- Email: [email protected]
Dissociation of physiology and behavior in PTSD
International Journal of Psychophysiology 62 (2006) 243 – 248 www.elsevier.com/locate/ijpsycho
Dissociation of physiology and behavior in PTSD J.H. Casada ⁎, J.D. Roache University of Texas Health Science Center at San Antonio, USA Received 6 May 2005; received in revised form 14 April 2006; accepted 25 April 2006 Available online 11 July 2006
Abstract We have previously reported that subjects with posttraumatic stress disorder (PTSD) differ from trauma controls in their ability to produce and withhold responses in the Stop-Signal Task depending on the motivational context as determined by financial reward. This experiment measured skin conductance and heart rate to assess autonomic changes accompanying these different patterns of behavior. Fowles hypothesized that heart rate would increase with behavioral activation and that increases in skin conductance would accompany behavioral inhibition. Both PTSD and comparison groups showed the expected behavioral changes in response to rewards, but they differed in their physiological responses. The subjects in the traumatized comparison group showed changes in skin conductance and heart rate consistent with Fowles' hypothesis and the observed changes in behavioral inhibition and activation. However, PTSD subjects showed no significant change in either physiological measure. These results demonstrate a dissociation between autonomic reactivity and motivated behavior in PTSD that may represent one aspect of emotional numbing. © 2006 Elsevier B.V. All rights reserved. Keywords: PTSD; Trauma; Inhibition; Heart rate; Skin conductance
1. Introduction Patients with posttraumatic stress disorder (PTSD) display a seemingly paradoxical mix of inhibited and activated behaviors. Consistent with its classification as an anxiety disorder in DSMIV (APA, 1994), PTSD patients show active and passive avoidance of distressing stimuli and reduced involvement in formerly pleasurable activities. At the same time, they have been characterized as irritable, danger seeking, or showing antisocial traits (Dutton, 1995; King et al., 1996; Munley et al., 1995). We have addressed this apparent paradox by examining the Stop-Signal Task behavior of PTSD subjects in a laboratory study (Casada and Roache, 2005). In that study, we found that subjects with PTSD were similar to traumatized comparison subjects in their acquisition of visually-cued motor responses and in responding more quickly when monetary rewards were provided for faster responding to visual cues. However, two important differences were found in PTSD subjects. First, during acquisition of cued inhibitory responses, in which a visual cue for a motor response was followed by an infrequently ⁎ Corresponding author. E-mail address: [email protected] (J.H. Casada). 0167-8760/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2006.04.005
occurring auditory stop-signal, PTSD subjects showed progressive slowing of motor responses. Second, PTSD subjects' inhibitory control was affected by the presence of monetary rewards for faster active responding to visual cues. When reward contingencies were absent, PTSD subjects were more inhibited and more likely to successfully withhold cued responses when stop-signals were present. However, when reward contingencies were present, they showed less ability to withhold inappropriate responses. Gray (1978) hypothesized that behaviors such as those in the Stop-Signal Task are controlled by two anatomically distinct neuronal systems responsible for behavioral inhibition and activation. Fowles (1980, 1988) further hypothesized that the activities of these systems resulted in distinct psychophysiologic changes. Based on studies using tasks carefully designed to measure either behavioral activation or inhibition (Fowles et al., 1982; Tranel, 1983), he showed that behavioral activation was associated with increases in heart rate and behavioral inhibition was associated with increased skin conductance. We have examined the autonomic changes in PTSD subjects as they perform an active, non-trauma-related task in order to improve our understanding of emotional regulation in PTSD. Clearly, PTSD subjects have been shown to differ from control
244
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
subjects in their emotional response and autonomic arousal in response to trauma-related stimuli (Casada et al., 1998; Pitman et al., 1990). However, the reaction of PTSD subjects to nontrauma-related stimuli is generally similar to controls (Blanchard et al., 1996, 1982; Gerardi et al., 1989; Malloy et al., 1983; McFall et al., 1990; Pallmeyer et al., 1986; Pitman et al., 1987), and they frequently show smaller reactions than controls in response to active, non-trauma-related tasks (Blanchard et al., 1989; Keane et al., 1998; McDonagh-Coyle et al., 2001). The present study examines the physiologic changes that accompany behavioral activation and inhibition in PTSD and traumatized comparison subjects during performance of the StopSignal Task (Logan and Cowan, 1984). Autonomic changes accompanying behavioral inhibition and activation were assessed by comparing skin conductance levels and heart rate between tasks that differed in their requirements for behavioral inhibition and by using monetary reward to experimentally enhance behavioral activation. 2. Materials and methods 2.1. Study design Two groups of subjects (10 PTSD and 13 traumatized but without PTSD) were initially screened for eligibility and then participated in an experimental laboratory study conducted over a day and a half wherein their performance on a modified StopSignal Task was tested. To develop acquisition of task performance and to prevent fatigue, the task was performed in five component sessions each lasting 30 to 45 min and separated by rest periods of at least 15 min. Subjects were paid an hourly rate of compensation commensurate with local IRB guidelines. Also, subjects could earn additional money dependent upon task performance as described below. Informed consent and experimental procedures were approved by the University of Texas Health Science Center at San Antonio Institutional Review Board and conformed to all current standards for protection of human subjects.
than those common to both PTSD and Major Depression. Comparison subjects had no psychiatric comorbidity. 2.3. The Stop-Signal Task The modified Stop-Signal Task used in this study was a computerized version based on the task described by Logan and Cowan (1984). Fig. 1 illustrates the tasks that subjects performed during study participation. Training for the StopSignal Task began by having subjects perform a less complex Simple Choice Reaction Time Task (Fig. 1A). In this task, subjects were presented with a series of letters (uppercase letters M, N, V, and W) at 3-s intervals. Each letter presentation comprised a single trial. Two of the letters signaled subjects to press the left mouse button, and two signaled them to press the right button. Subjects were instructed to press the correct button as quickly as possible. The computer recorded the button pushed and the response latency in ms. After acquiring stable performance on the Simple Choice Reaction Time Task, subjects performed the Stop-Signal Task (Fig. 1B). This task was identical to the first task except that in 39% of the trials an audible signal (stop-signal) followed the letter stimulus and indicated that the subject was not to press a button. In order to reduce the predictability of the stop-signal presentation, the stop-signals occurred at one of three equally probably delays. For additional information about the Stop-Signal Task used in this study, see Casada and Roache (2005). 2.4. Procedure Subjects presented to the laboratory at 8:00 a.m. on 2 days. They were encouraged to eat a normal breakfast and were allowed to smoke cigarettes up to 1-h prior to participation. No caffeine or nicotine was permitted until after completion of each
2.2. Participants Twenty-three male and female subjects who had experienced a trauma sufficient to meet criterion A for PTSD in DSM-IV (APA, 1994) were recruited from the community using fliers and newspaper advertisements designed to attract symptomatic and asymptomatic subjects. All subjects gave informed consent before evaluation and diagnosis by a psychiatrist (J.H.C.) using DSM-IV criteria. 10 subjects had a primary diagnosis of PTSD, and 13 comparison subjects had never met full criteria for PTSD. None of the subjects had current substance abuse or dependence diagnoses or a history of bipolar affective disorder, psychotic disorder, or non-PTSD anxiety disorder. No participants were on psychoactive medications. Seven of the 10 PTSD subjects had comorbid major depressive disorder that was considered to be secondary to PTSD based on the relative severity of depressive symptoms, onset of depressive symptoms after the development of PTSD, and the presence of few depressive symptoms other
Fig. 1. Schematic diagrams of the Simple Choice Reaction Time (A) and StopSignal Tasks. Letter stimuli signal subjects to produce a motor response. Adding stop-signals in 39% of trials (13% in each of early, middle, and late) results in the continued production of shorter latency but withholding of longer latency responses.
