Psychological Bulletin 1992, Vol. 112, No. 2, 218-238

Copyright 1992 by the American Psychological Association, Inc. 0033-2909/92/$3.00

Uncontrollability and Unpredictability in Post-Traumatic Stress Disorder: An Animal Model Edna B. Foa

Richard Zinbarg

Department of Psychiatry Medical College of Pennsylvania at Eastern Pennsylvania Psychiatric Institute

Phobia and Anxiety Disorders Clinic University at Albany State University of New \brk

Barbara Olasov Rothbaum Department of Psychiatry Medical College of Pennsylvania at Eastern Pennsylvania Psychiatric Institute The disturbances observed in animals subjected to unpredictable and uncontrollable aversive events resemble post-traumatic stress disorder (PTSD) symptoms and thus may constitute an animal model of this disorder. It is argued that the similarity between animals' symptoms and those of trauma victims may reflect common etiological factors. Relevant experiments in which animals exhibit generalized fear and arousal, discrete fear of a conditioned stimulus (CS), analgesia, and avoidance are reviewed with the view that these manifestations may be analogous to the PTSD symptom clusters of persistent arousal, reexperiencing, numbing, and avoidance, respectively. Finally, animal paradigms are suggested to test the validity of the model and specific hypotheses are derived from the animal literature regarding trauma variables that are predictive of particular PTSD symptom clusters.

Several authors (e.g., Kolb, 1987; van der Kolk, 1987; van der Kolk, Greenberg, Boyd, & Krystal, 1985) have noted that the behavioral disturbances observed in animals subjected to the various experimental neurosis paradigms (e.g., Gantt, 1944; Masserman, 1943; Pavlov, 1927; Wolpe, 1952) resemble posttraumatic stress disorder (PTSD) symptoms and, thus, may constitute an animal model of this disorder.' These disturbances include alternations between sudden outbursts of agitated behaviors, on the one hand, and a state of lethargy, passivity, and withdrawal, on the other (Mineka & Hendersen, 1985; Mineka & Kihlstrom, 1978). As is discussed below, some of these disturbances resemble features of other emotional disorders. However the entire syndrome is found only in PTSD sufferers. We propose that the similarity between the animals' symptoms and those of trauma victims reflects common etio-

logical factors. If so, the identification of which variables produce which disturbances in animals may serve to generate hypotheses about the development of PTSD in humans. In the present article, we will review the relevant animal experiments and discuss their relevance to PTSD sufferers. Obviously any animal model of human experience is limited to nonverbal observations. It follows that the subjective experience of symptoms such as flashbacks, nightmares, and intrusive recollections cannot be modeled in animals.2 \et, as noted by Mineka (1985), although animal models of anxiety disorders may not illuminate every feature or symptom of these disorders (at least in part because humans have cognitive capacities that are different from and often exceed those of even the highest nonhuman primates), they can and do illuminate many of the most prominent and cardinal features of the disorders, (p. 200) Following a similar argument, we suggest that the disturbances produced by experimental neurosis match enough of the features of PTSD in humans to be of heuristic value despite the inability of the model to directly address flashbacks and intrusive recollections. In 1980, PTSD was added to the Diagnostic and Statistical Manual of Mental Disorders (DSM-III; American Psychiatric Association, 1980) as an anxiety disorder that develops in response to a psychologically traumatic event outside the range of

Preparation of this article was supported by National Institute of Mental Health Grant MH42178-02 awarded to Edna B. Foa. We wish to thank Tim Brown, Anka Ehlers, Jennifer Jones, Jurgen Margraf, Richard McNally, William Mitchell, and Robert Rosellini for their helpful comments on drafts of this article. Our thanks are also extended to Susan Mineka, who contributed to this article through her many conversations with us. Finally, we would like to extend thanks to the reviewers for their helpful comments and constructive suggestions and to Beth Gershuny for editing the manuscript. Barbara Olasov Rothbaum is now at the Emory University School of Medicine, Atlanta, Georgia. Richard Zinbarg is now at the Department of Psychology, University of Oregon, Eugene, Oregon. Correspondence concerning this article should be addressed to Edna B. Foa, Department of Psychiatry, Medical College of Pennsylvania, Eastern Pennsylvania Psychiatric Institute, 3200 Henry Avenue, Philadelphia, Pennsylvania 19129.

1 Although Kolb (1987) and van der Kolk (1987) were instrumental in noting the relevance of experimental neurosis paradigms for PTSD, their arguments are brief and highly selective. 2 However, recent developments in animal cognitive psychophysiology may offer a methodology for studying the processes that may underlie these experiences.

218

AN ANIMAL MODEL OF PTSD

normal human experience. Later, in the DSM-III-R (American Psychiatric Association, 1987), the denning symptoms were classified into three categories: increased arousal, reexperiencing, and persistent avoidance of stimuli associated with the trauma or numbing of general responsiveness. These criteria are listed in the Appendix. The DSM-III-R requires that a minimum of two symptoms of arousal be present for a PTSD diagnosis. This criterion was validated in crime victims in a study by Kilpatrick and Resnick (1989). Ninety-one percent of rape victims (Resnick, Veronen, Saunders, Kilpatrick, & Cornelison, 1989) and 71% of victims of nonsexual assault (Kilpatrick et al, 1989) reported at least two arousal symptoms. Green (1989) noted that arousal symptoms were quite common in victims of environmental disasters as well. For example, 65% of victims experienced sleep disturbances after the Ramada jet crash (Smith & North, 1988). Heightened tonic physiological arousal has been repeatedly found in PTSD sufferers. Vietnam veterans with PTSD and people living within 5 miles of the Three Mile Island Nuclear Power Station showed elevated baseline levels of heart rate and blood pressure compared with controls (Blanchard, 1990; Blanchard, Kolb, Gerardi, Ryan, & Pallmeyer, 1986; Blanchard, Kolb, Pallmeyer, & Gerardi, 1982; Davidson & Baum, 1986). This elevated autonomic arousal may either indicate that trauma causes increased arousal or that people with high tonic autonomic responses are more susceptible to develop PTSD. To explore these alternative hypotheses, Pitman and his colleagues (Pitman, Orr, Forgue, Altaian, & Herz, 1990; Pitman, Orr, Forgue, deJong, & Claiborn, 1987) examined military records of inductees' pulse rates and blood pressure before combat activity and related it to their later PTSD status. Veterans who later developed PTSD were not more aroused before their traumatic combat events than those who did not develop the disorder, suggesting that the high autonomic arousal is a consequence of the trauma rather than an individual susceptibility for PTSD. The second category of symptoms, reexperiencing, seems to be prominent in nearly all PTSD sufferers. Among rape victims (Resnick et al, 1989) and mixed crime and trauma victims (Kilpatrick et al., 1989), a higher percentage of subjects met the DSM-III-R reexperiencing criteria for PTSD than any other symptom category. Reexperiencing symptoms are also prominent among disaster victims (Green, 1989). Nightmares, recurrent recollections of the event, and worsening of problems on being reminded of the event are commonly reported symptoms. Further support for the reexperiencing symptoms in PTSD comes from laboratory experiments examining psychophysiological responses after exposure to trauma-related cues. PTSD Vietnam veterans showed autonomic hyperreactivity to combat-related audiovisual stimuli as compared with nonPTSD controls (Blanchard, 1990; Blanchard, Kolb, Gerardi, et al., 1986; Blanchard, Kolb, Pallmeyer, & Gerardi, 1982; Malloy, Fairbank, & Keane, 1983; Pallmeyer, Blanchard, & Kolb, 1986; Pitman, 1989; Pitman et al., 1987). The specificity of this hyperresponsivity to traumatic material has been demonstrated by Pitman et al. (1987). Vietnam combat veterans with PTSD were more reactive than nonPTSD combat veteran controls, on skin conductance and forehead electromyograph (EMG), to imagery of their combat experiences but not to other non-PTSD-related stressful imagery

219

(Pitman et al., 1987). Moreover, combat veterans who suffered from anxiety disorders other than PTSD were not hyperresponsive to their combat imagery (Pitman, van der Kolk, Orr, & Greenberg, 1990). Conditioned endocrinological responses in Vietnam veterans with PTSD have also been found. PTSD sufferers responded to a combat film with greater levels of arterialized plasma epinephrine than control subjects (McFall, Murburg, Ko, & Veith, 1991; cited in Pitman, 1989). The third category, persistent avoidance, includes two types of symptoms: (a) avoidance of situations or thoughts, or both, associated with the trauma and (b) avoidance of emotional engagement with events and people (i.e, numbing). Because these two types of avoidance may represent different mechanisms, we address them separately. Avoidance of thoughts and activities related to the trauma is frequently observed in PTSD sufferers. Avoidance of thoughts and feelings was evidenced in 64% of rape victims, 65% of crime victims, and 52% of disaster victims (Rothbaum, Foa, Riggs, Murdock, & Walsh, in press). Avoidance of activities or situations was found in 61 % of rape victims and 45% of crime victims (Kilpatrick & Resnick, 1989) and 40% of disaster victims (Green, 1989). Numbing of general responsiveness is one of the characteristics that distinguishes PTSD from other anxiety disorders. The definition of numbing is more vague than that of avoidance. Detachment from others, constricted affect, and decreased interest in activities are taken to be signs of emotional numbing and have been found highly prevalent in rape and crime victims but less so in disaster victims. Detachment from others, for example, was reported in 70% of rape victims, in 40% of crime victims (Kilpatrick & Resnick, 1989), and in 26% of disaster victims (Green, 1989). Further evidence for the presence of numbing in PTSD sufferers comes from the investigation of PTSD and dissociation, a phenomenon that is commonly considered an indicator of emotional numbing. Indeed, PTSD sufferers scored significantly higher on a measure of dissociation (Dissociative Experiences Scale) than did other anxiety-disordered people (Bernstein & Putnam, 1986). Similarly, dissociation was found to be correlated with a variety of PTSD measures in Vietnam veterans (Marmar & Freeman, 1988). The important role of dissociative symptoms in defining PTSD is demonstrated by the finding that dissociation at the time of an environmental disaster was a stronger predictor of PTSD than were objective trauma variables (Holen, 1988). Another possible manifestation of numbing is analgesia. Evidence of stress-induced analgesia has been found in PTSD sufferers. Vietnam veterans with PTSD displayed a decrease in pain sensitivity after being exposed to audiovisual combat stimuli, as opposed to non-PTSD combat veterans, who showed no such decrease (Pitman, van der Kolk, Orr, & Greenberg, 1990; van der Kolk, Pitman, & Orr, 1989). The placement of PTSD among the anxiety disorders reflects the recognition that it shares some features with the other anxiety disorders. For example, symptoms of heightened arousal and hypervigilance are also found in generalized anxiety disorder (GAD), and fear and avoidance are shared with simple phobia, social phobia, and agoraphobia. However, as noted by Horowitz (1986), PTSD is characterized by two extremes of conscious experience: episodes of intrusion and episodes of avoidance or denial. A similar view was expressed by

220

E. FOA, R. ZINBARG, AND B. ROTHBAUM

van der Kolk (1987), who asserted that a hallmark feature of PTSD is a biphasic "reliving and denial, with alternating intrusive and numbing responses" (p. 3). This alternation of numbing and reexperiencing has been noticed in victims of combat trauma, rape, kidnapping, incest, accidents, concentration camp experiences, and natural disasters (van der Kolk, 1987). MacLeod, Mathews, and their associates have found an initial, automatic vigilance toward threatening information (MacLeod, Mathews, & Tata, 1986; MacLeod & Rutherford, 1990; Mathews, Mogg, May, & Eysenck, 1989) followed by a strategic effort to avoid elaborative processing of that information among GAD patients (MacLeod & Rutherford, 1990; Mathews et al., 1989; Mogg, Mathews, & Weinman, 1987). Perhaps a conflict between the tendency to allocate attention toward threat information and the tendency toward cognitive avoidance of elaborative processing of such information characterizes all the anxiety disorders, but these disorders may differ in terms of the pervasiveness or strength of these tendencies. In simple phobics, for example, this conflict is elicited by only a limited number of threat cues. Although the conflict between heightened arousal and hypervigilance on the one hand and avoidance on the other appears to be shared by all the anxiety disorders including PTSD, PTSD is distinguished from the other anxiety disorders by the alternation between reexperiencing and numbing symptoms (Krystal, 1990; van der Kolk, 1987). Some students of PTSD believe flashbacks, intrusive recollections, and nightmares to be the hallmark symptoms of PTSD. Indeed, the DSM-HI-R (American Psychiatric Association, 1987) lists four symptoms under the reexperiencing category (see Table 1). However, it must be remembered that only one of these four symptoms is required for the diagnosis of PTSD in contrast to three symptoms of avoidance and numbing and two symptoms of increased arousal. One of the four DSM-III-R reexperiencing symptoms is "intense psychological distress at exposure to events that symbolize or resemble an aspect of the traumatic event" (American Psychiatric Association, 1987, p. 250). Thus, although flashbacks, intrusive recollections, and nightmares are commonly observed in PTSD sufferers, they are not necessary for the diagnosis. In fact, Kilpatrick and Resnick (in press) found that among crime victims, nightmares and flashbacks were the symptoms least likely to be present among those with a diagnosis of PTSD (sensitivities of .48 and .44 respectively), whereas avoidance of exposure to events that symbolize or resemble the trauma had higher sensitivity (.73) as did emotional numbing (.85). Moreover, Keane (in press) conducted a principle-components analysis of the Mississippi Scale for Combat-Related PTSD (Keane, Malloy, & Fairbank, 1984) and found that distress at exposure to events reminiscent of the trauma loaded highly on a reexperiencing factor that also included intrusive thoughts and nightmares. These results suggest that the symptom of distress at exposure to reminiscent events is central to the construct of reexperiencing. In considering the etiology of PTSD, it is important to note that traumas differ in their likelihood to produce PTSD, and individuals differ with respect to their likelihood of developing the disorder. In this article, we primarily focus on trauma variables that may be predictive of PTSD. The DSM-III-R states that the event must be "outside the range of usual human experi-

ence and . . . markedly distressing to almost anyone" (American Psychiatric Association, 1987, p. 250). Examples provided in the manual suggest that the event should be perceived as threatening to one's physical integrity or pose a serious threat to significant others. Most studies reveal that the likelihood of developing PTSD is directly proportional to the severity of the stressor. Several studies found bodily injury to be related to PTSD (Foy, Sipprelle, Rueger, & Carroll, 1984; Helzer, Robins, & McEvoy, 1987; Kilpatrick et al., 1989; Pitman, Altman, & Macklin, 1989; Speed, Engdahl, Schwartz, & Eberly, 1989), but rape was found to be a stronger predictor than injury (Kilpatrick et al., 1989). Severity of the stressor is influenced not only by the actual traumatic events but also by one's subjective perception of threat. Indeed, Kilpatrick et al. (1989) found that PTSD frequency in crime victims was more than doubled if either injury or perceived life threat were present, and incidence was almost fourfold if both were present. Although injury and perception of danger increase the prevalence of PTSD, studies of civilians in war zones report surprisingly low incidence of this disorder (Rachman, 1989; Saigh, 1988). The discrepancy between the two areas of research indicates that exposure to life threat is not sufficient to cause PTSD. To generate hypotheses about specific trauma variables that are likely to produce PTSD, we will discuss relevant animal paradigms. Before discussing the similarities between experimental neurosis and PTSD symptoms, it is important to realize that the term experimental neurosis is used to describe a wide range of procedures that, at first glance, appear to differ considerably from one another (e.g., Gantt, 1944; Masserman, 1943; Pavlov, 1927; Wolpe, 1952). However, as noted by several authors (e.g., Maier & Seligman, 1976; Mineka & Kihlstrom, 1978), one can identify a common element among these various procedures. Mineka and Kihlstrom (1978) stated that "in each case, environmental events of vital importance to the organism become unpredictable, uncontrollable or both" (p. 257). Because of this commonality, we do not discuss each of the various experimental neurosis paradigms separately. Rather, we focus on (a) Masserman's (1943) observations because his procedures are the most clearly relevant to human PTSD and (b) the literature involving the systematic manipulation of predictability and controllability because these two variables appear to be central in mediating the effects of the various experimental neurosis procedures. In Masserman's (1943) experiments, cats were trained to associate a particular stimulus with the presentation of food. After the cats learned to approach the food box in the presence of this stimulus, some of them received punishment in the form of either an aversive blast of air or electric shock. These cats showed a variety of behavioral disturbances including strong fear and defensive responses, restlessness and agitation, phobic responses to food, trembling, and rapid and irregular pulse and respiration, as well as passivity and withdrawal. Masserman (1971) later interpreted these disturbances as resulting when "the organism apprehends a failure to predict and control events important to its welfare" (p. 9). More recent paradigms have demonstrated that uncontrollable, unpredictable aversive stimulation also produced analgesia (e.g., Maier, Drugan, &

