note is the finding that PD patients demonstrate selective encoding effects with both threat-relevant stimuli and positive-valenced stimuli. This finding suggests that attentional vigilance in PD is not specific to anxiety-relevant cues, but rather, may reflect a more generalized process of encoding emotionally-toned stimuli. These effects were not accompanied by increases in physiological responding in the PD sample, suggesting that elaboration of existing theoretical models is necessary to account for the role of cognitive processes in initiating panic attacks. Clearly, future research would benefit by the inclusion of alternative strategies for assessment of semantic memory, given the inconsistent pattern of results obtained in studies to date. In many respects, the usefulness of information processing paradigms for refining available cognitive models of the anxiety disorders appears clear and necessary.
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Acknowledgements -This research was supported in part by grants from the Higher Education Coordinating Boards (Nos 0116181-061 and 003652-I 18), awarded to the first and second authors. We gratefully acknowledge the help of A. Marie Barron for assisting with structured interviews and Tom Chase and Joy Breckenridge for help with data collection.
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