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
245
respectively. The Tridimensional Personality Questionnaire (Cloninger, 1989) was administered to determine differences in harm avoidance and reward dependence between groups. The severity of dissociative symptoms was assessed using the Dissociative Experiences Scale (Bernstein and Putnam, 1986).
study day. A blood alcohol level of zero was verified by breathalyzer. The experiment was conducted in five sessions. Sessions 1–3 were conducted on day 1, and Sessions 4 and 5 occurred on day 2. All sessions were conducted as multiple blocks of 100 trials each, with 2 min off task between blocks and at least a 15 min rest period between sessions. Session 1 allowed subjects to acquire the Simple Choice Reaction Time Task and consisted of 5 blocks of 100 trials. Session 2 allowed subjects to learn the full Stop-Signal Task for five additional blocks. Also, during Session 2 the stopsignal delays were adjusted using a staircase tracking algorithm to achieve a 50% failure-to-inhibit rate for each subject. Sessions 3–5 each consisted of 2 sets of 4 blocks, one set conducted without monetary rewards and one set including rewards for fast and accurate responses on trials lacking stop signals. Under reward contingencies, subjects were given $0.07 for each trial in which the latency of a correct response was less than the median response latency observed in the final three blocks of Session 2. This resulted in PTSD and the traumatized comparison groups earning similar amounts of money (PTSD: $55.46 vs. Comparison: $55.74). A running total of money earned during each block was displayed on the computer screen during rewarded performance. The presentation order for reward conditions was counter-balanced across diagnostic groups. Subjects were paid at the end of each study day.
Data were analyzed using SAS (SAS Institute, Cary, NC). Categorical demographic variables were analyzed using the Chi-square statistic. Quantitative differences between groups were assessed using a two-sample Student's t-test. Since Sessions 1–2 were used to acquire the Simple Choice Reaction Time Task and Stop-Signal Task, physiologic data from Sessions 1–2 and 3–5 were analyzed separately. Data from Sessions 1–2 were analyzed using a fully specified ANOVA model consisting of subjects nested in a diagnosis group factorialized with session (2 sessions) and block (5 blocks per session). Data from Sessions 3–5 were analyzed using a similar ANOVA model consisting of subjects nested in a diagnosis group factorialized with session (3 sessions), reward (2 reward conditions), and block (4 blocks per session). Baseline values were used as covariates in these analyses. For all hypothesis testing, two-tailed tests (α = 0.05) were performed.
2.5. Physiologic measures
3. Results
Heart rate and skin conductance were measured using a BIOPAC MP100 system (BIOPAC Systems, Inc., Santa Barbara, CA). Electrocardiogram (ECG) electrodes were placed on the arms bilaterally. Skin conductance (SC) electrodes were filled with an isotonic electrode paste and placed on the middle phalanges of the third and fourth digits of the non-dominant hand. Physiologic data were recorded for 1 min prior to task performance (baseline) and throughout each block of testing. ECG and SC signals were amplified using ECG100B and GSR100B amplifiers, digitized at 200 Hz, and stored electronically for off-line analysis. Physiological data were reduced by computing mean heart rate and skin conductance level for baseline and testing periods.
3.1. Subject characteristics
2.7. Data analysis
Table 1 shows that PTSD and comparison groups were similar in age and gender. As expected, PTSD subjects were found to have more severe PTSD symptoms by both self-report and clinician-administered ratings and had increased dissociative symptoms. PTSD subjects also endorsed more intense anxiety and depression than comparison subjects. With regard to personality characteristics, PTSD subjects reported a greater tendency to avoid distressing situations and a decreased role of rewards in influencing their behavior. Table 1 Demographic and self-report measures
2.6. Other measures Several clinician-administered and self-report scales were used to assess a variety of clinical symptoms and mood states. The Clinician-Administered PTSD Scale (CAPS)Diagnostic Version (Blake et al., 1997) was used to measure the current severity of PTSD symptoms in PTSD subjects and the most intense lifetime trauma-related symptoms in comparison subjects. The Impact of Events Scale (Horowitz et al., 1979) was also used to assess current PTSD symptoms. The State–Trait Anxiety Inventory (Spielberger et al., 1970) and 21-item Beck Depression Inventory (Beck et al., 1986) were used to measure anxiety and depressive symptoms,
Age, years Sex Clinician-Administered PTSD Scale Score Impact of Events Scale Dissociative Experiences Scale Spielberger State Anxiety Spielberger Trait Anxiety Beck Depression Inventory TPQ–Harm Avoidance TPQ–Novelty Seeking TPQ–Reward Dependence
PTSD
Control
43.3 ± 4.86 50.0% male 72.5 ± 6.3 ⁎ 79.3 ± 12.5 ⁎ 18.7 ± 3.4 ⁎ 58.7 ± 3.9 ⁎ 58.6 ± 2.9 ⁎ 26.1 ± 3.2 ⁎ 19.7 ± 3.2 ⁎ 17.6 ± 2.1 13.3 ± 1.4 ⁎
41.5 ± 13.2 61.5% male 15.1 ± 2.9 11.5 ± 6.2 4.0 ± 1.3 28.5 ± 1.8 31.5 ± 2.6 5.5 ± 1.5 10.5 ± 1.3 13.8 ± 2.1 20.3 ± 1.7
Values are expressed as mean ± standard error. TPQ = Tridimensional Personality Questionnaire. ⁎ Significant difference vs. control (p < 0.05).
246
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
Fig. 2. Estimated marginal means (±S.E.M) for heart rate during acquisition of the Simple Choice Reaction Time Task in PTSD (■) and traumatized comparison (O) subjects.
3.2. Stop-signal testing 3.2.1. Session 1: Acquisition of simple choice reaction time task During this session, PTSD and comparison subjects initially responded slowly to the letter stimuli but rapidly decreased their response times across testing blocks. There were no behavioral differences between the diagnostic groups (Casada and Roache, 2005). As expected, the mean skin conductance levels were stable across blocks in both groups, and no differences were observed between groups. However, mean heart rate showed greater variability across blocks in the comparison group [Fig. 2, diagnosis × block interaction, F(4,84) = 2.59, p < 0.05]. 3.2.2. Session 2: Acquisition of Stop-Signal Task Upon introducing stop-signals, PTSD subjects progressively slowed their response times while comparison subjects' times remained stable (Casada and Roache, 2005). In response to this new demand for behavioral inhibition, mean skin conductance was higher in comparison subjects than in PTSD [2.93 vs. 2.40 μS (micro-Siemens), respectively; diagnosis main effect, F(1,21) = 7.38, p = 0.01]. Mean heart rate did not differ between groups during this block.