AN ANIMAL MODEL OF PTSD Grau, 1982) and altered patterns of avoidance behavior (e.g., Rush, Mineka, & Suomi, 1982). Several parallels are apparent between Masserman's (1943) procedures and the uncontrollable, unpredictable shock paradigms on the one hand and PTSD on the other. First, as noted earlier, there are phenotypic similarities between many of the disturbances observed in these animals and PTSD symptoms. Most obvious is the heightened generalized fear and arousal that is characteristic of both. Indexes of increased arousal commonly observed among PTSD sufferers include symptoms both of disturbed functioning such as difficulty sleeping and elevated heart rate and blood pressure and of generalized fear such as hypervigilance and exaggerated startle. It seems reasonable to argue that these general disturbances are analogous to the general disturbances of functioning frequently exhibited by animals exposed to uncontrollable, unpredictable shock, such as ulcers and weight loss, and to indexes of heightened contextual fear, such as freezing and suppression of appetitive behavior when placed in the experimental context where shock was delivered. Likewise, some of the avoidance behaviors (heightened passive avoidance) displayed by animals seem to be analogous to the avoidance symptoms exhibited by PTSD sufferers. In addition, the stress-induced analgesia (Maier & Keith, 1987; Moye, Hyson, Grau, & Maier, 1983) observed in animals exposed to uncontrollable, unpredictable shock may be analogous to the numbing often seen in PTSD sufferers. Indeed, both stress-induced analgesia and PTSD numbing appear to be phasic responses evoked by trauma-related stress. More problematic are those symptoms of reexperiencing that rely on self-report, that is, flashbacks and intrusive recollections, and that, therefore, cannot be directly measured in animals. However, as discussed earlier, the symptom of "intense psychological distress at exposure to events that symbolize or resemble an aspect of the traumatic event" (American Psychiatric Association, 1987, p. 250) is central to the construct of reexperiencing and is not necessarily dependent on self-report. Moreover, many contemporary conditioning theorists would consider the description of the reexperiencing symptom mentioned above to be an adequate definition of a conditioned fear response. Therefore, we propose that a conditioned fear response is analogous to this symptom and therefore can model important aspects of the construct of reexperiencing. It is important to note that we are not proposing that reexperiencing of a traumatic event is always preceded by a discrete conditioned stimulus (CS). Rather, we propose that the mechanism that underlies conditioned fear is similar to one of the crucial processes that underlie the reexperiencing symptoms. In both instances, the underlying mechanism may be seen as the activation of a fear memory. As noted above, the drawing of this parallel between the mechanisms underlying fear conditioning and PTSD reexperiencing symptoms is consistent with contemporary conceptualizations of classical conditioning paradigms in animals and humans (Grossberg, 1982; Konorski, 1967; Ohman, 1979,1986; Rescorla, 1988; Wagner, 1979,1981). Wagner's (1979,1981) model is of particular relevance here because it emphasizes the role of memorial processes in animal conditioning and has received considerable empirical support. He suggests that the strength of the connection from the CS representation to the unconditioned stimulus (US) representa-

221

tion grows as a result of joint rehearsal in a limited-capacity, short-term (or active) memory mechanism. Repeated trials, which produce joint rehearsal, result in the ability of the presentation of the CS to elicit "associatedly generated priming" of the US representation in short-term memory (see Wagner, 1979, 1981, for detailed explications of this model and for reviews of the evidence bearing on it). Adopting Wagner's interpretive framework suggests that a conditioned fear response is a sign that the animal is reprocessing or reexperiencing the US. In addition to similarity of symptoms, a second parallel between Masserman's (1943) paradigms and PTSD is the seeming etiological similarity of an association between aversive consequences and a stimulus or a response that previously had appetitive meaning. For example, in Masserman's (1943) experiments, cats received aversive stimulation contingent on actions that previously had led to food rewards. This paradigm may be analogous to child abuse situations in which parents repeatedly shift between being sources of reward and sources of pain. It may also parallel a rape situation, in which sex, which is usually associated with pleasure and gratification, becomes paired with violence. A third parallel is that the persistent course of the symptoms observed by Masserman (1943) parallels the chronicity of untreated PTSD symptoms. Masserman (1943) noted that these disturbances were markedly persistent, often lasting for many months without further aversive stimulation. These important similarities regarding symptoms, etiology, and developmental course suggest that the uncontrollable and unpredictable shock paradigm may provide a useful model for understanding PTSD in humans as well as for understanding some aspects of other disorders of emotions. In the remainder of this article, we focus on the relevance of uncontrollable, unpredictable aversive stimulation as a model of PTSD. However, given the overlap between PTSD and the other anxiety disorders discussed above, the animal model of PTSD presented here may also be relevant to those features of other anxiety disorders that are shared with PTSD. It is important to note that in addition to the overlap that exists among the anxiety disorders, there is also substantial overlap between depression and anxiety (e.g., Clark & Watson, 1991; Foa & Foa, 1982; Kendall & Watson, 1989; Tellegen, 1985). Indeed, many PTSD symptoms, such as decreased interest in activities, difficulty concentrating, and sleep disturbances, are also common symptoms of depression. Therefore, the animal model presented here may also be relevant to those features of depression that are shared with PTSD. Thus, particular aspects of the uncontrollable, unpredictable aversive stimulation model may shed light on variables relevant to the core features of the full spectrum of disturbances of negative affect (i.e., anxiety and depressive disorders). However, because the entire syndrome produced by uncontrollable, unpredictable aversive stimulation appears to most closely resemble the PTSD syndrome, we propose that this model is most relevant for the study of PTSD.

Uncontrollability and Unpredictability As noted above, several theorists have proposed that the factors common across the various experimental neurosis procedures are Uncontrollability and unpredictability of the aversive

222

E. FOA, R. ZINBARG, AND B. ROTHBAUM

stimulus (e.g., Masserman, 1971; Mineka & Kihlstrom, 1978; Seligman, 1975). Given the parallels between PTSD and the disturbed behaviors produced by experimental neurosis procedures such as those used by Masserman, these factors may be important in the etiology of PTSD in humans. Therefore, we will now review the animal literature on uncontrollable and unpredictable aversive events with the specific aim of generating hypotheses regarding the etiology and nature of PTSD. Before discussing the animal literature, it is helpful to define what is usually meant by the terms uncontrollability and unpredictability (for a more technical discussion of uncontrollability and unpredictability, see Mineka & Kihlstrom, 1978). Controllability is defined in terms of the probability that a given response will prevent or terminate the US. An uncontrollable shock, as is administered in a typical Pavlovian paradigm, is one for which the probability of its onset and offset is unrelated to the organism's responses. Thus, an unescapable shock is one that can neither be escaped nor avoided. Accordingly, instrumental procedures such as escape or avoidance training are seen as involving the administration of controllable shock. In a similar fashion, predictability is defined in terms of the probability of the onset or termination of the US given the presence or absence of a given signal. An unpredictable shock is one for which the probability of its occurrence is the same regardless of the events preceding it. Here, it is important to keep in mind the distinction between danger unpredictability and safety unpredictability that is often drawn in the learning literature (Mackintosh, 1983; Rescorla & Wagner, 1972; Wagner & Rescorla, 1972). That is, certain procedures are known to produce conditioned exciters of fear (danger predictability), whereas other procedures produce conditioned inhibitors of fear (safety predictability). Thus, danger unpredictability is denned by the lack of a signal that predicts the onset of the US more reliably than the experimental context itself. Safety unpredictability is defined by the lack of a signal that reliably predicts the termination or absence of the US. It is clear that danger and safety predictability are empirically independent of each other because a procedure that produces a strong fear excitor may not produce a strong fear inhibitor. For example, in a typical Pavlovian fear-conditioning procedure, the context, which reliably predicts safety when presented alone, does not usually become a strong inhibitor of fear even though the CS becomes a strong excitor of fear. In fact, to produce a strong inhibitor of fear, one typically either has to arrange a negative correlation between the signal and the US or has to present the signal in a nonreinforced compound with an excitor of fear (Mackintosh, 1983; Wagner & Rescorla, 1972). In other words, signals become fear inhibitors to the extent that they predict the nonoccurrence of an otherwise expected shock. Because the two types of predictability often produce very different effects, we follow this distinction in our review of the literature.3 Note that the understanding of the effects of uncontrollability and unpredictability has been complicated by several issues. Perhaps the greatest obstacles to a theoretical analysis of these effects are the overlap between these two constructs and the possibility that controllability and predictability may not be unidimensional constructs (Miller, 1981; Miller & Grant, J979).

Several theorists have noted that uncontrollability and unpredictability are not conceptually independent of each other (e.g., Averill, 1973; Masserman, 1943; Mineka & Hendersen, 1985; Mineka & Kihlstrom, 1978). An organism that controls the termination of an event ipso facto can predict when that event will terminate. Similarly, an organism that controls the onset of an event can predict whether that event will occur. On the surface, it would appear that the converse is not true; predictable events are not necessarily controllable. However, some theorists argue that a signal that predicts the occurrence of an event allows the organism to emit responses that alter its impact. These preparatory responses may be construed as providing control over the perceived intensity of the event (Cantor, 1981; Dinsmoor, 1983; Perkins, 1968,1971). The overlap between controllability and predictability has made it difficult to discern which of the diverse effects of experimental neurosis are due to which factor. Backward conditioning procedures have been used to disentangle the effects of controllability from those of predictability. A typical experiment (e.g., Mineka, Cook, & Miller, 1984) includes three groups of subjects. One group, designated the master group, can escape and avoid shock. A second group, the yoked-feedback group, receives the same number, intensity, and duration of shocks as the master group but receives some form of an external feedback signal concurrent with shock offset. Thus, the yoked-feedback group has no control over shock onset or offset but is able to predict the occurrence of shock-free intervals on the basis of the feedback signal. A third group is also yoked to the master group but does not receive feedback signals concurrent with shock offset. Hence this third group is typically labeled the yoked-no-feedback group and has neither control over shock onset or offset nor environmental cues that reliably predict shock-free intervals. Two pairwise comparisons are crucial in teasing apart the effects of controllability from predictability in backward conditioning paradigms demonstrating greater behavioral disturbances among the yoked-no-feedback group than the master group. The first is a comparison between the two yoked groups; the second is the comparison between the yoked-feedback group and the master group. When the yoked-feedback group displays less disturbances than the yoked-no-feedback group but is roughly equivalent to the master group, the differences between the master and yoked-no-feedback group are interpreted as being mediated entirely by the predictability that an escape or avoidance response provides.4 When the yoked-feedback group is less disturbed than the yoked-no-feedback group but more disturbed than the master group, the differences between the master and yoked-no-feedback group have often

3 It has been suggested that there may be several dimensions of controllability including onset controllability, severity controllability, and termination controllability (Minor, Dess, & Overmier, 1989). Unfortunately, most research has not made these distinctions, and thus it is not possible at present to determine whether these different types of control produce different effects. 4 Note that the comparison between the yoked-feedback and yoked-no-feedback groups allows one to rule out Church's (1964) individual differences in stressfulness argument.

AN ANIMAL MODEL OF PTSD been interpreted as being mediated, at least in part, by controllability per se. Note that the interpretation of differences between a master group and a yoked-feedback group is complicated by the fact that an escape or avoidance response provides information regarding shock termination as well as information regarding the beginning of a shock-free interval. In contrast, feedback stimuli presented concurrently with shock offset do not predict shock termination. Therefore, when the yoked-feedback group is less disturbed than the yoked-no-feedback group but more disturbed than the master group, there are at least two plausible explanations: Either the effect of an escape or avoidance response is at least partially mediated by controllability per se, or the crucial mediating variable is predictability of shock termination (Rosellini, Warren, & DeCola, 1987). In fact, Minor, Trauner, Lee, and Dess (1990) recently demonstrated that the prediction of shock termination is crucial to at least some of the stress-reducing effects of an escape response. Despite these complications, the backward conditioning paradigm allows us to disentangle the effects of controllability from those of unpredictability of a shock-free period. Our analysis of the different effects of uncontrollability and unpredictability (of a traumafree period) therefore focus on the results from studies using this paradigm. With respect to the issue of multidimensionality, stress-modulating variables often have different effects on different stress measures (Minor, Dess, & Overmier, 1989; Warren, Rosellini, & Maier, 1989). Accordingly, we present the effects of uncontrollability and unpredictability on several response systems analogous to the major PTSD symptom categories. Specifically, we discuss the effects of uncontrollability and unpredictability on generalized (contextual) fear and arousal, discrete fear of a CS, analgesia, and avoidance, which may be analogous to the PTSD symptom clusters of persistent arousal, reexperiencing, numbing, and avoidance, respectively.