Fig. 4. Estimated marginal means (±S.E.M.) for skin conductance in PTSD (■) and traumatized control (O) subjects. The Stop-Signal Task was performed with ($) and without (No $) monetary reward.
3.3. Sessions 3–5: Performance of rewarded and non-rewarded Stop-Signal Tasks The presence of monetary reward had a significant effect on both behavioral and physiological changes during Sessions 3–5. Behaviorally, monetary rewards for fast responses produced similar reductions in the response times of both PTSD and comparison subjects. However, while comparison subjects showed similar abilities to inhibit responses with and without monetary reward, PTSD subjects were more inhibited during non-rewarded performance and less inhibited during reward (Casada and Roache, 2005). As shown in Fig. 3, performing with reward contingencies increased heart rate compared to non-reward conditions [reward main effect, F(1,21) = 5.99, p < 0.05] although PTSD subjects showed smaller and less consistent changes than did the comparison group [diagnosis × reward interaction, F(1,21) = 4.29, p = 0.05]. Skin conductance showed a similar pattern with the comparison group exhibiting marked increases during performance under reward contingencies and PTSD subjects showing little change [Fig. 4, diagnosis × reward interaction, F(1,21) = 10.44, p < 0.01]. These differences are unrelated to any change in baseline physiological levels since they were used as covariates in the analysis. 4. Discussion
Fig. 3. Estimated marginal means (±S.E.M.) for heart rate in PTSD (■) and traumatized control (O) subjects. The Stop-Signal Task was performed with ($) and without (No $) monetary reward.
The main finding of this study is that PTSD subjects did not show the physiological changes expected to accompany behavioral activation or inhibition. On the other hand, the traumatized comparison subjects' physiological responses were consistent with Fowles' (1980, 1988) hypotheses. During acquisition of the Simple Choice Reaction Time Task (Session 1), subjects were required to produce active behaviors but were not exposed to inhibitory signals. The comparison subjects, but not the PTSD subjects, showed the expected variability in heart rate and stable skin conductance. When stop-signals were added in Session 2, the comparison subjects, but not the PTSD subjects, showed the increases in skin conductance expected to accompany the increased inhibitory demands. In Sessions 3–5,
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
behavioral activation was manipulated using monetary rewards. Again, comparison subjects showed the increases in heart rate accompanying the reward-induced behavioral activation predicted by Fowles, while PTSD subjects showed little change. The lack of physiological responsiveness of PTSD subjects to the behavioral demands of the Stop-Signal Task stands in stark contrast to numerous studies showing increased heart rate and skin conductance reactivity to trauma-related stimuli (Casada et al., 1998; Pitman et al., 1990) and normal responsiveness to non-trauma-related stimuli (Blanchard et al., 1996, 1982; Gerardi et al., 1989; Malloy et al., 1983; McFall et al., 1990; Pallmeyer et al., 1986; Pitman et al., 1987). Physiological reactivity to trauma stimuli is the common pattern seen in PTSD (Casada et al., 1998; McDonagh-Coyle et al., 2001) and is hypothesized to be important to the pathophysiology of PTSD (Foa et al., 1989; Keane et al., 1985). On the other hand, our finding of reduced reactivity during the performance of an active task is consistent with studies showing decreased responsiveness during performance of mental arithmetic (Blanchard et al., 1989; Keane et al., 1998; McDonagh-Coyle et al., 2001). The lack of physiological response of our PTSD subjects also is in stark contrast to their behavioral responses to the Stop-Signal Task demands and reward contingencies (Casada and Roache, 2005). PTSD and comparison subjects showed very distinct behavioral activation during the reward contingency. In addition, compared to the comparison group, PTSD subjects showed marked reductions in behavioral inhibition during reward. While the physiological changes accompanying behavioral activation and inhibition in traumatized comparison subjects are consistent with Fowles' hypothesis, they may be interpreted in other ways as well. Increased heart rate during behavioral activation may be due to the increased physical demands of responding (Fowles, 1988) or may reflect general arousal (Stewart et al., 2001). Similarly, skin conductance is a sensitive indicator of nonspecific arousal (Casada et al., 1998) and may be unrelated to behavioral inhibition. Nevertheless, we believe that the physiological changes observed in comparison subjects reflect, at least in part, the physiological activity of behavioral activating and inhibiting neuronal systems. The heart rate changes observed in comparison subjects are unlikely to be due to changes in physical response demands since the motor task performed with and without reward was unchanged. Interpretation of the skin conductance increases in comparison subjects is less certain since this study did not independently control the motivation to inhibit behavior. We would expect increased behavioral inhibition as subjects acquire new inhibitory behaviors (Session 2) or strive to maintain inhibition in the face of increased motivation to produce responses (reward condition in Sessions 3–5). Therefore, the increased skin conductance of comparison subjects observed under these conditions is consistent with Fowles' hypothesis. Still, these conditions also would be expected to increase nonspecific arousal. Nevertheless, regardless of how the physiological changes are interpreted, it is noteworthy that PTSD subjects failed to show these changes despite producing the expected behavioral responses.
247
There are several possible explanations for the decreased responsiveness observed in PTSD subjects. First, PTSD subjects may appraise the Stop-Signal Task differently than the comparison subjects. Tomaka et al. (1993) found that subjects who appraised an active task as a threat showed less cardiovascular reactivity than subjects who appraised it as a challenge. Second, PTSD subjects may limit physiologic arousal as a means of controlling negative emotion. This is similar to elements of somatoform dissociation described by Nijenhuis et al. (2004) and may represent a physiological counterpart of emotional numbing. It also is consistent with several findings in which PTSD subjects were found to be less responsive than comparison subjects or other anxiety disorder subjects to a variety of stressors (Cuthbert et al., 2003; Orr et al., 1998). Overall, our findings suggest that, while PTSD subjects have intact behavioral activating and inhibiting systems, they do not display the associated physiological changes hypothesized by Fowles and observed in comparison subjects. This evidence is consistent with clinically described decreases in emotional expression in PTSD. Thus, we conclude that PTSD and comparison subjects differ in their physiological and emotion responses to stimuli even when their behavior is similar. The results of this study should be interpreted with care due to the small sample size and prevalent depressive comorbidity in the PTSD group. Further research is required to define the neuroanatomical and neurochemical systems controlling the suppression of autonomic responses to non-trauma-related, active tasks in PTSD subjects. Additional clinical research may also help clarify how the physiological changes accompanying PTSD affect long-term health and functioning. Acknowledgements This research was supported by an Institutional Research Grant from the University of Texas Health Science Center at San Antonio and by the Frederic C. Bartter General Clinical Research Center. Preparation of the manuscript was supported by National Institute on Drug Abuse Award K08 DA00507 to John Casada. References American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Press, Washington, DC. Beck, A.T., Steer, R.A., Brown, G.K., 1986. Beck Depression Inventory– Second Edition Manual, Psychological Corporation, Harcourt, Brace, San Antonio, TX. Bernstein, E.M., Putnam, F.W., 1986. Development, reliability, and validity of a dissociation scale. J. Nerv. Ment. Dis. 174 (12), 727–735. Blake, D.D., Weathers, F.W., Nagy, L.M., Kaloupek, D.G., Charney, D.S., Keane, T.M., 1997. Clinician-Administered PTSD Scale for DSM-IV: Current and Lifetime Version. National Center for PTSD. Blanchard, E.B., Hickling, E.J., Buckley, T.C., Taylor, E., Vollmer, A., Loos, W.R., 1996. Psychophysiology of posttraumatic stress disorder related to motor vehicle accidents: replication and extension. J. Consult. Clin. Psychol. 64 (4), 742–751. Blanchard, E.B., Kolb, L.C., Pallmeyer, T.P., Gerardi, R.J., 1982. A psychophysiological study of post traumatic stress disorder in Vietnam veterans. Psychiatr. Q. 54 (4), 220–229.
248
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
Blanchard, E.B., Kolb, L.C., Taylor, A.E., Wittrock, D.A., 1989. Cardiac response to relevant stimuli an adjunct in diagnosing posttraumatic stress disorder: replication and extension. Behav. Ther. 535–543. Casada, J.H., Amdur, R., Larsen, R., Liberzon, I., 1998. Psychophysiologic responsivity in posttraumatic stress disorder: generalized hyperresponsiveness versus trauma specificity. Biol. Psychiatry 44, 1037–1044. Casada, J.H., Roache, J.D., 2005. Behavioral inhibition and activation in posttraumatic stress disorder. J. Nerv. Ment. Dis. 193 (2), 102–109. Cloninger, C.R., 1989. The Tridimensional Personality Questionnaire. Department of Psychiatry and Genetics. Washington University School of Medicine, St. Louis, MO. Cuthbert, B.N., Lang, P.J., Strauss, C., Drobes, D., Patrick, C.J., Bradley, M.M., 2003. The psychophysiology of anxiety disorder: fear memory imagery. Psychophysiology 40 (3), 407–422. Dutton, D.G., 1995. Trauma symptoms and PTSD-like profiles in perpetrators of intimate abuse. J. Trauma Stress 8, 299–316. Foa, E.B., Steketee, G.S., Rothbaum, B.O., 1989. Behavioral/cognitive conceptualizations of posttraumatic stress disorder. Behav. Ther. 20, 229–243. Fowles, D.C., 1980. The three arousal model: implications of gray's two-factor learning theory for heart rate, electrodermal activity, and psychopathy. Psychophysiology 17 (2), 87–104. Fowles, D.C., 1988. Psychophysiology and psychopathology: a motivational approach. Psychophysiology 25 (4), 373–391. Fowles, D.C., Fisher, A.E., Tranel, D.T., 1982. The heart beats to reward: the effect of monetary incentive on heart rate. Psychophysiology 19 (5), 506–513. Gerardi, R.J., Blanchard, E.B., Kolb, L.C., 1989. Ability of Vietnam veterans to dissimulate a psychophysiological assessment for posttraumatic stress disorder. Behav. Ther. 20, 229–243. Gray, J.A., 1978. The neuropsychology of anxiety. Br. J. Psychol. 69, 417–434. Horowitz, M., Wilner, N., Alvarez, W., 1979. Impact of Events Scale: a measure of subjective stress. Psychosom. Med. 41, 209–218. Keane, T.M., Kolb, L.C., Kaloupek, D.G., Orr, S.P., Blanchard, E.B., Thomas, R.G., Hseih, Y.F., Lavori, P.W., 1998. Results of a multisite clinical trial on the psychophysiological assessment of posttraumatic stress disorder. J. Consult. Clin. Psychol. 66, 914–923. Keane, T.M., Zimering, R.T., Caddell, J.M., 1985. A behavioral formulation of posttraumatic stress disorder in Vietnam veterans. Behav. Ther. 8 (1), 9–12. King, D.W., King, L.A., Foy, D.W., Gudanowski, D.M., 1996. Prewar factors in combat-related posttraumatic stress disorder: structural equation modeling with a national sample of female and male Vietnam veterans. J. Consult. Clin. Psychol. 64, 520–531.
Logan, G.D., Cowan, W.B., 1984. On the ability to inhibit thought and action: a theory of an act of control. Psychol. Rev. 91, 295–327. Malloy, P.F., Fairbank, J.A., Keane, T.M., 1983. Validation of a multimethod assessment of posttraumatic stress disorders in Vietnam veterans. J. Consult. Clin. Psychol. 51 (4), 488–494. McDonagh-Coyle, A., McHugo, G.J., Friedman, M.J., Schnurr, P.P., Zayfert, C., Descamps, M., 2001. Psychophysiological reactivity in female sexual abuse survivors. J. Trauma Stress 14 (4), 667–683. McFall, M.E., Murburg, M.M., Ko, G.N., Veith, R.C., 1990. Autonomic responses to stress in Vietnam combat veterans with posttraumatic stress disorder. Biol. Psychiatry 27 (10), 1165–1175. Munley, P.H., Bains, D.S., Bloem, W.D., Busby, R.M., Pendziszewski, S., 1995. Posttraumatic stress disorder and the MCMI-II. Psychol. Rep. 76, 939–944. Nijenhuis, E.R.S., van der Hart, O., Kruger, K., Steele, K., 2004. Somatoform dissociation, reported abuse and animal defence-like reactions. Aust. N. Z. J. Psychiatry 38, 678–686. Orr, S.P., Meyerhoff, J.L., Edwards, J.V., Pitman, R.K., 1998. Heart rate and blood pressure resting levels and responses to generic stressors in Vietnam veterans with posttraumatic stress disorder. J. Trauma Stress 11 (1), 155–164. Pallmeyer, T.P., Blanchard, E.B., Kolb, L.C., 1986. The psychophysiology of combat-induced post-traumatic stress disorder in Vietnam veterans. Behav. Res. Ther. 24 (6), 645–652. Pitman, R.K., Orr, S.P., Forgue, D.F., Altman, B., de Jong, J.B., Herz, L.R., 1990. Psychophysiologic responses to combat imagery of Vietnam veterans with posttraumatic stress disorder versus other anxiety disorders. J. Abnorm. Psychology 99 (1), 49–54. Pitman, R.K., Orr, S.P., Forgue, D.F., de Jong, J.B., Claiborn, J.M., 1987. Psychophysiologic assessment of posttraumatic stress disorder imagery in Vietnam combat veterans. Arch. Gen. Psychiatry 44 (11), 970–975. Spielberger, C.D., Gorsuch, R.R., Luchene, R.E., 1970. State–Trait Anxiety Inventory. Consulting Psychologists Press, Palo Alto, CA. Stewart, S.H., Buffett-Jerrott, S.E., Kokaram, R., 2001. Heartbeat awareness and heart rate reactivity in anxiety sensitivity: a further investigation. J. Anxiety Disord. 15 (6), 535–553. Tomaka, J., Blascovich, J., Kelsey, R.M., Leitten, C.L., 1993. Subjective, physiological, and behavioral effects of threat and challenge appraisal. J. Pers. Soc. Psychol. 65, 248–260. Tranel, D.T., 1983. The effects of monetary incentive and frustrative nonreward on heart rate and electrodermal activity. Psychophysiology 20 (6), 652–657.