Persistent Symptoms of Increased Arousal In the DSM-III-R (American Psychiatric Association, 1987), persistent symptoms of increased arousal include symptoms of both disturbed functioning (e.g., difficulty sleeping, irritability, decreased concentration) and generalized fear (e.g., exaggerated startle response, hypervigilance). Therefore, our review of the disturbances that appear analogous to the persistent arousal symptoms of PTSD sufferers focuses on measures of both disturbed functioning (ulceration, body temperature, weight loss) and generalized fear (contextual fear indexes such as freezing and suppression of appetitive behaviors). Effects of controllability. The early literature on the stressful effects of uncontrollability produced conflicting findings. Mowrer and Viek (1948) and Weiss (1968) reported that rats that could avoid or escape shocks showed less contextual fear than did rats that received uncontrollable shock. Conversely, Brady, Porter, Conrad, and Mason (1958) found that control increased generalized stress in monkeys. This apparent contradiction may reflect methodological differences between the studies. Weiss (1968) randomly assigned rats to either an avoidance-escape or a yoked group, whereas Brady et al. (1958) used a shock avoidance pretest and assigned the monkeys that re-

223

sponded at the highest rates on this pretest to the avoidance group. Moreover, Sines, Cleeland, and Adkins (1963) found that rats susceptible to ulcers learned an avoidance response faster than normal controls. Therefore, the results obtained by Brady et al. (1958) may have reflected the effects of individual differences in stress responsivity rather than the effect of controllability. More recent investigations have been consistent with the findings of Mowrer and Viek (1948) and Weiss (1968) in demonstrating that control reduces the effects of a stressor on contextual fear and generalized arousal (Brennan & Riccio, 1975; Mineka et al., 1984). These results may be taken as evidence supporting the hypothesis that uncontrollable shock leads to greater generalized fear than controllable shock. This effect seems to require extensive experience with the shock contingencies. Rosellini et al. (1987) found that escapable and inescapable shock lead to comparable levels of contextual fear after 20 trials. However, the escapable group displayed a decrease in fear from 20 to 80 trials, whereas an inescapable group showed the expected increase in fear over time. This implies that when the organism processes the information that it has control over the aversive stimulation, a mechanism is activated that inhibits generalization of fear to the context. Note also that Annau and Kamin (1961) found that weak uncontrollable shocks led to habituation of fear over time but that strong uncontrollable shocks did not. Taken together, these results give rise to the hypothesis that controllability is a more crucial determinant of the habituation of fear to strong shocks than to weak shocks. There is also some evidence to suggest that the loss of control is even more stressful than the lack of control (Mineka & Kihlstrom, 1978). For example, Weiss (197la) found that rats that received shock contingent on a well-learned avoidance response evidenced more severe stomach ulceration and higher corticosterone levels than did yoked rats that received noncontingent shock. Similarly, Tsuda and Hirai (1975) found that rats that originally received training to escape or avoid shock by pressing a lever just once and that were later required to make five or eight lever presses, respectively, to avoid or escape shock showed more extensive gastric lesions than their yoked counterparts. If it is reasoned that the transition from the simple requirement of a single lever press to the requirement of five or eight lever presses was perceived as a loss of control by the subjects, then these results are consistent with those of Weiss (1971b). That is, they suggest that the loss of control leads to even greater levels of arousal than the lack of control. Further support for this notion was reported by Hanson, Larson, and Snowdon (1976), who found that when a lever that had previously controlled loud noise was removed, monkeys showed greater elevations in cortisol levels than did monkeys that never had control over the noise. There is some converging evidence from human subjects that the loss of control leads to greater fear and arousal than the lack of control (Staub, Tursky, & Schwartz, 1971). Two conclusions seem warranted regarding the effect of uncontrollability on generalized fear and persistent arousal. First, uncontrollable shock leads to greater generalized fear and arousal than controllable shock, but the attenuating effect of control appears only after extensive experience. Second, the

224

E. FOA, R. ZINBARG, AND B. ROTHBAUM

loss of control may lead to even greater levels of generalized fear and arousal than does the lack of control. Effects of predictability. In one of the classic studies investigating the relationship between predictability and generalized fear and arousal, Seligman (1968) found that unpredictable shock led to more generalized fear and arousal than predictable shock. That is, unpredictable shock led to a continual freezing response and ulceration, but predictable shock did not. Similar results were reported by Weiss (1970), who found that rats that received unpredictable shock evidenced greater stomach ulceration, a greater rise in body temperature, higher plasma corticosterone levels, and greater weight loss than either a group receiving predictable shock or a nonshocked control group. Not only does unpredictable shock produce greater generalized fear and arousal than predictable shock, but organisms also show a preference for predictable over unpredictable shock (e.g, Badia & Culbertson, 1972,1974; Collier, 1977; Lockard, 1963). In an attempt to elucidate the mechanisms underlying this preference, Fanselow (1980) compared the preference for the context in which danger signals had been presented with that in which signals negatively correlated with shock had been presented. He found that danger signals led to greater preference for the context in which signals were presented than did the negatively correlated signals. Moreover, the negatively correlated signal context was even less preferred than was that associated with random signals. Furthermore, preference for the context in which the signal was presented was positively correlated with the degree of fear produced by the signal. These results suggest that the danger signals may block association between fear and the context, whereas the negatively correlated signals may block associations between safety and the context.5 In other words, animals presented with a reliable predictor of shock (danger signals) were able to discriminate between this predictor of shock and the context and thus did not become fearful of the context. In contrast, the negatively correlated signal group had no predictor of shock onset more reliable than the context itself and therefore showed increased fear of the context. By varying the degree of predictability, Odling-Smee (1975) was able to demonstrate more clearly the relationship between contextual fear, danger signals, and negatively correlated signals. The degree of contextual fear was inversely related to the probability of the CS being followed by the US. The four studies cited above all used only uncontrollable shocks. Therefore, it is impossible to determine whether the increased generalized fear demonstrated by animals lacking danger signals in these studies resulted from danger unpredictability alone or from its combination with uncontrollability. In an experiment designed to tease apart the effects of danger predictability from controllability, Weiss (1971 a) found that animals developed more ulceration in a no-signal (unpredictable) condition than when shock was signaled (predictable), regardless of whether the shock was controllable. However, unpredictable shock led to greater weight loss than predictable shock only when the shock was also uncontrollable. Thus, it appears that whether danger unpredictability per se or its combination with uncontrollability will produce generalized fear may depend on the particular measure of fear used. Perhaps autonomic nervous system responses, such as ulceration, are more influenced

by predictability, whereas voluntary responses, such as eating or licking for water, are more affected by controllability. With respect to safety signals, several investigators have reported results that seem to contradict those that Fanselow (1980) and Odling-Smee (1975) found for danger predictability. For example, Overmier, Murison, Skoglund, and Ursin (1985) found that animals given backward conditioned feedback signals developed less ulcers than animals given random toneshock pairings and animals that were not shocked. However, they also found that corticosterone levels were higher in the animals given backward conditioned feedback signals than in the other two groups. If ulceration and corticosterone levels are taken to be parallel measures of fear-stress, then these results seem to contradict each other. On the other hand, if corticosterone can be considered an index of nonspecific arousal or activation (as suggested by Overmier et al.), then these results may indicate that backward conditioned feedback signals reduce generalized fear but do not reduce nonspecific arousal, which may keep the animal prepared for action. Unambiguous evidence supporting the hypothesis that backward conditioned feedback signals reduce contextual fear was reported by Mineka et al. (1984) and by Maier and Keith (1987). A reduction of contextual fear by backward conditioned feedback signals was also reported by Rosellini et al. (1987), but only after extended training. This result parallels the finding that the effect of control on reducing contextual fear appears only after extended training and suggests that the effects of both control and predictability depend on the animals' recognition of the environmental contingencies. The apparent inconsistencies in the animal literature on the effects of backward conditioned feedback and negatively correlated signals on generalized fear may reflect procedural differences between the experiments. Odling-Smee (1975) used fewer training trials than Overmier et al. (1985), Mineka et al. (1984), or Rosellini et al. (1987). Given that conditioned inhibition is known to develop slowly (see Wagner & Rescorla, 1972), the apparently discrepant findings may be due to differences in the strength of the fear-inhibitory properties accruing to the feedback signals in each experiment. We propose that weak safety signals may compete with contextual cues for inhibitory strength, whereas strong safety signals produce counterconditioning or related fear-reducing mechanisms. Accordingly, we would predict that in the absence of danger signals that compete with contextual cues for excitatory strength, weak safety signals would produce an increase in contextual fear as found by Odling-Smee (1975). Conversely, strong safety signals would produce a decrease in contextual fear as found by Mineka et al. (1984) and Rosellini et al. (1987). Indeed, Rosellini et al. (1987) found that only those signals that acquired strong fear-inhibitory properties reduced contextual fear. In one study using humans, the pivotal role of controllability over safety predictability in reducing general fear and arousal (when the latter referred not to onset but to offset of the aversive event) was demonstrated by Geer and Maisel (1972). All sub5

Note, however, that Abbott (1985) failed to replicate Fanselow's (1980) findings.

AN ANIMAL MODEL OF PTSD jects viewed slides of dead bodies. Those who could escape by turning off the slide (i.e., had predictability and controllability of offset) showed less arousal before and during slide presentations than those who could only predict offset. In summary, the evidence regarding the relationships between unpredictability and generalized fear is more consistent for danger than safety unpredictability. At the very least, it can be concluded that danger unpredictability moderates the effect of uncontrollability in producing increased generalized fear. Moreover, Weiss's (197la) ulceration results indicate that at least for some response systems, danger unpredictability can directly produce increased generalized fear regardless of the degree of control. Fanselow's (1980) and Odling-Smee's (1975) findings suggest that when organisms are exposed to danger unpredictability, all the contextual stimuli are treated as predictors of shock by the organism, thereby leading to heightened levels of generalized fear. At present, the available evidence regarding the relationship between feedback signals and generalized fear does not permit firm conclusions. One speculation that may resolve the inconsistencies in this literature is that weak safety signals may lead to an increase in contextual fear, whereas strong safety signals may decrease contextual fear. However, this hypothesis was constructed to explain available data and has not been adequately tested. Given the inconsistencies in the results on feedback signals, it is difficult to determine whether the generalized fear and arousal produced by the lack of control is due to the lack of predictability of a shock-free period that control provides.

Reexperiencing Earlier, we argued that in the obvious absence of self-report data in animal experiments, we consider fear conditioned to a discrete signal to be analogous to the reexperiencing symptoms of PTSD. Measures of fear to a discrete signal are similar to those used to index contextual fear and include suppression of appetitive behavior and freezing. Effects of controllability. Several studies have found that a CS for inescapable shock produced greater fear than did a CS for escapable shock (Desiderato & Newman, 1971; Mineka et al., 1984; Osborne, Mattingly, Redmon, & Osborne, 1975). Further investigation of the effect of control on fear to a discrete CS has demonstrated that attenuation of fear appears only after extensive experience with control (Cook, Mineka, & Trumble, 1987; Starr & Mineka, 1977). A close examination of Cook et al.'s (1987) findings reveals that the differences between the effects of controllable and uncontrollable shock are due to a reduction of fear over time in the controllable condition rather than increased fear in the uncontrollable condition. The finding that controllable shock decreases fear to a discrete CS over time parallels Rosellini et al.'s (1987) results for contextual fear. Both studies demonstrated that fear reduction with controllable shock occurs over time, indicating that control exerts its effects through an active fear-inhibitory process. Even in the Rosellini et al. (1987) experiment where uncontrollable shock produced increased fear with extended training, the fear-excitatory process activated by uncontrollability was weak in relation to the fear-inhibitory process activated by control. This inter-

225

pretation has intuitive appeal, because it implies that organisms are equipped to respond to stressors with fear, but to decrease fear they must learn that they have control over the stressor. Extensive experience with control has been shown to reduce fear of discrete CSs and enhance discrimination between danger signals and similar stimuli (Brennan & Riccio, 1975). This result suggests that a failure of discrimination may account for the increased generalized fear produced by uncontrollable shocks. Brennan and Riccio (1975) also reported results suggesting that loss of control produces more fear of a discrete CS than lack of control. Rats given Pavlovian discrimination training after extensive experience with controllable shock displayed more fear to the danger signal than did yoked rats. This increased fear may have been due to the loss of control inherent in the shift from the escape contingency to the Pavlovian contingency. Evidence indicating that uncontrollable shock leads to greater fear of a CS than controllable shock in humans was reported by Szpiler and Epstein (1976). They found that a CS for unavoidable shock was associated with a greater number of nonspecific skin conductance responses than was a CS for avoidable shock. Furthermore, the groups that received unavoidable shock reported greater increase in anxiety after being informed that they would receive shocks than the group that received avoidable shock. In general, the effects of control on discrete fear to a CS are similar to those on generalized fear and arousal. Specifically, the following three conclusions may be drawn from the evidence reviewed above. First, inescapable shock produces greater conditioned fear to a CS than does escapable shock, but the fear-attenuating effects of control appear only after extensive experience. Second, loss of control may produce even greater conditioned fear to a CS than does lack of control. Third, the ability to discriminate a danger signal from similar stimuli is enhanced by extensive experience with controllable shock. Effects of predictability. The effects of previous experience with unpredictable, uncontrollable shock on the subsequent acquisition of conditioned fear to a discrete CS were examined by Seligman (1968). A group that previously had received unpredictable uncontrollable shock did not acquire fear to a CS as rapidly as a group without such experience. The finding that experience with uncontrollable, unpredictable shock retards subsequent acquisition of discrete fear has been replicated many times, using either unsignaled shock (Domjan & Best, 1977; Randich, 1981; Randich & LoLordo, 1979) or uncorrelated presentations of signals and shocks (Baker, 1976). However, it is impossible to determine from these experiments if this effect is due to uncontrollability, unpredictability, their combination, or to the effect of shock per se because these experiments did not include the control groups required for such a distinction. Results from a separate line of research suggest that neither experience with shock per se nor with uncontrollability per se are crucial in producing the decrement in subsequent acquisition of discrete fear. Preexposure to uncontrollable shocks that are reliably predicted by danger signals facilitates, rather than