Dissociation of physiology and behavior in PTSD J.H. Casada ⁎, J.D. Roache University of Texas Health Science Center at San Antonio, USA Received 6 May 2005; received in revised form 14 April 2006; accepted 25 April 2006 Available online 11 July 2006
Abstract We have previously reported that subjects with posttraumatic stress disorder (PTSD) differ from trauma controls in their ability to produce and withhold responses in the Stop-Signal Task depending on the motivational context as determined by financial reward. This experiment measured skin conductance and heart rate to assess autonomic changes accompanying these different patterns of behavior. Fowles hypothesized that heart rate would increase with behavioral activation and that increases in skin conductance would accompany behavioral inhibition. Both PTSD and comparison groups showed the expected behavioral changes in response to rewards, but they differed in their physiological responses. The subjects in the traumatized comparison group showed changes in skin conductance and heart rate consistent with Fowles' hypothesis and the observed changes in behavioral inhibition and activation. However, PTSD subjects showed no significant change in either physiological measure. These results demonstrate a dissociation between autonomic reactivity and motivated behavior in PTSD that may represent one aspect of emotional numbing. © 2006 Elsevier B.V. All rights reserved. Keywords: PTSD; Trauma; Inhibition; Heart rate; Skin conductance
1. Introduction Patients with posttraumatic stress disorder (PTSD) display a seemingly paradoxical mix of inhibited and activated behaviors. Consistent with its classification as an anxiety disorder in DSMIV (APA, 1994), PTSD patients show active and passive avoidance of distressing stimuli and reduced involvement in formerly pleasurable activities. At the same time, they have been characterized as irritable, danger seeking, or showing antisocial traits (Dutton, 1995; King et al., 1996; Munley et al., 1995). We have addressed this apparent paradox by examining the Stop-Signal Task behavior of PTSD subjects in a laboratory study (Casada and Roache, 2005). In that study, we found that subjects with PTSD were similar to traumatized comparison subjects in their acquisition of visually-cued motor responses and in responding more quickly when monetary rewards were provided for faster responding to visual cues. However, two important differences were found in PTSD subjects. First, during acquisition of cued inhibitory responses, in which a visual cue for a motor response was followed by an infrequently ⁎ Corresponding author. E-mail address: [email protected] (J.H. Casada). 0167-8760/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2006.04.005
occurring auditory stop-signal, PTSD subjects showed progressive slowing of motor responses. Second, PTSD subjects' inhibitory control was affected by the presence of monetary rewards for faster active responding to visual cues. When reward contingencies were absent, PTSD subjects were more inhibited and more likely to successfully withhold cued responses when stop-signals were present. However, when reward contingencies were present, they showed less ability to withhold inappropriate responses. Gray (1978) hypothesized that behaviors such as those in the Stop-Signal Task are controlled by two anatomically distinct neuronal systems responsible for behavioral inhibition and activation. Fowles (1980, 1988) further hypothesized that the activities of these systems resulted in distinct psychophysiologic changes. Based on studies using tasks carefully designed to measure either behavioral activation or inhibition (Fowles et al., 1982; Tranel, 1983), he showed that behavioral activation was associated with increases in heart rate and behavioral inhibition was associated with increased skin conductance. We have examined the autonomic changes in PTSD subjects as they perform an active, non-trauma-related task in order to improve our understanding of emotional regulation in PTSD. Clearly, PTSD subjects have been shown to differ from control
244
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
subjects in their emotional response and autonomic arousal in response to trauma-related stimuli (Casada et al., 1998; Pitman et al., 1990). However, the reaction of PTSD subjects to nontrauma-related stimuli is generally similar to controls (Blanchard et al., 1996, 1982; Gerardi et al., 1989; Malloy et al., 1983; McFall et al., 1990; Pallmeyer et al., 1986; Pitman et al., 1987), and they frequently show smaller reactions than controls in response to active, non-trauma-related tasks (Blanchard et al., 1989; Keane et al., 1998; McDonagh-Coyle et al., 2001). The present study examines the physiologic changes that accompany behavioral activation and inhibition in PTSD and traumatized comparison subjects during performance of the StopSignal Task (Logan and Cowan, 1984). Autonomic changes accompanying behavioral inhibition and activation were assessed by comparing skin conductance levels and heart rate between tasks that differed in their requirements for behavioral inhibition and by using monetary reward to experimentally enhance behavioral activation. 2. Materials and methods 2.1. Study design Two groups of subjects (10 PTSD and 13 traumatized but without PTSD) were initially screened for eligibility and then participated in an experimental laboratory study conducted over a day and a half wherein their performance on a modified StopSignal Task was tested. To develop acquisition of task performance and to prevent fatigue, the task was performed in five component sessions each lasting 30 to 45 min and separated by rest periods of at least 15 min. Subjects were paid an hourly rate of compensation commensurate with local IRB guidelines. Also, subjects could earn additional money dependent upon task performance as described below. Informed consent and experimental procedures were approved by the University of Texas Health Science Center at San Antonio Institutional Review Board and conformed to all current standards for protection of human subjects.
than those common to both PTSD and Major Depression. Comparison subjects had no psychiatric comorbidity. 2.3. The Stop-Signal Task The modified Stop-Signal Task used in this study was a computerized version based on the task described by Logan and Cowan (1984). Fig. 1 illustrates the tasks that subjects performed during study participation. Training for the StopSignal Task began by having subjects perform a less complex Simple Choice Reaction Time Task (Fig. 1A). In this task, subjects were presented with a series of letters (uppercase letters M, N, V, and W) at 3-s intervals. Each letter presentation comprised a single trial. Two of the letters signaled subjects to press the left mouse button, and two signaled them to press the right button. Subjects were instructed to press the correct button as quickly as possible. The computer recorded the button pushed and the response latency in ms. After acquiring stable performance on the Simple Choice Reaction Time Task, subjects performed the Stop-Signal Task (Fig. 1B). This task was identical to the first task except that in 39% of the trials an audible signal (stop-signal) followed the letter stimulus and indicated that the subject was not to press a button. In order to reduce the predictability of the stop-signal presentation, the stop-signals occurred at one of three equally probably delays. For additional information about the Stop-Signal Task used in this study, see Casada and Roache (2005). 2.4. Procedure Subjects presented to the laboratory at 8:00 a.m. on 2 days. They were encouraged to eat a normal breakfast and were allowed to smoke cigarettes up to 1-h prior to participation. No caffeine or nicotine was permitted until after completion of each
2.2. Participants Twenty-three male and female subjects who had experienced a trauma sufficient to meet criterion A for PTSD in DSM-IV (APA, 1994) were recruited from the community using fliers and newspaper advertisements designed to attract symptomatic and asymptomatic subjects. All subjects gave informed consent before evaluation and diagnosis by a psychiatrist (J.H.C.) using DSM-IV criteria. 10 subjects had a primary diagnosis of PTSD, and 13 comparison subjects had never met full criteria for PTSD. None of the subjects had current substance abuse or dependence diagnoses or a history of bipolar affective disorder, psychotic disorder, or non-PTSD anxiety disorder. No participants were on psychoactive medications. Seven of the 10 PTSD subjects had comorbid major depressive disorder that was considered to be secondary to PTSD based on the relative severity of depressive symptoms, onset of depressive symptoms after the development of PTSD, and the presence of few depressive symptoms other
Fig. 1. Schematic diagrams of the Simple Choice Reaction Time (A) and StopSignal Tasks. Letter stimuli signal subjects to produce a motor response. Adding stop-signals in 39% of trials (13% in each of early, middle, and late) results in the continued production of shorter latency but withholding of longer latency responses.