226

E. FOA, R. ZINBARG, AND B. ROTHBAUM

retards, future acquisition of fear to a novel danger signal (Holt & Kehoe, 1985; Kehoe & Holt, 1984; Kehoe, Morrow, & Holt, 1984; Schreurs & Kehoe, 1987). These results suggest that the proactive interference of unpredictable, uncontrollable shocks with the acquisition of discrete fears can be attributable to either unpredictability per se or to the combination of unpredictability and uncontrollability. The proactive interference often found in animals with previous experience with uncontrollable, unpredictable shock may reflect an artifact in the manner that fear was measured in these experiments. Discrete fear in animals is typically measured by a suppression ratio, that is, the ratio of the amount of activity in the presence of the CS divided by the total amount of activity. Because greater freezing in the presence of the CS, given a fixed activity baseline, reduces the value of the suppression ratio, smaller values of a suppression ratio typically have been taken to indicate greater fear. However, note that increases in contextual fear can also lead to increases in the value of the suppression ratio (R. Rosellini, personal communication, March 29, 1991). In addition, the results of an elegant series of studies conducted by Hinson (1982) suggest that fear associated with the context as a result of preexposure to uncontrollable, unpredictable shock blocks subsequent fear conditioning to a discrete CS presented in that context. Hence, the proactive interference effect of unpredictable, uncontrollable shock may reflect their tendency to produce greater contextual fear. That is, it seems likely that animals pretrained with uncontrollable, unpredictable shock will show greater generalization of fear than either a naive group or a group pretrained with uncontrollable but predictable shock. The previous experiments were concerned exclusively with danger predictability. Starr and Mineka (1977) and Mineka et al. (1984) found that a yoked-no-feedback group demonstrated more fear during a danger signal than did either a master or a yoked-feedback group, which did not differ from each other. These results indicate that feedback signals mimic the effect of control in reducing fear to a danger signal. Further evidence for the crucial role of feedback signals in reduction of discrete fear was provided by Mineka et al. A master group that received feedback signals did not differ in their fear of a danger signal from a master group that did not receive feedback signals or a yoked group that received feedback signals. Mineka et al. concluded that controllability added little to the effect of feedback signals in reducing the amount of conditioned fear to a danger signal. The effects of feedback signals in reducing discrete fears were also found by Cook et al. (1987) but only after extensive training. This result parallels the finding that control reduces discrete fear only after extensive training. The studies of Mineka and her colleagues (Cook et al., 1987; Mineka et al., 1984; Starr & Mineka, 1977) demonstrated that feedback signals play a crucial role in reducing fear to danger signals. In these paradigms, feedback signals were always preceded by a shock, which was, in turn, preceded by the danger signal. We suggest that this particular paradigm resulted in the following associations: (a) Danger signal acquires aversive meaning through its relationship with the shock, (b) feedback signal acquires appetitive meaning through its relationship to the nonoccurrence of shock, (c) shock acquires some appetitive meaning through its association with feedback signals, and (d)

danger signal acquires some appetitive meaning through its relationship with the feedback signal. Assuming that appetitive and aversive representations are mutually inhibitory (Dickinson & Pearce, 1977), then the relationships hypothesized above lead to the prediction that feedback signals reduce the aversiveness of both danger signals and shock itself, thereby decreasing the fear that danger signals evoke. If so, a different paradigm (i.e., one that does not allow the formation of associations between feedback signals and both shock and danger signals) would not produce the fear-reduction effect of feedback signals. (See Cook et al., 1987; Mineka et al., 1984; Starr & Mineka, 1977, for a related discussion.). An alternative explanation for the effect of feedback signals in reducing discrete fear is that any information about the shock reduces its aversiveness. Accordingly, by adding information about the shock, feedback signals decrease the aversiveness of the representation of shock and thereby reduce the aversiveness of the associated danger signal. The information explanation was supported by Katz, Webb, and Stotland (1971), who found that predictability of the intensity of shock reduced conditioned fear in human subjects. A group that received signaled shock of variable magnitude displayed less habituation of fear during acquisition and greater resistance to extinction of fear than did a group that received signaled shock of consistent magnitude. These differences emerged despite the fact that the mean shock intensity was actually higher in the consistent intensity group than in the variable intensity group. In summarizing the effects of predictability on discrete fear, two conclusions seem warranted. First, complete unpredictability about the occurrence or nonoccurrence of shock (a lack of both danger and safety signals) leads to proactive interference in acquiring discrete fear (as measured by suppression ratios). This interference may result from a failure to discriminate danger signals from contextual cues or from a blocking effect that is due to the heightened contextual fear produced by unpredictability. Second, feedback signals reduce fears of discrete danger only after extensive experience.

Numbing Earlier, we suggested that analgesia observed in stressed animals parallels the numbing symptoms of PTSD. Stress-induced analgesia has been produced by diverse stimuli such as footshock, centrifugal rotation, and injection of intraperitoneal hypertonic saline (Terman, Shavit, Lewis, Cannon, & Liebeskind, 1984; Watkins & Meyer, 1982). It has typically been measured by the latency to tail flick in response to aversive stimulation to the tail or by a decrease in the amount of recuperative behaviors such as paw licking. Stress-induced analgesia can be conditioned. For example, rats showed more freezing and decreased pain sensitivity in the same chamber in which they had been shocked than in a different chamber (Fanselow & Baackes, 1982). At least two types of stress-induced analgesia have been identified: one mediated by endogenous opiods and one nonopiod. Stressors differ with respect to the type of analgesia they produce (Terman et al, 1984; Watkins & Meyer, 1982). However, some stressors do not produce analgesia at all (Watkins & Meyer, 1982). Thus, issues in this literature address the charac-

AN ANIMAL MODEL OF PTSD teristics of a stressor that are crucial in producing analgesia and the characteristics of a stressor that determine whether the opiod system will be activated. Consistent with the purpose of this article, in reviewing the literature on analgesia, we focus on the effects of controllability and predictability in determining the extent of analgesia and the activation of the opiod analgesia system. Effects of controllability. Inescapable shock has been found to produce more durable analgesia than does escapable shock (Drugan, Ader, & Maier, 1985; Maier et al, 1982). This difference suggests that separate mechanisms may mediate the analgesia produced by inescapable and escapable shock. Maier and his colleagues hypothesized that escapable and inescapable shock differ in the extent to which they activate the opiod system. To examine this hypothesis, rats were given naltrexone, an opiate receptor antagonist, or saline before receiving escapable shock, yoked-inescapable shock, or restraint with no shock (Hyson, Ashcraft, Drugan, Grau, & Maier, 1982). Naltrexone produced a larger attenuating effect on the analgesia of the rats that received inescapable shock than on that evidenced by the rats that received escapable shock. This indicates that the analgesia produced by inescapable shock has a larger opiod involvement than that produced by escapable shock. To elucidate further the role of opiods in the analgesia produced by inescapable shock, Hyson et al. (1982) varied the dose of naltrexone and tested analgesia at various points during the administration of 80 inescapable shocks. Inescapably shocked saline controls showed both an early peak (20 trials) and a late peak (60-80 trials) of analgesia. The early analgesic peak was not sensitive to the effects of naltrexone at any dose, whereas the later analgesic peak was attenuated by naltrexone in a dose-dependent fashion. However, Hyson et al. did not study the degree of opiod involvement in the early peak produced by escapable shock. This issue was addressed by Drugan et al. (1985), who found that both escapable and yoked-inescapable shock led to the double-peak pattern of analgesia. Naltrexone had no effect on the early analgesic peak of either type of shock but did block the late analgesic peak only for inescapable shock. Thus, only the late analgesic peak following inescapable shock appears to be opiod mediated. To examine further the relationship between inescapability and opiod-mediated analgesia, rats were given either escapable shock, yoked-inescapable shock, or restraint and were tested for analgesia 24 hours later after receiving a low dose of morphine (Hyson et al., 1982). Inescapable shock produced greater analgesia during this test than the other two conditions, suggesting that it produced hyperactivity to morphine. The authors suggested that this hyperactivity may be explained by sensitization of the endogenous opiod system by inescapable shock. Indeed, evidence for such sensitization was reported by Drugan, Moye, and Maier (1982), who found that previous experience with inescapable shock hastened the production of opiod-mediated analgesic peak to inescapable shock, whereas previous experience with escapable shock blocked the appearance of this analgesic peak. This finding, that previous experience with escapable but not inescapable footshock prevented the occurrence of the late opiod-mediated analgesic reaction to subsequent inescapable shock, has been replicated (Moye et al., 1983). Moye et al. (1983) concluded that "control over a stressor

227

such as shock may trigger physiological reactions that oppose the activation of opiod analgesia systems" (p. 250). The evidence reviewed above suggests that controllability affects biological systems. In a series of experiments, Grau (1987a, 1987b) demonstrated the role of cognitive processing in producing these effects. Analgesia produced by inescapable shock was attenuated by postshock distractors (either a flashing light or weak shocks), suggesting that the effect of uncontrollability may be mediated by limited-capacity cognitive processing mechanisms (is., attention, working memory). Note that in each of the studies reviewed above, both inescapable and escapable shocks were unsignaled. Therefore, it is impossible to determine whether the effects are due entirely to uncontrollability or to its combination with danger unpredictability. Maier and Keith (1987) demonstrated that the presence of a danger signal had no effect on either the early or late peaks of analgesia produced by uncontrollable shocks, suggesting that controllability alone accounts for the effects. In summary, the evidence reviewed above supports the following conclusions. First, inescapable shock leads to a more durable analgesia than does escapable shock. Second, the analgesia produced by extensive inescapable shock is mediated by opiods to a greater extent than analgesia produced by escapable shock. Third, inescapable shock leads to a sensitization of the opiod system, so that it facilitates the production of future opiod-mediated analgesia. The effects above are due to uncontrollability per se rather than to its combination with danger unpredictability. Finally, a limited-capacity processing mechanism such as attention or working memory may mediate the effects of controllability on analgesia. Effects of predictability. Danger signals, but not feedback signals, produce analgesia (Fanselow & Baackes, 1982; Fanselow & Bolles, 1979). Rats displayed pain sensitivity in the presence of safety cues and analgesia in the presence of danger cues. Naltrexone reversed the analgesia produced by the danger cues indicating mediation by endogenous opiods. Evidence suggesting that analgesia may be associated with discrete fear rather than contextual fear has been reported by Ross and Randich (1985). They compared acquisition of conditioned analgesia displayed by rats that received shocks signaled by a CS with conditioned analgesia displayed by rats in control groups receiving exposure to the CS and US explicitly unpaired, to US only, to CS only, or to the apparatus alone. Only the rats that received signaled shock and were tested for analgesia in the presence of the CS displayed analgesia. This suggests that fear per se is not sufficient to produce analgesia because the US-only group displayed contextual fear but not analgesia. These results are inconsistent with those reported by Maier and his colleagues demonstrating analgesia with unsignaled inescapable shocks (Drugan et al., 1985; Hyson et al., 1982; Maier et al., 1982; Maier & Keith, 1987; Maier, Sherman, Lewis, Terman, & Liebeskind, 1983). However, Ross and Randich's (1985) rats received one shock per day for a total of 5 days, whereas the rats in the experiments of Maier and his colleagues received many shocks in the same shock session. In addition, Ross and Randich found that naloxone did not affect conditioned analgesia, which is inconsistent with the findings of Fanselow and Baackes (1982). In light of these differences, it is important to

228

E. FOA, R. ZINBARG, AND B. ROTHBAUM

replicate Ross and Randich's results before further attempts to interpret these discrepancies are made. Ross and Randich (1985) also found that conditioned analgesia extinguished before freezing behavior. This result may suggest that the relationship between fear and analgesia is different from that between fear and freezing. It seems that a greater threshold of fear may be necessary to produce analgesia than to produce freezing. Consistent with this interpretation are the findings that freezing (in nature) is more prominent when danger is far away whereas tonic immobility, which may include both freezing and analgesia, emerges when danger is imminent (Marks, 1987). This interpretation may account for the apparent discrepancies between the findings of Ross and Randich and those of Maier and his colleagues. Perhaps the greater number of shocks administered in Maier's paradigms produced more fearful rats than did Ross and Randich's paradigm, and therefore, only animals in the former paradigm exhibited analgesia to the apparatus. In a series of experiments, Maier and Keith (1987) examined the relationship among feedback signals, danger signals, and analgesia. They found that feedback signals blocked the late analgesic peak that normally occurs after many inescapable shocks. This finding is particularly interesting because results reviewed above indicated that escapable shock reduced opiod system activation but did not reduce the late analgesic response. Thus, with regards to analgesia, feedback signals do not simply mimic the effects of control as they do with regard to discrete fear. Furthermore, feedback signals blocked the development of the late analgesic response rather than simply masking its expression. Increasing the delay between shock termination and the onset of feedback signals reduced their ability to block analgesia. In fact, the analgesia-blocking effect of the feedback signals was completely absent at delays of 17.5 s and greater. A danger signal or a signal presented simultaneously with shock did not block analgesia. In contrast, a signal that was presented randomly within the intershock intervals blocked analgesia just as feedback signals did. Moreover, random signals occurring within 15 s after shock delayed the appearance of the late analgesic peak, whereas random signals occurring outside of a 15-s postshock interval did not. Maier and Keith (1987) argued that the random signals occurring within 15 s after shock displaced the shock trial events from the limited-capacity processing necessary for learning. Taken together with Grau's (1987a, 1987b) findings discussed above, these results suggest that shock contingencies (uncontrollability, unpredictability) will affect the organism's response to shock only if the contingency is processed and stored in memory. Thus, conditions that facilitate such information processing will facilitate the development of analgesia, whereas conditions that hinder this processing will delay or block analgesia. The ability of feedback signals to block the future development of analgesia was examined by Maier and Warren (1988), who compared analgesia observed during the shock session with analgesia observed 24 h later. Previous experience with control, but not with feedback signals, blocked future analgesia. These results again suggest that the feedback signals do not simply mimic the effects of control on analgesia. In summary, signaled shock (with danger signals) produces

analgesia. However, it is unclear whether this effect is due to danger predictability alone or to its combination with uncontrollability. The inclusion of feedback signals blocks the occurrence of the late opiod-related analgesia during initial training with uncontrollable shock but does not prevent the future occurrence of such analgesia. These results contrast with the effect of control; control does not block the late analgesic peak during initial training but does reduce the opiod involvement in this analgesia and prevents its future occurrence. Thus, although the relationship between unpredictability and analgesia is not well understood at present, the evidence suggests that the analgesic effects of uncontrollability reviewed above are not mediated by unpredictability. Avoidance In the DSM-IH-R, avoidance symptoms include efforts to avoid thoughts or feelings as well as activities or situations that are associated with the trauma. The animal literature readily lends itself to an analysis of the effects of uncontrollability and unpredictability on avoidance of activities and situations. Learning theorists have often made the distinction between active and passive avoidance. In a typical two-way active avoidance or escape paradigm, the organism is placed in one side of a shuttle box, where shock is delivered. The organism may jump over the barrier to the other side of the box during the presentation of a warning signal and avoid shock. In a typical passive avoidance paradigm, the organism is punished on the emission of a specified appetitive response, either learned (e.g., bar pressing) or innate (e.g., licking). It is thought that different motivational and physiological systems mediate these two types of avoidance (Gray, 1982). Whereas fear and aversive motivation undoubtedly are related to both active and passive avoidance, relief and appetitive motivation are thought to play a larger role in the maintenance of active avoidance than of passive avoidance (Holies, 1970; Gray, 1982; Mineka, 1979; Weisman & Litner, 1972). Effects of controllability. Many dogs exposed to unpredictable-inescapable (uncontrollable) shock subsequently displayed a generalized deficit in learning to escape and actively avoid shock (Overmier & Seligman, 1967; Seligman & Maier, 1967). This learning deficit appears to depend on the complexity of the task. Rats did not show learning deficits when they were required to cross a shuttle box only once to terminate shock. However, when required either to cross the shuttle box twice or to turn a wheel to terminate shock, rats displayed a learning deficit (Maier, Albin, & Testa, 1973). Similar results demonstrating a more pronounced learning deficit on complex than on simple tasks were reported by Volpicelli, Ulm, and Altenor (1984) and Maier and Warren (1988). The relationship between the learning deficit and task complexity can be explained by the limited availability of attentional resources. That is, the increased fear and anxiety produced by unpredictable-uncontrollable shock may compete for limited attentional resources and, thereby, reduce the processing capacity for task performance. Similar effects have been observed in humans. Anxiety impairs cognitive performance more on difficult than on easy tasks (Eysenck, 1982; Wine, 1971). Moreover, anxious persons evidence an attentional bias

229

AN ANIMAL MODEL OF PTSD to threat material typically observed only on dual tasks that involve competition for attentional resources (Eysenck & Mathews, 1987; Mathews & Eysenck, 1987). When rats learn to escape the CS rather than the US, the learning deficit produced by uncontrollable shock is evident even on a simple task (Osborne et al., 1975). At first glance, these results appear to conflict with those of Maier et al. (1973). However, the apparent inconsistency can be resolved if escaping a CS is thought to require more processing resources than escaping a US. Escaping a CS requires the association between the CS and US in addition to that between responding and US occurrence. In contrast, escaping a US only requires the second association. Because Osborne et al. (1975) used signaled uncontrollable shock and found results similar to that of Maier et al. (1973), who used unsignalled uncontrollable shock, their results suggest that the learning deficit seen on complex escape and avoidance tasks can be attributed solely to the effects of uncontrollability. As discussed earlier, uncontrollable shock leads to activation of opiod systems in addition to causing learning deficits. The relationship between these two phenomena was examined by Maier and his colleagues. Drugan and Maier (1983) found that naltrexone attenuated escape deficits, indicating that endogenous opiods may be involved in the escape deficit produced by uncontrollable shock. Further evidence for the involvement of opiods in escape deficits was derived from Maier et al.'s (1983) finding that two shock procedures that produced opiod-mediated analgesia also produced escape deficits. Moreover, two shock procedures that produced analgesia that was either nonopiod or only partly mediated by opiod did not produce escape deficits. The learning deficit produced by uncontrollable shocks in the experiments above has often been interpreted within the context of learned helplessness theory (Maier & Seligman, 1976). According to learned helplessness theory, uncontrollable shock leads to a generalized deficit in associating responses with consequences. Note that this interpretation is based solely on performance in active avoidance tasks. A different interpretation emerges when one also considers the effects of uncontrollable shock on performance in passive avoidance tasks. Uncontrollable shock has often produced superior learning of passive avoidance (e.g., Hollis & Overmier, 1973; Pearl, Walters, & Anderson, 1964). Rush et al. (1982) examined performance of both active and passive avoidance and found that uncontrollable shocks impaired active avoidance learning but enhanced passive avoidance learning (Rush et al., 1982). This facilitation of passive avoidance clearly disconfirms the learned helplessness hypothesis of a generalized deficit in associating responses and consequences. It seems, then, that with respect to active avoidance, uncontrollability produces a learning deficit that is most pronounced on complex tasks, and this deficit appears to be mediated, at least in part, by opiod system activation. The fact that uncontrollability interacts with task complexity and the evidence that limited-capacity cognitive processes may be involved in the activation of the opiod system (Grau, 1987a, 1987b; Maier & Keith, 1987) suggests that this learning deficit is mediated by limited-capacity attentional variables. As noted earlier, uncontrollability appears to facilitate rather than impair passive avoid-

ance learning. Antianxiety drugs produce the opposite effects: They facilitate active avoidance and impair passive avoidance (Gray, 1982). Therefore, the effects of uncontrollability on escape and on passive avoidance may be attributable to the heightened fear it produces. Evidence consistent with this hypothesis was reported by Minor and LoLordo (1984), who found that escape deficits after uncontrollable shock emerged only in animals that were both trained and tested in the presence of stress-produced odors. The authors suggested that the stress-produced odors became a CS for fear, which, in turn, mediated the effect of uncontrollable shock. The role of fear in mediating escape deficit after uncontrollable shock is also suggested by the finding that administration of benzodiazapines during uncontrollable shock blocks the escape deficit (Drugan, Ryan, Minor, & Maier, 1984). Effects of predictability. If uncontrollability produces escape deficits and improves passive avoidance through increased discrete fear and if the absence of safety predictability mediates this increased fear, then feedback signals should attenuate the effect of uncontrollability on performance. Indeed, Volpicelli et al. (1984) and Maier and Warren (1988) found that the presence of feedback signals eliminated the escape deficit produced by uncontrollable shock. Previous experience with control, but not with feedback signals alone, blocks future escape deficits to inescapable shock (Maier & Warren, 1988; Minor et al., 1990). However, in examining the effects of signaling the termination of inescapable shock (cessation conditioning) on later escape deficits, Minor et al. (1990) found that prior experience with a cessation signal alone reduced future inescapable shock-escape deficits and that a combination of prior cessation and feedback signals completely eliminated these deficits. Previous experience with unpredictable shock was found to impair future passive avoidance learning (Baker, 1976). This is consistent with the conclusion that previous exposure to unpredictable shock impairs the acquisition of discrete fears. Given that extensive experience with feedback signals appears to reduce discrete fears, we would expect that feedback signals would impair passive avoidance, but to our knowledge no studies examining this relationship have been conducted to date. In summary, feedback signals reverse the escape deficit produced by uncontrollability, and prior experience with a combination of cessation and feedback signals eliminates the escape deficit produced by later inescapable shock. These results suggest that the escape deficit, like heightened discrete fear produced by uncontrollability, is mediated by safety unpredictability. However, the effects of feedback signals and cessation signals on passive avoidance have not been studied. Previous experience with danger unpredictability appears to impair future passive avoidance learning, but its effect on active avoidance or escape has not been studied. Discussion The evidence reviewed above suggests that uncontrollable, unpredictable shock has remarkably consistent effects across the four response categories examined in this article. Extensive experience with uncontrollable, unpredictable shock produces persistent arousal and increased generalized fear, increased

230

E. FOA, R. ZINBARG, AND B. ROTHBAUM

discrete fear, lasting opiod-mediated analgesia as well as opiod system sensitization, and enhanced learning of passive avoidance and impaired learning of active avoidance. Aversive stimuli lead to heightened stress to which, in the absence of an effective escape or avoidance response and in the absence of information regarding the occurrence of the stressor, the organism responds with analgesia, which minimizes the pain, resulting in what appears as a passive coping style, or resignation. These effects closely resemble the syndrome of PTSD in humans and may imply that the uncontrollable, unpredictable nature of a monumental trauma plays an important role in the etiology of PTSD. Obviously, we are not suggesting that the uncontrollabilityunpredictability model is all-encompassing. From the outset, we have acknowledged that these variables act in concert with many other variables to produce PTSD in humans. With this limitation in mind, the animal model we proposed may be pursued in two directions. The first involves generating hypotheses that are based on clinical observations of PTSD in humans and then testing them in animals exposed to uncontrollable, unpredictable aversive stimuli. The second strategy involves generating hypotheses from the animal model about PTSD, which can then be tested with trauma victims. Implications for Animal Research The first research strategy, the examination of features believed to be characteristic of PTSD in the context of animal experiments, not only allows for testing the validity of the model but, more importantly, offers the potential to gain insights regarding the psychopathology of PTSD. Specifically, the animal model allows for systematic examination of the biological and psychological processes underlying PTSD psychopathology. In Gorenstein and Newman's (1980) words, "in this respect, the animal model serves as a sort of experimental crucible, permitting thorough, controlled examination" (p. 312). At the same time, testing hypotheses derived from clinical observations regarding PTSD features that have not been examined in animals submits the model to the possibility of refutation. One important issue that should receive more experimental attention is the degree to which the effects of uncontrollable, unpredictable shock generalize across contexts. Many of the animal studies examined such effects only in the same context in which the shock was delivered. Given the highly pervasive nature of PTSD symptoms, if the model is valid, then one would expect that the effects of uncontrollable, unpredictable shock would generalize from the experimental context to other contexts. Evidence from the "learned helplessness" literature is supportive of the generality prediction. In the early learned helplessness studies (e.g., Overmier, 1968; Overmier & Seligman, 1967), dogs were given unsignaled, unescapable shock while they were restrained in a hammock in a distinctly different context from the shuttle box where escape and avoidance performance was examined. The escape deficits observed in the shuttle box therefore suggest generalization across contexts. More recently, Rosellini, Widman, Abrahamsen, and Bassuk (1990) found that reinstatement of fear generalized to novel contexts in animals with a prior history of uncontrollable, unpredictable

shock but not in animals with a prior history of controllable shock. Examining a different response system, opiod-mediated analgesia, Maier and Warren (1988) tested analgesia in a different context from that where the initial training with either controllable or uncontrollable shock occurred. The finding of greater analgesia in animals with a prior history of uncontrollable, unpredictable shock than in animals with a history of either controllable shock or uncontrollable shock with feedback signals again suggests that the effects of uncontrollable, unpredictable shock generalize across contexts. Further research is needed to elucidate the variables that affect the degree of generalization and the mechanisms that mediate it. At the outset of this article, we noted that the subjective experience of private events such as flashbacks, nightmares, and intrusive recollections cannot be modeled in lower animals. However, recent advances in the field of the cognitive psychophysiology of sleep processes may be adapted to test hypotheses regarding the effects of uncontrollable, unpredictable shock on information processing during sleep in animals. Winson (1972) pointed out that theta rhythm is observed in awake animals when they are engaged in behavior crucial to survival as well as during REM sleep and suggested that the presence of theta rhythm reflects "a neural process whereby information essential to the survival of a species—gathered during the day—was reprocessed into memory during REM sleep" (Winson, 1990, p. 88). Pavlides and Winson (1989) developed an elegant paradigm that enables the measurement of memory processing in rats during sleep (see Winson, 1990, for a detailed review). They located and recorded electrical activity from two CA1 hippocampal neurons in the rat that corresponded to two different place fields. That is, each neuron fired only when the awake animal moved to a particular location. When, during the day, the rat was restricted to just one of the two locations, then later on, during sleep, the neuron that mapped that location fired at a significantly higher rate compared with its previous sleeping baseline and to the neuron that had not mapped that location. Winson suggested that this pattern of results indicated that the animals were reprocessing information during sleep that was encoded when the animal was awake. We propose that the selective firing of place neurons when the animal is not in the corresponding place field can be viewed as a model of dreams when the animal is asleep and perhaps as a model of recollections when the animal is awake. If one accepts this proposition, the paradigm described above could be adapted to examine whether uncontrollable, unpredictable shock is more likely to be reprocessed during either sleep or wakefulness than controllable, predictable shock. In terms of the animal model of PTSD, it is predicted that neurons that map locations where uncontrollable, unpredictable shock is delivered will fire at a higher rate during sleep than neurons that code the location where controllable, predictable shock is delivered. According to Winson (1990), evidence in support of this hypothesis would indicate that the memory of stimuli associated with uncontrollable, unpredictable events is especially important for survival and elicits enhanced reprocessing. Such evidence would be consistent with Horowitz's (1986) view that reexperiencing symptoms reflect an attempt to integrate trauma-related information into currently existing cognitive structures. This line of research would not omy test

AN ANIMAL MODEL OF PTSD

the validity of the model, but more importantly, may provide an opportunity for a systematic examination of the mechanisms underlying nightmares and, perhaps, also flashbacks and intrusive recollections. Implications for PTSD Research The second research strategy we proposed was to draw on empirical and theoretical development in the animal literature to generate hypotheses about the psychopathology of human PTSD. Implications of the animal model for PTSD may vary in their degree of conceptual generality. At the most general level, we hypothesized that the degree to which a stressful event is uncontrollable and unpredictable is related to the likelihood of the development of the PTSD syndrome. All other factors being equal, the greater the degree of uncontrollability and unpredictability associated with a given stressor, the more likely the victim will be to develop PTSD symptoms. For the victim of an uncontrollable, unpredictable important stressor, daily life is marked by a sense of impending doom because threat pertinent to his or her survival can be neither predicted nor controlled. Relief from such an existence is possible only by modulating the psychological impact of the trauma. Thus, psychogenie amnesia, detachment, and restricted aifect, the dissociative symptoms of PTSD, may be functionally similar to avoidance and escape behaviors; both provide escape from pain. This is not to say that the mechanisms underlying numbing and behavioral avoidance are the same. Avoidance may be driven by strategic psychological processes, whereas numbing may be mediated by more automatic psychological mechanisms resembling the ones underlying freezing behavior in animals. Beyond this general prediction, what else can the animal literature teach us about PTSD in trauma victims? Effects of perceived contingencies: An information-processing perspective. It seems reasonable to assume that perception of threat may be at least as important as the actual danger in determining the severity of PTSD symptoms. Indeed, using path-analytic methods, Riggs, Foa, Rothbaum, and Murdock (1991) found that among recent rape and crime victims, the relationship between the severity of the assault and the severity of PTSD was mediated by perceived life threat. Given the importance we place on the organism's perception of an event, the hypotheses explicated in this article refer to perceived controllability and predictability rather than to actual contingencies. Note that both animals and humans enter a stressful experience with preexisting memory networks. These preexisting networks will almost certainly influence the organism's perception of the stressor. The view that the person's pretrauma memory network plays a crucial role in the development of PTSD symptoms has been discussed in detail by Horowitz (1980). There are at least two ways in which the information embedded in the stressful experience interacts with the individual's pretrauma networks to produce PTSD symptoms. The first occurs when a traumatic event violates strongly held knowledge contained in a preexisting network. Such a mismatch seems to be evident in Masserman's (1943) procedures in which the animals had formed a strong appetitive association with a stimulus that was later paired with an uncontrollable, aversive stimuli. Note that in Masserman's paradigms, when the expectation of a

231

pleasant experience was violated, a single uncontrollable, aversive encounter was sufficient to produce long-lasting, intense disturbances. Such a mismatch is also evident in Rescorla's (1971) "superconditioning" procedure. Using this procedure, Rescorla found that pairing a novel stimulus with uncontrollable shock resulted in greater behavioral suppression if the stimulus was presented in compound with a stimulus that had been present in prior inhibitory training. In other words, greater fear to the excitatory stimulus was displayed when the fear conditioning trials occurred in a context that previously signaled safety. This scenario is similar to the conceptualization advanced by Perloff (1983) suggesting that PTSD is more likely to occur when the victim's "previous" 'illusions of invulnerability' are suddenly shattered" (p. 42). Accordingly, if the severity of the trauma is held constant, we predict that one is most likely to develop chronic symptoms of PTSD if the trauma occurred in a previously safe or pleasant environment or despite a response that previously produced safety or pleasure. Support for the hypothesis that violation of positively valenced expectations is associated with PTSD comes from the finding that PTSD is more likely to occur following sexual abuse in childhood when the perpetrator is the father rather than a stranger or an older child (McLeer, Deblinger, Atkins, Foa, & Ralphe, 1988). Our explanation of this finding rests on the assumption that the representation of one's father, in contrast to an older child or a stranger, is universally associated with safety. Seen in this light, abuse by one's father violates basic safety rules more than abuse by a stranger or an older child. The second scenario for the development of PTSD occurs when the preexisting network does not include appetitive associations with the context in which the uncontrollable, unpredictable aversive stimuli is experienced. In this instance, repeated experience with uncontrollable, unpredictable stress is necessary for the formation of expectations that danger can occur at any time and is inescapable. The consistent finding that the effects of uncontrollability and unpredictability were evidenced in animals only after extensive experience with the experimental contingencies supports the hypothesis that in the absence of violating preexisting appetitive expectations, repeated experience is necessary for the formation of memory networks supporting such a pervasively threatening world view. Thus, the animal model anticipates that soldiers will be at risk for developing PTSD after experiencing repeated uncontrollable, unpredictable stressors even though they obviously had not had prior appetitive associations with war. Evidence consistent with this prediction was found by Foy and his colleagues (Foy, Resnick, Sipprelle, & Carroll, 1987; Foy et al., 1984), who reported that the incidence of PTSD among Vietnam veterans was positively correlated with the length of time spent in combat. The animal literature reviewed earlier also suggests that once a memory network supporting representation of a pervasively threatening world is formed, it serves to sensitize the organism to the disturbing effects of future uncontrollable, unpredictable stress (for a related discussion see Chemtob, Roitblat, Hamada, Carlson, & Twentyman, 1988). This finding leads to the prediction that repeated childhood abuse would lead to the formation of such memory networks that, in turn, would predispose the victim to developing PTSD following later victimization. Pre-