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
245
respectively. The Tridimensional Personality Questionnaire (Cloninger, 1989) was administered to determine differences in harm avoidance and reward dependence between groups. The severity of dissociative symptoms was assessed using the Dissociative Experiences Scale (Bernstein and Putnam, 1986).
study day. A blood alcohol level of zero was verified by breathalyzer. The experiment was conducted in five sessions. Sessions 1–3 were conducted on day 1, and Sessions 4 and 5 occurred on day 2. All sessions were conducted as multiple blocks of 100 trials each, with 2 min off task between blocks and at least a 15 min rest period between sessions. Session 1 allowed subjects to acquire the Simple Choice Reaction Time Task and consisted of 5 blocks of 100 trials. Session 2 allowed subjects to learn the full Stop-Signal Task for five additional blocks. Also, during Session 2 the stopsignal delays were adjusted using a staircase tracking algorithm to achieve a 50% failure-to-inhibit rate for each subject. Sessions 3–5 each consisted of 2 sets of 4 blocks, one set conducted without monetary rewards and one set including rewards for fast and accurate responses on trials lacking stop signals. Under reward contingencies, subjects were given $0.07 for each trial in which the latency of a correct response was less than the median response latency observed in the final three blocks of Session 2. This resulted in PTSD and the traumatized comparison groups earning similar amounts of money (PTSD: $55.46 vs. Comparison: $55.74). A running total of money earned during each block was displayed on the computer screen during rewarded performance. The presentation order for reward conditions was counter-balanced across diagnostic groups. Subjects were paid at the end of each study day.
Data were analyzed using SAS (SAS Institute, Cary, NC). Categorical demographic variables were analyzed using the Chi-square statistic. Quantitative differences between groups were assessed using a two-sample Student's t-test. Since Sessions 1–2 were used to acquire the Simple Choice Reaction Time Task and Stop-Signal Task, physiologic data from Sessions 1–2 and 3–5 were analyzed separately. Data from Sessions 1–2 were analyzed using a fully specified ANOVA model consisting of subjects nested in a diagnosis group factorialized with session (2 sessions) and block (5 blocks per session). Data from Sessions 3–5 were analyzed using a similar ANOVA model consisting of subjects nested in a diagnosis group factorialized with session (3 sessions), reward (2 reward conditions), and block (4 blocks per session). Baseline values were used as covariates in these analyses. For all hypothesis testing, two-tailed tests (α = 0.05) were performed.
2.5. Physiologic measures
3. Results
Heart rate and skin conductance were measured using a BIOPAC MP100 system (BIOPAC Systems, Inc., Santa Barbara, CA). Electrocardiogram (ECG) electrodes were placed on the arms bilaterally. Skin conductance (SC) electrodes were filled with an isotonic electrode paste and placed on the middle phalanges of the third and fourth digits of the non-dominant hand. Physiologic data were recorded for 1 min prior to task performance (baseline) and throughout each block of testing. ECG and SC signals were amplified using ECG100B and GSR100B amplifiers, digitized at 200 Hz, and stored electronically for off-line analysis. Physiological data were reduced by computing mean heart rate and skin conductance level for baseline and testing periods.
3.1. Subject characteristics
2.7. Data analysis
Table 1 shows that PTSD and comparison groups were similar in age and gender. As expected, PTSD subjects were found to have more severe PTSD symptoms by both self-report and clinician-administered ratings and had increased dissociative symptoms. PTSD subjects also endorsed more intense anxiety and depression than comparison subjects. With regard to personality characteristics, PTSD subjects reported a greater tendency to avoid distressing situations and a decreased role of rewards in influencing their behavior. Table 1 Demographic and self-report measures
2.6. Other measures Several clinician-administered and self-report scales were used to assess a variety of clinical symptoms and mood states. The Clinician-Administered PTSD Scale (CAPS)Diagnostic Version (Blake et al., 1997) was used to measure the current severity of PTSD symptoms in PTSD subjects and the most intense lifetime trauma-related symptoms in comparison subjects. The Impact of Events Scale (Horowitz et al., 1979) was also used to assess current PTSD symptoms. The State–Trait Anxiety Inventory (Spielberger et al., 1970) and 21-item Beck Depression Inventory (Beck et al., 1986) were used to measure anxiety and depressive symptoms,
Age, years Sex Clinician-Administered PTSD Scale Score Impact of Events Scale Dissociative Experiences Scale Spielberger State Anxiety Spielberger Trait Anxiety Beck Depression Inventory TPQ–Harm Avoidance TPQ–Novelty Seeking TPQ–Reward Dependence
PTSD
Control
43.3 ± 4.86 50.0% male 72.5 ± 6.3 ⁎ 79.3 ± 12.5 ⁎ 18.7 ± 3.4 ⁎ 58.7 ± 3.9 ⁎ 58.6 ± 2.9 ⁎ 26.1 ± 3.2 ⁎ 19.7 ± 3.2 ⁎ 17.6 ± 2.1 13.3 ± 1.4 ⁎
41.5 ± 13.2 61.5% male 15.1 ± 2.9 11.5 ± 6.2 4.0 ± 1.3 28.5 ± 1.8 31.5 ± 2.6 5.5 ± 1.5 10.5 ± 1.3 13.8 ± 2.1 20.3 ± 1.7
Values are expressed as mean ± standard error. TPQ = Tridimensional Personality Questionnaire. ⁎ Significant difference vs. control (p < 0.05).
246
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
Fig. 2. Estimated marginal means (±S.E.M) for heart rate during acquisition of the Simple Choice Reaction Time Task in PTSD (■) and traumatized comparison (O) subjects.
3.2. Stop-signal testing 3.2.1. Session 1: Acquisition of simple choice reaction time task During this session, PTSD and comparison subjects initially responded slowly to the letter stimuli but rapidly decreased their response times across testing blocks. There were no behavioral differences between the diagnostic groups (Casada and Roache, 2005). As expected, the mean skin conductance levels were stable across blocks in both groups, and no differences were observed between groups. However, mean heart rate showed greater variability across blocks in the comparison group [Fig. 2, diagnosis × block interaction, F(4,84) = 2.59, p < 0.05]. 3.2.2. Session 2: Acquisition of Stop-Signal Task Upon introducing stop-signals, PTSD subjects progressively slowed their response times while comparison subjects' times remained stable (Casada and Roache, 2005). In response to this new demand for behavioral inhibition, mean skin conductance was higher in comparison subjects than in PTSD [2.93 vs. 2.40 μS (micro-Siemens), respectively; diagnosis main effect, F(1,21) = 7.38, p = 0.01]. Mean heart rate did not differ between groups during this block.