232

E. FOA, R. ZINBARG, AND B. ROTHBAUM

liminary evidence consistent with this hypothesis comes from the finding that childhood sexual abuse, which often occurs repeatedly, is associated with PTSD severity in response to rape and to nonsexual assault in adulthood (Dancu, Shoyer, Riggs, &Foa, 1991). The role of cognitive processes in mediating PTSD-like symptoms is also suggested by the findings that distractor stimuli interfere with the production of stress-induced analgesia (Grau, 1987a, 1987b; Maier & Keith, 1987) and that task difficulty interacts with uncontrollability in producing escape deficits (e.g., Maier et al., 1973). This conceptualization further highlights the notion that the perception of the stressor is extremely important in the etiology of PTSD in humans. It also suggests that studies of individual differences in the processing of emotionally laden information will provide important insight into the factors that render some people more vulnerable to PTSD than others. Loss of control. Following Mineka and Kihlstrom (1978), in our analysis of the unpredictability and uncontrollability literature, we have highlighted the distinction between loss of control and lack of control. The animal data lead to seemingly paradoxical hypotheses regarding the effect of previous experience of control on the development of PTSD in humans. Some experiments suggest that history of control before the traumatic event (i.e., loss of control) sensitizes the organism. Animals with such history manifested more general arousal and circumscribed fear than animals without such history. These results lead to the prediction that prior control would facilitate the development of persistent arousal and reexperiencing. Other data suggest that prior history of control immunizes the organism. Animals with such history did not show opiod analgesia and sensitization. These data lead to the hypotheses that people who had experienced prior control over stress would be less likely to develop passive avoidance and dissociative symptoms such as numbing. The question arises as to why pretraumatic experience with control over aversive events would be patholytic for some symptoms but pathogenic for others. The available data cannot provide a definitive answer to this question. However, two possible resolutions may be entertained. First, it is possible that the etiological factors underlying one cluster of PTSD symptoms may differ from those underlying another cluster and, thus, that the different symptom clusters show different patterns of relationship to etiological factors such as loss of control. A second possibility, that context mediates the effects of prior control, was suggested by Mineka and Kelly (1989). These authors proposed that prior control may sensitize the organism to the future effects of uncontrollability that is experienced in the same context where, previously, the organism had control over aversive stimulation. This explanation is consistent with our mismatching hypothesis discussed earlier, which states that PTSD is likely to develop when the controlling response, which previously was associated with safety, becomes associated with danger and thus violates previously held safety rules. Mineka and Kelly further suggested that prior control may immunize the organism against the future effects of uncontrollability experienced in contexts that are dissimilar to that context in which prior control had been experienced. We propose that the crucial mechanism operative here is that the preexisting associations with safety remain intact and

protect the organism from generalizing that the world is uncontrollable and unpredictable. In addition to the hypotheses regarding the effects of perceived contingencies and loss of control on the development of the PTSD syndrome, our analysis of the animal literature enables one to derive more specific hypotheses regarding the relative importance of uncontrollability and unpredictability in producing each of the four individual clusters of PTSD symptoms. In the following two sections, we extrapolate such specific hypotheses. Controllability. The animal literature clearly indicates that uncontrollable stress leads to greater signs of generalized arousal than controllable stress, although it is unclear whether this effect is mediated by safety predictability. This finding leads us to predict that uncontrollable stress would be more likely to produce the generalized arousal symptoms characteristic of PTSD than would controllable stress. Evidence consistent with this prediction has been reported by Kuch (1989), who found that passengers tend to exhibit more postaccident psychopathology than do drivers. Our explanation of this finding rests on the assumption that drivers are more likely to perceive themselves as being in control over the accident than are passengers. Further research is needed to clarify the role of safety predictability in protecting the victim from developing persistent symptoms of generalized arousal. The animal literature on the effects of uncontrollable shock suggests that uncontrollable stress leads to opiod-mediated analgesia. It is therefore hypothesized that opiod-mediated analgesia may underlie the numbing symptoms characteristic of PTSD. This hypothesis is supported by the findings that the decrease in pain sensitivity during exposure to combat stimuli among Vietnam veterans with PTSD was reversed by naloxone (van der Kolk et al., 1989). Moreover, uncontrollable shock in animals produces opiod system sensitization. We propose that such opiod system sensitization produced by uncontrollable stress may underlie the numbing often observed as a response to reexperiencing symptoms. The animal literature further suggests that this prediction is likely to hold only after extensive experience with the aversive stimulus. This prediction is consistent with the findings in the PTSD literature that victims of a single trauma (e.g., flood victims) display fewer numbing symptoms than people who have experienced repeated traumas such as incest and combat (Green, 1989; Kilpatrick & Resnick, 1989). Clinical observations of people with dissociative disorders are also consistent with this prediction. Ninety-seven percent of multiple-personality-disordered persons (the most extreme of dissociative states) were victims of childhood abuse or neglect (Putnam, Guroff, Silberman, Barban, & Post, 1986; Schultz, Braum, & Kluft, 1985). Perhaps repeated experiences with uncontrollable stress such as repeated child abuse are more likely to lead to the dissociative disorders, whereas a single uncontrollable stress is more likely to produce anxiety disorders. Predictability. The available evidence suggests that danger unpredictability, similar to uncontrollability, produces persistent arousal and increased generalized fear. It appears that danger unpredictability interferes with the animal's ability to discriminate discrete CSs from similar stimuli. Therefore, we predict that danger unpredictability would lead to less discrimi-

AN ANIMAL MODEL OF PTSD

nation between stimuli that are distinctly related to the stressor and those that are less related (i.e., produce greater generalization). This would result in a greater number of cues that would potentially elicit reexperiencing. For example, the woman who is raped in her own bed in the middle of the day would be expected to display more frequent reexperiencing symptoms that are easily triggered by a plethora of stimuli. In contrast, a woman who is raped while walking alone in a high-crime neighborhood at night would be less likely to develop widespread cues for reexperiencing. The interactive effect of uncontrollability with danger unpredictability on increased arousal and generalized arousal and fear remains unclear. Each of the two variables seems to be sufficient but not necessary to produce generalized arousal. This leads to the prediction of additivity as found by Weiss (1970). Thus, stressors that are uncontrollable and whose onset cannot be predicted are expected to result in more intense symptoms of increased arousal than stressors that are characterized by either variable alone. Danger unpredictability reduces passive avoidance, whereas the effects of safety unpredictability on this behavior have not yet been studied. Accordingly, we predict that in the absence of the recognition of cues that could indicate elevated risk for the occurrence of the stressor, victims will be less likely to display phobic avoidance specific to particular situations. For example, the incest victim who is assaulted at various times of the day or night and in various places would not be expected to avoid particular situations, whereas the incest victim who is always assaulted at night in his or her own room may protect himself or herself by opting to not sleep there. Feedback signals appear to reduce discrete fears, block opiod-mediated analgesia but not opiod system sensitization, and suppress escape deficits produced by uncontrollable shock. These findings suggest the hypothesis that even when a stressor is uncontrollable, to the extent that the victim can recognize cues signaling relief, he or she would be less likely to develop symptoms of reexperiencing, numbing during the stressor, and passivity. The literature regarding the effects of feedback signals on generalized arousal and fear is less consistent. One possible interpretation of this inconsistency is that weak safety signals may augment generalized arousal symptoms, but strong safety signals reduce them. Because the literature on PTSD is mostly derived from reactions to either a one-time event (e.g., rape) or a series of events that may differ greatly from each other (e.g., combat), the opportunity to acquire strong safety signals is often absent or limited in these situations. Perhaps this explains why many people with PTSD ignore obvious safety cues and exhibit generalized fear in spite of their presence (e.g, a Vietnam veteran being hypervigilant back in the United States). On the other hand, the presence of safety signals may be more likely to attenuate generalized arousal symptoms in long-term victimization such as sexually abused children or battered

Conclusions The DSM-H1-R (American Psychiatric Association, 1987) states that the stressor producing PTSD must be "markedly distressing to almost anyone" (p. 250). Examples provided in

233

the manual imply that the event should be perceived as threatening to one's physical integrity or pose a serious threat to significant others. Indeed, rape victims who perceived that their life was endangered or who experienced physical harm were more likely to develop PTSD symptoms than those who did not (Kilpatrick, Best, Veronen, Villeponteaux, & Amick-McMullan, 1986). However, the most important conclusion emerging from this review is that not only must the stressor be perceived as a potential threat to survival, it must also be experienced as uncontrollable or unpredictable. This suggests that the constructs of uncontrollability and unpredictability should be incorporated into the definition of what constitutes a trauma for Criterion A in the DSM-III-R criteria for PTSD. In this review, the effects of uncontrollability and unpredictability as independent variables were emphasized. The question of what mechanisms mediate these effects is beyond the scope of this article. In fact, several theories of the effects of uncontrollability and unpredictability have been put forth (e.g., Abramson, Seligman, & Teasdale, 1978; Glazer & Weiss, 1976a, 1976b; Gray, 1982; Maier & Seligman, 1976; Miller, 1981; Miller & Grant, 1979; Minor et al, 1989; Seligman, 1975; Seligman & Binik, 1977; Weiss, Glazer, & Pohorecky, 1976), implicating such apparently disparate mechanisms as attention, attributions, memory processing, and neurotransmitter functioning.6 Therefore, one of the most important questions that remains to be answered relates to the relative efficacy of current psychological theories in accounting for the phenomena reviewed in this article. Our exposition of the relationship of uncontrollability and unpredictability to PTSD is intended to bring into sharper focus some of the phenomena that need to be explained in both of these areas. We hope that this analysis provides a conceptual framework for specifying the phenomena that need to be addressed by a comprehensive theory of the experimental effects of uncontrollability and unpredictability and from which an integrative research program can be launched. That is, any successful theory of the effects of uncontrollable, unpredictable aversive events must be able to account for the four clusters of behavioral phenomena addressed here: persistent symptoms of increased arousal, reexperiencing, numbing, and avoidance. Furthermore, we believe that such an integrative program of research will promote further understanding of the psychopathological processes associated with PTSD and thus be invaluable in efforts to identify essential target mechanisms for therapeutic intervention. Finally, our synthesis of the animal and PTSD literatures anticipates that information-processing constructs will play a central role in advances in formal theorizing in both areas. In particular, our conceptualization suggests that a comprehensive theory will have to address the following three sources of variability that contribute to the etiology and maintenance of PTSD: the victim's pretrauma memory networks, the information encoded during the traumatic episode, and the posttrauma strategic procedures (such as elaboration 6 The discrepancies among at least some of these theories may be more apparent than real. That is, many of these theories may not be necessarily incompatible with each other, rather, they may simply be applicable at different levels of analysis.

234

E. FOA, R. ZINBARG, AND B. ROTHBAUM

vs. cognitive avoidance) that are adopted by the victim to process the traumatic information.

References Abbott, B. (1985). Rats prefer signalled over unsignalled shock-free periods. Journal of Experimental Psychology: Animal Behavior Processes, 11,215-221. Abramson, L. U, Seligman, M. E. P., & Teasdale, J. D. (1978). Learned helplessness in humans: Critique and reformulation. Journal of Abnormal Psychology, 87, 49-74. American Psychiatric Association (1980). Diagnostic and statistical manual of mental disorders (3rd ed.). Washington, DC: Author. American Psychiatric Association (1987). Diagnostic and statistical manual of mental disorders (3rd ed., rev). Washington, DC: Author. Annau, Z., & Kamin, L. J. (1961). The conditioned emotional response as a function of intensity of the US. Journal of Comparative Physiological Psychology, 54, 428-432. Averill, J. R. (1973). Personal control overaversive stimuli and its relationship to stress. Psychological Bulletin, 80, 286-303. Badia, P., & Culbertson, S. (1972). The relative aversiveness of signalled vs. unsignalled escapable and inescapable shock. Journal of the Experimental Analysis of Behavior, 17, 463-471. Badia, P., & Culbertson, S. (1974). Changeover from unsignalled to signalled avoidance with and without a feedback stimulus in rats. Animal Learning and Behavior, 2, 278-284. Baker, A. G. (1976). Learned irrelevance and learned helplessness: Rats learn that stimuli, reinforcers, and responses are uncorrelated. Journal of Experimental Psychology: Animal Behavior Processes, 2, 130-141. Bernstein, E. M., & Putnam, F. W (1986). Development, reliability, and validity of a dissociation scale. Journal of Nervous and Mental Disease, 174,121-134. Blanchard, E. B. (1990). Elevated basal levels of cardiovascular responses in Vietnam veterans with PTSD: A health problem in the making? Journal of Anxiety Disorders, 4, 233-237. Blanchard, E. B., Kolb, L. C, Gerardi, R. J., Ryan, D, & Pallmeyer, T. P. (1986). Cardiac response to relevant stimuli as an adjunctive tool for diagnosing post-traumatic stress disorder in Vietnam veterans. Behavior Therapy, 17, 592-606. Blanchard, E. B., Kolb, L. C., Pallmeyer, T. P., & Gerardi, R. J. (1982). A psychophysiological study of post-traumatic stress disorder in Vietnam veterans. Psychiatric Quarterly, 54, 220-229. Bolles, R. C. (1970). Species-specific defense reactions and avoidance learning. Psychological Review, 77, 32-48. Brady, J. V, Porter, R. W, Conrad, D. G, & Mason, J. W (1958). Avoidance behavior and the development of gastroduodenal ulcers. Journal of Experimental Analysis of Behavior, 1, 69-72. Brennan, J. F, & Riccio, D. C. (1975). Stimulus generalization of suppression in rats following aversively motivated instrumental or Pavlovian training. Journal of Comparative and Physiological Psychology, 88, 570-579. Cantor, M. (1981). Information theory: A solution to two big problems in the analysis of behavior. In P. Harzem & M. Zeiler (Eds.), Predictability, correlation, and contiguity, (pp. 286-320). New York: Wiley. Chemtob, C., Roitblat, H., Hamada, R., Carlson, J., & Twentyman, C. (1988). A cognitive action theory of post-traumatic stress disorder. Journal of Anxiety Disorders, 2, 253-275. Church, R. M. (1964). Systematic effects of random error in the yoked control design. Psychological Bulletin, 62,122-131. Clark, L. A., & Watson, D. (1991). A tripartite model of anxiety and depression: Psychometric evidence and tavonomic implications. Journal of Abnormal Psychology, 100, 316-336. Collier, A. C. (1977). Preference for shock signals as a function of the