Fig. 4. Estimated marginal means (±S.E.M.) for skin conductance in PTSD (■) and traumatized control (O) subjects. The Stop-Signal Task was performed with ($) and without (No $) monetary reward.
3.3. Sessions 3–5: Performance of rewarded and non-rewarded Stop-Signal Tasks The presence of monetary reward had a significant effect on both behavioral and physiological changes during Sessions 3–5. Behaviorally, monetary rewards for fast responses produced similar reductions in the response times of both PTSD and comparison subjects. However, while comparison subjects showed similar abilities to inhibit responses with and without monetary reward, PTSD subjects were more inhibited during non-rewarded performance and less inhibited during reward (Casada and Roache, 2005). As shown in Fig. 3, performing with reward contingencies increased heart rate compared to non-reward conditions [reward main effect, F(1,21) = 5.99, p < 0.05] although PTSD subjects showed smaller and less consistent changes than did the comparison group [diagnosis × reward interaction, F(1,21) = 4.29, p = 0.05]. Skin conductance showed a similar pattern with the comparison group exhibiting marked increases during performance under reward contingencies and PTSD subjects showing little change [Fig. 4, diagnosis × reward interaction, F(1,21) = 10.44, p < 0.01]. These differences are unrelated to any change in baseline physiological levels since they were used as covariates in the analysis. 4. Discussion
Fig. 3. Estimated marginal means (±S.E.M.) for heart rate in PTSD (■) and traumatized control (O) subjects. The Stop-Signal Task was performed with ($) and without (No $) monetary reward.
The main finding of this study is that PTSD subjects did not show the physiological changes expected to accompany behavioral activation or inhibition. On the other hand, the traumatized comparison subjects' physiological responses were consistent with Fowles' (1980, 1988) hypotheses. During acquisition of the Simple Choice Reaction Time Task (Session 1), subjects were required to produce active behaviors but were not exposed to inhibitory signals. The comparison subjects, but not the PTSD subjects, showed the expected variability in heart rate and stable skin conductance. When stop-signals were added in Session 2, the comparison subjects, but not the PTSD subjects, showed the increases in skin conductance expected to accompany the increased inhibitory demands. In Sessions 3–5,
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
behavioral activation was manipulated using monetary rewards. Again, comparison subjects showed the increases in heart rate accompanying the reward-induced behavioral activation predicted by Fowles, while PTSD subjects showed little change. The lack of physiological responsiveness of PTSD subjects to the behavioral demands of the Stop-Signal Task stands in stark contrast to numerous studies showing increased heart rate and skin conductance reactivity to trauma-related stimuli (Casada et al., 1998; Pitman et al., 1990) and normal responsiveness to non-trauma-related stimuli (Blanchard et al., 1996, 1982; Gerardi et al., 1989; Malloy et al., 1983; McFall et al., 1990; Pallmeyer et al., 1986; Pitman et al., 1987). Physiological reactivity to trauma stimuli is the common pattern seen in PTSD (Casada et al., 1998; McDonagh-Coyle et al., 2001) and is hypothesized to be important to the pathophysiology of PTSD (Foa et al., 1989; Keane et al., 1985). On the other hand, our finding of reduced reactivity during the performance of an active task is consistent with studies showing decreased responsiveness during performance of mental arithmetic (Blanchard et al., 1989; Keane et al., 1998; McDonagh-Coyle et al., 2001). The lack of physiological response of our PTSD subjects also is in stark contrast to their behavioral responses to the Stop-Signal Task demands and reward contingencies (Casada and Roache, 2005). PTSD and comparison subjects showed very distinct behavioral activation during the reward contingency. In addition, compared to the comparison group, PTSD subjects showed marked reductions in behavioral inhibition during reward. While the physiological changes accompanying behavioral activation and inhibition in traumatized comparison subjects are consistent with Fowles' hypothesis, they may be interpreted in other ways as well. Increased heart rate during behavioral activation may be due to the increased physical demands of responding (Fowles, 1988) or may reflect general arousal (Stewart et al., 2001). Similarly, skin conductance is a sensitive indicator of nonspecific arousal (Casada et al., 1998) and may be unrelated to behavioral inhibition. Nevertheless, we believe that the physiological changes observed in comparison subjects reflect, at least in part, the physiological activity of behavioral activating and inhibiting neuronal systems. The heart rate changes observed in comparison subjects are unlikely to be due to changes in physical response demands since the motor task performed with and without reward was unchanged. Interpretation of the skin conductance increases in comparison subjects is less certain since this study did not independently control the motivation to inhibit behavior. We would expect increased behavioral inhibition as subjects acquire new inhibitory behaviors (Session 2) or strive to maintain inhibition in the face of increased motivation to produce responses (reward condition in Sessions 3–5). Therefore, the increased skin conductance of comparison subjects observed under these conditions is consistent with Fowles' hypothesis. Still, these conditions also would be expected to increase nonspecific arousal. Nevertheless, regardless of how the physiological changes are interpreted, it is noteworthy that PTSD subjects failed to show these changes despite producing the expected behavioral responses.
247
There are several possible explanations for the decreased responsiveness observed in PTSD subjects. First, PTSD subjects may appraise the Stop-Signal Task differently than the comparison subjects. Tomaka et al. (1993) found that subjects who appraised an active task as a threat showed less cardiovascular reactivity than subjects who appraised it as a challenge. Second, PTSD subjects may limit physiologic arousal as a means of controlling negative emotion. This is similar to elements of somatoform dissociation described by Nijenhuis et al. (2004) and may represent a physiological counterpart of emotional numbing. It also is consistent with several findings in which PTSD subjects were found to be less responsive than comparison subjects or other anxiety disorder subjects to a variety of stressors (Cuthbert et al., 2003; Orr et al., 1998). Overall, our findings suggest that, while PTSD subjects have intact behavioral activating and inhibiting systems, they do not display the associated physiological changes hypothesized by Fowles and observed in comparison subjects. This evidence is consistent with clinically described decreases in emotional expression in PTSD. Thus, we conclude that PTSD and comparison subjects differ in their physiological and emotion responses to stimuli even when their behavior is similar. The results of this study should be interpreted with care due to the small sample size and prevalent depressive comorbidity in the PTSD group. Further research is required to define the neuroanatomical and neurochemical systems controlling the suppression of autonomic responses to non-trauma-related, active tasks in PTSD subjects. Additional clinical research may also help clarify how the physiological changes accompanying PTSD affect long-term health and functioning. Acknowledgements This research was supported by an Institutional Research Grant from the University of Texas Health Science Center at San Antonio and by the Frederic C. Bartter General Clinical Research Center. Preparation of the manuscript was supported by National Institute on Drug Abuse Award K08 DA00507 to John Casada. References American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Press, Washington, DC. Beck, A.T., Steer, R.A., Brown, G.K., 1986. Beck Depression Inventory– Second Edition Manual, Psychological Corporation, Harcourt, Brace, San Antonio, TX. Bernstein, E.M., Putnam, F.W., 1986. Development, reliability, and validity of a dissociation scale. J. Nerv. Ment. Dis. 174 (12), 727–735. Blake, D.D., Weathers, F.W., Nagy, L.M., Kaloupek, D.G., Charney, D.S., Keane, T.M., 1997. Clinician-Administered PTSD Scale for DSM-IV: Current and Lifetime Version. National Center for PTSD. Blanchard, E.B., Hickling, E.J., Buckley, T.C., Taylor, E., Vollmer, A., Loos, W.R., 1996. Psychophysiology of posttraumatic stress disorder related to motor vehicle accidents: replication and extension. J. Consult. Clin. Psychol. 64 (4), 742–751. Blanchard, E.B., Kolb, L.C., Pallmeyer, T.P., Gerardi, R.J., 1982. A psychophysiological study of post traumatic stress disorder in Vietnam veterans. Psychiatr. Q. 54 (4), 220–229.