temporal accuracy of the signals. Learning and Motivation, 8, 159170. Cook, M., Mineka, S., & Trumble, D. (1987). The role of response-produced and exteroceptive feedback in the attenuation of fear over the course of avoidance learning. Journal of Experimental Psychology: Animal Behavior Processes, 13, 239-249. Dancu, C. V, Shoyer, B., Riggs, D. S., Foa, E. B. (1991). [Childhood sexual abuse and crime-related PTSD]. Unpublished raw data. Davidson, L. M. & Baum, A. (1986). Chronic stress and post-traumatic stress disorders. Journal of Consulting and Clinical Psychology, 54, 303-308. Desiderate, O., & Newman, A. (1971). Conditioned suppression produced in rates by tones paired with escapable or inescapable shock. Journal of Comparative and Physiological Psychology, 77, 427-431. Dickinson, A., & Pearce, J. M. (1977). Inhibitory interactions between appetitive and aversive stimuli. Psychological Bulletin, 84, 690-711. Dinsmoor, J. A. (1983). Observing and conditioned reinforcement. Behavioral Brain Science, 6, 693-728. Domjan, M., & Best, M. R. (1977). Paradoxical effects of proximal unconditioned stimulus preexposure: Interference with and conditioning of a taste aversion. Journal of Experimental Psychology: Animal Behavior Processes, 3, 310-321. Drugan, R. C., Ader, D. N., & Maier, S. F. (1985). Shock controllability and the nature of stress-induced analgesia. Behavioral Neuroscience, 99,791-801. Drugan, R. C, & Maier, S. F (1983). Analgesic and opiod involvement in the shock-elicited activity and escape deficity produced by inescapable shock. Learning and Motivation, 14, 30-47. Drugan, R. C, Moye, T. B., & Maier, S. F. (1982). Opiod and nonopiod forms of stress induced analgesia: Some environmental determinants and characteristics. Behavioral and Neural Biology, 35, 251264. Drugan, R. C., Ryan, S. M., Minor, T. R., & Maier, S. F. (1984). Librium prevents the analgesia and shuttlebox escape deficit typically observed following inescapable shock. Pharmacology Biochemistry and Behavior, 21, 749-754. Eysenck, M. (1982). Attention and arousal: Cognition and performance. New York: Springer-Verlag. Eysenck, M., & Mathews, A. (1987). Trait anxiety and cognition. In H. J. Eysenck & I. Martin (Eds.), Theoretical foundation ofbehaviour therapy (pp. 197-216). New York: Plenum Press. Fanselow, M. S. (1980). Signalled shock-free periods and preference for signalled shock. Journal of Experimental Psychology: Animal Behavior Processes, 6, 65-80. Fanselow, M. S., & Baackes, M. P. (1982). Conditioned fear-induced opiate analgesia on the formalin test: Evidence for two aversive motivational systems. Learning and Motivation, 13, 200-221. Fanselow, M. S., & Bolles, R. C. (1979). Naloxone and shock-elicited freezing in the rat. Journal of Comparative and Physiological Psychology, 93, 736-744. Foa, E. B., & Foa, U G. (1982). Differentiating depression from anxiety: Is it possible? Is it useful? Psychopharmacology Bulletin, 18, 6268. Foy, D. W, Resnick, H. S., Sipprelle, R. C, & Carroll, E. M. (1987). Premilitary, military, and post-military factors in the development of combat-related posttraumatic stress disorder. Behavior Therapist, 10, 3-9. Foy, D. W, Sipprelle, R. C, Rueger, D. B., & Carroll, E. M. (1984). Etiology of posttraumatic stress disorder in Vietnam veterans: Analysis of premilitary, military, and combat exposure influences. Journal of Consulting and Clinical Psychology, 52, 79-87. Gantt, W H. (1944). Experimental basis for neurotic behavior: Origin and development of artificially produced disturbances of behavior in dogs. New York: Hoeber.

AN ANIMAL MODEL OF PTSD Geer, J. H., & Maisel, E. (1972). Evaluating the effects of the prediction-control confound. Journal of Personality and Social Psychology, 25,314-319. Glazer, H. I., & Weiss, J. M. (1976a). Long-term and transitory interference effects. Journal of Experimental Psychology: Animal Behavior Processes, 2,191-201. Glazer, H. I, & Weiss, J. M. (1976b). Long-term interference effect: An alternative to "learned helplessness." Journal of Experimental Psychology: Animal Behavior Processes, 2, 202-213. Gorenstein, E. E., & Newman, J. P. (1980). Disinhibitory psychopathology: A new perspective and a model for research. Psychological Review, 87, 301-315. Grau, J. W (1987a). Activation of the opiod and nonopiod analgesic systems: Evidence for a memory hypothesis and against the coulometric hypothesis. Journal of Experimental Psychology, 13,215-225. Grau, J. W (1987b). The central representation of an aversive event maintains the opiod and nonopiod forms of analgesia. Behavioral Neuroscience, 101, 272-288. Gray, J. (1982). Precis of the neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. Behavioral and Brain Sciences, 5, 469-534. Green, B. (1989, October). Disasters and PTSD. Position paper prepared for the DSM-IV Post-Traumatic Stress Disorder Advisory Group, San Francisco. Grossberg, S. (1982). Processing of expected and unexpected events during conditioning and attention: A psychophysiological theory. Psychological Review, 89, 529-572. Hanson, J. P., Larson, M. E., & Snowdon, C. T. (1976). The effects of control over high intensity noise on plasma control levels in rhesus monkeys. Behavioral Biology, 16, 333-340. Helzer, J. E. Robins, L. N, & McEvoy, L. (1987). Posttraumatic stress disorder in the general population. New England Journal of Medicine, 5/7,1630-1634. Hinson, R. E. (1982). Effects of UCS preexposure on excitatory and inhibitory rabbit eyelid conditioning: An associative effect of conditioned contextual stimuli. Journal of Experimental Psychology: Animal Behavior Processes, 8, 49-61. Holen, A. (1988, October). A longitudinal study of the occurrence and persistence of post-traumatic health problems in disaster survivors. Paper presented at the meeting of the Society for Traumatic Stress Studies, Dallas, TX. Hollis, K. L., & Overmier, J. B. (1973). Effect of inescapable shock on efficacy of punishment of appetitive instrumental responding by dogs. Psychological Reports, 33, 903-906. Holt, P. & Kehoe, E. (1985). Cross-modal transfer as a function of similarities between training tasks in classical conditioning of the rabbit. Animal Learning and Behavior, 13, 51-59. Horowitz, M. J. (1980). Psychological response to serious life events. In V Hamilton & D. Warburton (Eds.), Human stress and cognition (pp. 235-263). New York: Wiley. Horowitz, M. J. (1986). Stress response syndromes. Northvale, NJ: Aronson. Hyson, R. L., Ashcraft, L. J., Drugan, R. C., Grau, J. W, & Maier, S. F. (1982). Extent and control of shock affects naltrexone sensitivity of stress-induced analgesia and reactivity to morphine. Biochemistry and Behavior, 17,1019-1025. Katz, A., Webb, L., & Stotland, E. (1971). Cognitive influences on the rate of GSR extinction. Journal of Experimental Research in Personality, 5, 208-215. Keane, T. M. (in press). Symptomatology of Vietnam veterans with post-traumatic stress disorder. In J. Davidson & E. B. Foa (Eds.), Post-traumatic stress disorder in review: Recent research and future directions. Washington, DC: American Psychiatric Press. Keane, T. M., Malloy, P. F, & Fairbank, J. A. (1984). Empirical develop-

235

ment of an MMPI subscale for the assessment of combat-related posttraumatic stress disorder. Journal of Consulting and Clinical Psychology, 52, 888-891. Kehoe, E. J., & Holt, P. E. (1984). Transfer across CS-US intervals and sensory modalities in classical conditioning of the rabbit. Animal Learning and Behavior, 12,122-128. Kehoe, E. J., Morrow, L. D., & Holt, P. E. (1984). General transfer across modalities survivors reduction in the original conditioned reflex in the rabbit. Animal Learning and Behavior, 12,129-136. Kendall, P. C, & Watson, D. (1989). Anxiety and depression: Distinctive and overlapping features. San Diego, CA: Academic Press. Kilpatrick, D. G, Best, C. L., Veronen, L. I, Villeponteaux, L. A., & Amick-McMullan, A. E. (1986, March). Predicting the impact of a stressful life experience: Criminal victimization. Presented at the 7th Annual Meeting of the Society of Behavioral Medicine, San Francisco. Kilpatrick, D. G, & Resnick, H. (1989, October). PTSD associated with exposure to criminal victimization in clinical and community populations. Position paper prepared for the DSM-IV Post-Traumatic Stress Disorder Advisory Group, San Francisco. Kilpatrick, D. G, & Resnick, H. (in press). PTSD associated with exposure to criminal victimization in clinical and community populations. In J. Davidson & E. B. Foa (Eds.), Post-traumatic stress disorder in review: Recent research and future directions. Washington, DC: American Psychiatric Press. Kilpatrick, D. G., Saunders, B. E., Amick-McMullan, A., Best, C. L., Veronen, L. J., & Resnick, H. S. (1989). Victim and crime factors associated with the development of crime-related post-traumatic stress disorder. Behavior Therapy, 20,177-198. Kolb, L. C. (1987). A neuropsychological hypothesis explaining posttraumatic stress disorders. American Journal of Psychiatry, 144,989995. Konorski, J. (1967). Integrative activity of the brain. Chicago: University of Chicago Press. Krystal, H. (1990). An information processing view of object-relations. Psychoanalytic Inquiry, 10, 221-251. Kuch, K. (1989). Enigmatic disability after minor accidents. Modem Medicine of Canada, 44, 38-41. Lockard, J. S. (1963). Choice of a warning signal or no warning signal in an unavoidable shock situation. Journal ofComparative and Physiological Psychology, 56, 526-530. Mackintosh, N. J. (1983). Conditioning and associative learning. San Diego, CA: Academic Press. MacLeod, C, Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95,15-20. MacLeod, C, & Rutherford, E. M. (1990, November). Anxiety and the selective processing of emotional information: Mediating roles of awareness, trait and state variables, and personal relevance of stimulus materials. Presented at the Annual Meeting of the Association for the Advancement of Behavior Therapy, San Francisco. Maier, S. E, Albin, R. W, & Testa, T. J. (1973). Failure to learn to escape in rats previously exposed to inescapable shock depends on nature of escape response. Journal ofComparative and Physiological Psychology, 85, 581-592. Maier, S. F, Drugan, R., & Grau, J. (1982). Controllability, coping behavior, and stress-induced analgesia in the rat. Pain, 12, 47-56. Maier, S. E, & Keith, J. R. (1987). Shock signals and the development of stress-induced analgesia. Journal of Experimental Psychology: Animal Behavior Processes, 13, 226-238. Maier, S. F, & Seligman, M. E. P. (1976). Learned helplessness: Theory and evidence. Journal of Experimental Psychology, General, 105, 3-46. Maier, S. F, Sherman, J. E., Lewis, J. W, Terman, G. W, & Liebeskind, J. C. (1983). The opiod/nonopiod nature of stress-induced analgesia

236

E. FOA, R. ZINBARG, AND B. ROTHBAUM

and learned helplessness. Journal of Experimental Psychology: Animal Behavior Processes, 9, 80-90. Maier, S. E, & Warren, D. A. (1988). Controllability and safety signals exert dissimilar proactive effects on nociception and escape performance. Journal of Experimental Psychology: Animal Behavior Processes, 14,18-25. Malloy, P. E., Fairbank, J. A., & Keane, T. M. (1983). Validation of a multimethod assessment of post-traumatic stress disorder in Vietnam veterans. Journal of Consulting and Clinical Psychology, 51, 488-494. Marks, I. M. (1987). Fears, phobias, and rituals: Panic, anxiety, and their disorders. London: Oxford University Press. Marmar, C. R., & Freeman, M. (1988). Brief dynamic psychotherapy of post-traumatic stress disorders: Management of narcissistic regression. Journal of Traumatic Stress, J, 323-337. Masserman, J. H. (1943). Behavior and neurosis: An experimental psychoanalytic approach to psychobiologic principles. Chicago: University of Chicago Press. Masserman, J. H. (1971). The principle of uncertainty in neurotigenesis. In H. D. Dimmel (Ed.), Experimental psychopathology: Recent research and theory. San Diego, CA: Academic Press. Mathews, A., & Eysenck, M. (1987). Clinical anxiety and cognition. In H. J. Eysenck & I. Martin (Eds.), Theoretical foundation of behavior therapy. New York: Plenum Press. Mathews, A., Mogg, K., May, J., & Eysenck, M. (1989). Implicit and explicit memory bias in anxiety. Journal of Abnormal Psychology, 98, 236-240. McFall, M. E., Murburg, M. D., Ko, G. N, & Veith, R. C. (1991). Autonomic responses to stress in Vietnam combat veterans with post-traumatic stress disorder. Manuscript submitted for publication. McLeer, S., Deblinger, E, Atkins, M. S., Foa, E. B., & Ralphe, D. L. (1988). Post-traumatic stress disorder in sexually abused children. Journal of the American Academy of Child and Adolescent Psychiatry, 27, 650-654. Miller, S. M. (1981). Predictability and human stress: Towards a clarification of evidence and theory. In L. Berkowitz (Ed.), Advances in experimental social psychology (Vol. 14, pp. 204-254) San Diego, CA: Academic Press. Miller, S. M., & Grant, R. (1979). The blunting hypothesis: A view of predictability and human stress. In P. Sjoden, S. Bates, & W Dockens (Eds.), Trends in behavior therapy (pp. 135-151). San Diego, CA: Academic Press. Mineka, S. (1979). The role of fear in theories of avoidance learning, flooding, and extinction. Psychological Bulletin, 5, 985-1010. Mineka, S. (1985). Animal models of anxiety based disorders. In R. Tuma& J. Maser (Eds.), Anxiety and anxiety disorders (pp. 199-244). Hillsdale, NJ: Erlbaum. Mineka, S., Cook, M., & Miller, S. (1984). Fear conditioned withescapable and inescapable shock: Effects of a feedback stimulus. Journal of Experimental Psychology: Animal Behavior Processes, 10, 307323. Mineka, S., & Hendersen, R. W. (1985). Controllability and predictability in acquired motivation. Annual Review of Psychology, 36, 495529. Mineka, S., & Kelly, K. A. (1989). The relationship between anxiety, lack of control, and loss of control. In A. Steptoe & A. Appelo (Eds.), Stress, personal control and health. New 'York: Wiley. Mineka, S., & Kihlstrom, J. F. (1978). Unpredictable and uncontrollable events: A new perspective on experimental neurosis. Journal of Abnormal Psychology, 2, 256-271. Minor, X, Dess, N., & Overmier, J. (1989). Inverting the traditional view of "learned helplessness": A reinterpretation in terms of anxiety and modulator operations. In M. R. Denny (Ed.), Aversive events and behavior. Hillsdale, NJ: Erlbaum.