248
J.H. Casada, J.D. Roache / International Journal of Psychophysiology 62 (2006) 243–248
Blanchard, E.B., Kolb, L.C., Taylor, A.E., Wittrock, D.A., 1989. Cardiac response to relevant stimuli an adjunct in diagnosing posttraumatic stress disorder: replication and extension. Behav. Ther. 535–543. Casada, J.H., Amdur, R., Larsen, R., Liberzon, I., 1998. Psychophysiologic responsivity in posttraumatic stress disorder: generalized hyperresponsiveness versus trauma specificity. Biol. Psychiatry 44, 1037–1044. Casada, J.H., Roache, J.D., 2005. Behavioral inhibition and activation in posttraumatic stress disorder. J. Nerv. Ment. Dis. 193 (2), 102–109. Cloninger, C.R., 1989. The Tridimensional Personality Questionnaire. Department of Psychiatry and Genetics. Washington University School of Medicine, St. Louis, MO. Cuthbert, B.N., Lang, P.J., Strauss, C., Drobes, D., Patrick, C.J., Bradley, M.M., 2003. The psychophysiology of anxiety disorder: fear memory imagery. Psychophysiology 40 (3), 407–422. Dutton, D.G., 1995. Trauma symptoms and PTSD-like profiles in perpetrators of intimate abuse. J. Trauma Stress 8, 299–316. Foa, E.B., Steketee, G.S., Rothbaum, B.O., 1989. Behavioral/cognitive conceptualizations of posttraumatic stress disorder. Behav. Ther. 20, 229–243. Fowles, D.C., 1980. The three arousal model: implications of gray's two-factor learning theory for heart rate, electrodermal activity, and psychopathy. Psychophysiology 17 (2), 87–104. Fowles, D.C., 1988. Psychophysiology and psychopathology: a motivational approach. Psychophysiology 25 (4), 373–391. Fowles, D.C., Fisher, A.E., Tranel, D.T., 1982. The heart beats to reward: the effect of monetary incentive on heart rate. Psychophysiology 19 (5), 506–513. Gerardi, R.J., Blanchard, E.B., Kolb, L.C., 1989. Ability of Vietnam veterans to dissimulate a psychophysiological assessment for posttraumatic stress disorder. Behav. Ther. 20, 229–243. Gray, J.A., 1978. The neuropsychology of anxiety. Br. J. Psychol. 69, 417–434. Horowitz, M., Wilner, N., Alvarez, W., 1979. Impact of Events Scale: a measure of subjective stress. Psychosom. Med. 41, 209–218. Keane, T.M., Kolb, L.C., Kaloupek, D.G., Orr, S.P., Blanchard, E.B., Thomas, R.G., Hseih, Y.F., Lavori, P.W., 1998. Results of a multisite clinical trial on the psychophysiological assessment of posttraumatic stress disorder. J. Consult. Clin. Psychol. 66, 914–923. Keane, T.M., Zimering, R.T., Caddell, J.M., 1985. A behavioral formulation of posttraumatic stress disorder in Vietnam veterans. Behav. Ther. 8 (1), 9–12. King, D.W., King, L.A., Foy, D.W., Gudanowski, D.M., 1996. Prewar factors in combat-related posttraumatic stress disorder: structural equation modeling with a national sample of female and male Vietnam veterans. J. Consult. Clin. Psychol. 64, 520–531.
Logan, G.D., Cowan, W.B., 1984. On the ability to inhibit thought and action: a theory of an act of control. Psychol. Rev. 91, 295–327. Malloy, P.F., Fairbank, J.A., Keane, T.M., 1983. Validation of a multimethod assessment of posttraumatic stress disorders in Vietnam veterans. J. Consult. Clin. Psychol. 51 (4), 488–494. McDonagh-Coyle, A., McHugo, G.J., Friedman, M.J., Schnurr, P.P., Zayfert, C., Descamps, M., 2001. Psychophysiological reactivity in female sexual abuse survivors. J. Trauma Stress 14 (4), 667–683. McFall, M.E., Murburg, M.M., Ko, G.N., Veith, R.C., 1990. Autonomic responses to stress in Vietnam combat veterans with posttraumatic stress disorder. Biol. Psychiatry 27 (10), 1165–1175. Munley, P.H., Bains, D.S., Bloem, W.D., Busby, R.M., Pendziszewski, S., 1995. Posttraumatic stress disorder and the MCMI-II. Psychol. Rep. 76, 939–944. Nijenhuis, E.R.S., van der Hart, O., Kruger, K., Steele, K., 2004. Somatoform dissociation, reported abuse and animal defence-like reactions. Aust. N. Z. J. Psychiatry 38, 678–686. Orr, S.P., Meyerhoff, J.L., Edwards, J.V., Pitman, R.K., 1998. Heart rate and blood pressure resting levels and responses to generic stressors in Vietnam veterans with posttraumatic stress disorder. J. Trauma Stress 11 (1), 155–164. Pallmeyer, T.P., Blanchard, E.B., Kolb, L.C., 1986. The psychophysiology of combat-induced post-traumatic stress disorder in Vietnam veterans. Behav. Res. Ther. 24 (6), 645–652. Pitman, R.K., Orr, S.P., Forgue, D.F., Altman, B., de Jong, J.B., Herz, L.R., 1990. Psychophysiologic responses to combat imagery of Vietnam veterans with posttraumatic stress disorder versus other anxiety disorders. J. Abnorm. Psychology 99 (1), 49–54. Pitman, R.K., Orr, S.P., Forgue, D.F., de Jong, J.B., Claiborn, J.M., 1987. Psychophysiologic assessment of posttraumatic stress disorder imagery in Vietnam combat veterans. Arch. Gen. Psychiatry 44 (11), 970–975. Spielberger, C.D., Gorsuch, R.R., Luchene, R.E., 1970. State–Trait Anxiety Inventory. Consulting Psychologists Press, Palo Alto, CA. Stewart, S.H., Buffett-Jerrott, S.E., Kokaram, R., 2001. Heartbeat awareness and heart rate reactivity in anxiety sensitivity: a further investigation. J. Anxiety Disord. 15 (6), 535–553. Tomaka, J., Blascovich, J., Kelsey, R.M., Leitten, C.L., 1993. Subjective, physiological, and behavioral effects of threat and challenge appraisal. J. Pers. Soc. Psychol. 65, 248–260. Tranel, D.T., 1983. The effects of monetary incentive and frustrative nonreward on heart rate and electrodermal activity. Psychophysiology 20 (6), 652–657.