Minor, T. & Lolordo, V (1984). Escape deficits following inescapable shock: The role of contextual odor. Journal of Experimental Psychology: Animal Behavior Processes, 10,168-181. Minor, X, Trauner, M., Lee, C., & Dess, N. (1990). Modeling signal features of escape response: Effects of cessation conditioning in "learned helplessness" paradigm. Journal of Experimental Psychology: Animal Behavior Processes, 16,123-126. Mogg, K., Mathews, A., & Weinman, J. (1987). Memory bias in clinical anxiety. Journal of Abnormal Psychology, 96, 94-98. Mowrer, H., & Viek, P. (1948). An experimental analogue of fear from a sense of helplessness. Journal of Abnormal and Social Psychology, 43, 193-200. Moye, T. B., Hyson, R. L., Grau, J. W, & Maier, S. F. (1983). Immunization of opiod analgesia: Effects of prior escapable shock on subsequentshock-induced and morphine-inducedantinociception. Learning and Motivation, 14, 238-251. Odling-Smee, F. J. (1975). Background stimuli and the inter-stimulus interval during Pavlovian conditioning. Quarterly Journal of Experimental Psychology, 27, 387-392. Ohman, A. (1979). The orienting response, attention and learning: An information-processing perspective. In H. D. Kimmel, E. H. van Olst, & J. F. Orlebeke (Eds.), The orienting reflex in humans (pp. 443-472). Hillsdale, NJ: Erlbaum. Ohman, A. (1986). Face the beast and fear the face: Animal and social fears as prototypes for evolutionary analyses of emotion. Psychophysiology, 23, 123-145. Osborne, F H., Mattingly, B. A., Redmon, W K., & Osborne, J. S. (1975). Factors affecting the measurement of classically conditioned fear in rats following exposure to escapable versus inescapable signalled shock. Journal of Experimental Psychology: Animal Behavior Processes, 1, 364-373. Overmier, B. J. (1968). Interference with avoidance behavior: Failure to avoid traumatic shock. Journal of Experimental Psychology, 78, 340343. Overmier, B. J., Murison, R., Skoglund, E. J., & Ursin, H. (1985). Safety signals can mimic responses in reducing the ulcerogenic effects of prior shock. Physiological Psychology, 13, 243-247. Overmier, B., & Seligman, M. (1967). Effects of inescapable shock upon subsequent escape and avoidance responding. Journal of Comparative and Physiological Psychology, 63, 28-33. Pallmeyer, X P., Blanchard, E. B., & Kolb, L. C. (1986). The psychophysiology of combat induced post-traumatic stress disorder in Vietnam veterans. Behaviour Research and Therapy, 24, 645-652. Pavlides, C., & Winson, J. (1989). Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. Journal of Neuroscience, 9, 2907-2918. Pavlov, I. P. (1927). Conditioned reflexes. London: Oxford University Press. Pearl, J., Walters, G. C, & Anderson, D. C. (1964). Suppressing effects of aversive stimulation on subsequently punished behaviour. Canadian Journal of Psychology, 18, 343-355. Perkins, C. C. (1968). An analysis of the concept of reinforcement. Psychological Review, 75, 155-172. Perkins, C. (1971). Reinforcement in classical conditioning. In H. Kendler & J. X Spence (Eds.), Essays in neobehaviorism: A memorial volume to Kenneth W Spence (pp. 113-136). New York: AppletonCentury-Croft. Perloff, L. S. (1983). Perception of vulnerability to victimization. Journal of Social Issues, 39, 41-61. Pitman, R. K. (1989, October). Biological findings in PTSD: Implications for DSM-IV classification. Position paper presented for the DSM-IV Post-Xraumatic Stress Disorder Advisory Group, San Francisco. Pitman, R. K., Altman, B., & Macklin, M. L. (1989). Prevalence of

AN ANIMAL MODEL OF PTSD posttraumatic stress disorder in wounded Vietnam veterans. American Journal of Psychiatry, 146, 667-669. Pitman, R. K., Orr, S. P., Forgue, D. F., Altaian, B., & Herz, L. R. (1990). Psychophysiologic responses to combat imagery of Vietnam veterans with post-traumatic stress disorder vs. other anxiety disorders. Journal of Abnormal Psychology, 99, 49-54. Pitman, R. K., Orr, S. P., Forgue, D. F, deJong, J. B., & Claiborn, J. M. (1987). Psychophysiologic assessment of post-traumatic stress disorder imagery in Vietnam combat veterans. Archives of General Psychiatry. 14, 970-975. Pitman, R. K., van der Kolk, B. A., Orr, S. P., & Greenberg, M. S. (1990). Naloxone-reversible analgesic response to combat-related stimuli in post-traumatic stress disorder: A pilot study. Unpublished manuscript. Putnam, F. W, Guroff, J. 1, Silberman, E. K., Barban, L., & Post, R. M. (1986). The clinical phenomenology of multiple personality disorder: 100 recent cases. Journal of Clinical Psychiatry, 47, 285-293. Rachman, S. (1989). Fear and courage (2nd ed.). New York: W H. Freeman. Randich, A. (1981). The US preexposure phenomenon in the conditioned suppression paradigm: A role for conditioned situational stimuli. Learning and Motivation, 12, 321-341. Randich, A., & LoLordo, V M. (1979). Associative and nonassociative theories of the UCS preexposure phenomenon: Implications for Pavlovian conditioning. Psychological Bulletin, 86, 523-548. Rescorla, R. A. (1971). Variation in the effectiveness of reinforcement and nonreinforcement following prior inhibitory conditioning. Learning and Motivation, 2,113-123. Rescorla, R. A. (1988). Pavlovian conditioning: It's not what you think it is. American Psychologist, 43,151-160. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. Black & W F. Prokasy (Eds.), Classical conditioning II. New York: Appleton-Century-Crofts. Resnick, H., Veronen, L. J., Saunders, B., Kilpatrick, D. G., &Cornelison, V (1989). Assessment of PTSD in a subset of rape victims at 12 to 36 months post-assault. Unpublished manuscript. Riggs, D., Foa, E. B., Rothbaum, B. O, & Murdock, T. (1991). Post-traumatic stress disorder following rape and non-sexual assault: A predictive model. Unpublished manuscript. Rosellini, R., Warren, D., & DeCola, J. (1987). Predictability and controllability: Differential effects upon contextual fear. Learning and Motivation, 18, 392-420. Rosellini, R., Widman, D, Abrahamsen, G., & Bassuk, A. (1990). Reinstatement offear following uncontrollable and/or unpredictable stress. Unpublished manuscript. Ross, R. T., & Randich, A. (1985). Associative aspects of conditioned analgesia evoked by a discrete CS. Animal Learning and Behaviour, 13, 419-431. Rothbaum, B. O., Foa, E. B., Riggs, D, Murdock, T, & Walsh, W (in press). Post-traumatic stress disorder in rape victims. Journal ofTraumatic Stress. Rush, D. K., Mineka, S., & Suomi, S. J. (1982). The effects of control and lack of control on active and passive avoidance in Rhesus monkeys. Behaviour Research and Therapy, 20,135-152. Saigh, P. A. (1988). Anxiety, depression, and assertion across alternating intervals of stress. Journal of Abnormal Psychology, 97,338-341. Schreurs, B. & Kehoe, E. (1987). Cross-modal transfer as a function of initial training level in classical conditioning with the rabbit. Animal Learning and Behavior, 15, 47-54. Schultz, R., Braum, B. G., & Kluft, R. P. (1985, October). Creativity and imaginary companion phenomena: Prevalence and phenomenology in MPD. Paper presented at the Second International Conference on Multiple Personality/Dissociative States, Chicago.

237

Seligman, M. E. P. (1968). Phobias and preparedness. Behavior Therapy, 2, 307-320. Seligman, M. E. P. (1975). Helplessness: On depression, development and death. San Francisco, CA: Freeman. Seligman, M. E. P., & Binik, Y M. (1977). The safety signal hypothesis. In H. Davis & H. M. B. Hurwitz (Eds.), Operant Pavlovian interactions. Hillsdale, NJ: Erlbaum. Seligman, M. E. P., & Maier, S. (1967). Failure to escape traumatic shock. Journal of Experimental Psychology, 74,1-9. Sines, J., Cleeland, C, & Adkins, J. (1963). The behavior of normal and stomach lesion susceptible rats in several learning situations. The Journal of Genetic Psychology, 102, 91-94. Smith, E. M., & North, C. S. (1988). Aftermath of a disaster: Psychological response to the Indianapolis Ramada jet crash (Quick Response Research Report No. 23). Boulder, CO: Natural Hazards Research and Applications Information Center. Speed, N., Engdahl, B., Schwartz, I, & Eberly, R. (1989). Posttraumatic stress disorder as a consequence of the POW experience. Journal of Nervous and Mental Disease, 177,1447-1453. Starr, M. D., & Mineka, S. (1977). Determinants of fear over the course of avoidance learning. Learning and Motivation, 8, 332-350. Staub, E., Tursky, B., & Schwartz, G. E. (1971). Self-control and predictability: Their effects on reactions to aversive stimulation. Journal of Personality and Social Psychology, 18,157-162. Szpiler, J. A., & Epstein, S. (1976). Availability of an avoidance response as related to autonomicarousa\. Journal of Abnormal Psychology, 85, 73-82. Tellegen, A. (1985). Structures of mood and personality and their relevance to assessing anxiety, with an emphasis on self-report. In A. H. Tuma & J. D. Maser (Eds.), Anxiety and the anxiety disorders. Hillsdale, NJ: Erlbaum. Terman, G., Shavit, Y, Lewis, J., Cannon, J., & Liebeskind, J. (1984). Intrinsic mechanisms of pain inhibition and their activation by stress. Science, 226,1270-1277. Tsuda, A., & Hirai, H. (1975). Effects of the amount of required coping response taskson gastrointestinal lesions in rats. Japanese Psychological Research, 17,119-132. van der Kolk, B. A. (1987). Psychological trauma. Washington, DC: American Psychiatric Press. van der Kolk, B. A., Greenberg, M. S., Boyd, H., & Krystal, J. (1985). Inescapable shock, neurotransmitters, and addiction to trauma: Toward a psychology of post-traumatic stress. Biological Psychiatry, 20,314-325. van der Kolk, B. A., Pitman, R. K., & Orr, M. S. (1989). Endogenous opiods, stress-induced analgesia and post-traumatic stress disorder. Psychopharmacology Bulletin, 25,108-112. Volpicelli, J. R., Ulm, R. R., & Altenor, A. (1984). Feedback during exposure to inescapable shocks and subsequent shock-escape performance. Learning and Motivation, 15, 279-286. Wagner, A. R. (1979). Habituation and memory. In A. Dickinson & R. A. Boakes(Eds-), Mechanisms of learning and motivation (pp. 5382). Hillsdale, NJ: Erlbaum. Wagner, A. R. (1981). SOP: A model of automatic memory processing in animal behavior. In N. Spear & R. Miller (Eds.), Information processing in animals: Memory mechanisms (pp. 5-47). Hillsdale, NJ: Erlbaum. Wagner, A. R., & Rescorla, R. A. (1972). Inhibition in Pavlovian conditioning: Applications of a theory. In R. A. Boakes & M. S. Halliday (Eds.), Inhibition and learning (pp. 301-336). San Diego, CA: Academic Press. Warren, D., Rosellini, R., & Maier, S. (1989). Fear, feedback, and stressor controllability. InG. H. Bower (Ed.), TVie psychology of'learn-

238

E. FOA, R. ZINBARG, AND B. ROTHBAUM

ing and motivation (Volume 24, pp. 167-207). San Diego, CA: Academic Press. Watkins, L., & Meyer, D. (1982). Organization of endogenous opiate and nonopiate pain control systems. Science, 216,1185-1192. Weisman, R., & Litner, J. (1972). The role of Pavlovian events in avoidance training. In R. Brooks & M. Halliday (Eds.), Inhibition and learning. San Diego, CA: Academic Press. Weiss, J. M. (1968). Effects of coping responses on stress. Journal of Comparative and Physiological Psychology, 65, 251-260. Weiss, J. M. (1970). Somatic effects of predictable and unpredictable shock. Psychosomatic Medicine, 32, 397-408. Weiss, J. M. (197 la). Effects of coping behavior in different warning signal conditions on stress pathology in rats. Journal ofComparative and Physiological Psychology, 77, 1-13. Weiss, J. M.(1971b). Effects of punishing the coping response (conflict)

on stress pathology in rats. Journal ofComparative and Physiological Psychology, 77, 14-21. Weiss, J. M., Glazer, H. L, & Pohorecky, L. A. (1976). Coping behavior and neurochemical changes: An alternative explanation for the original "learned helplessness" experiments. In A. Seban & A. Kline (Eds.), Animal models in human psychobiology (pp. 141-173). New \brk: Plenum Press. Wine, J. (1971). Test anxiety and direction of attention. Psychological Bulletin, 76,92-104. Winson, J. (1972). Interspecies differences in the occurrence of theta. Behavioral Biology, 7, 479-487. Winson, J. (1990). The meaning of dreams. Scientific American, 263, 86-96. Wolpe, J. (1952). Experimental neuroses as learned behavior. British Journal of Psychology, 43, 243-268.

Appendix Diagnostic and Statistical Manual of Mental Disorders Criteria for Post-Traumatic Stress Disorder A. Trauma B. Reexperiencing(needl) 1. Intrusive distressing recollections 2. Nightmares 3. Flashbacks 4. Emotional distress on reminders C. Avoidance (need 3) 1. Avoid thoughts or feelings 2. Avoid activities-situations 3. Psychogenic amnesia 4. Decreased interest in activities 5. Detachment from others 6. Restricted range of affect 7. Foreshortened future

D. Arousal (need 2) 1. Sleep problems 2. Irritability-outbursts of anger 3. Problems concentrating 4. Hypervigilance 5. Exaggerated startle 6. Physiological reactivity on reminders E. Duration at least 1 month

Received November 28,1990 Revision received October 11,1991 Accepted October 14,1991

Hill Appointed Editor of the Journal of Counseling Psychology, 1994-1999 The Publications and Communications Board of the American Psychological Association announces the appointment of Clara E. Hill, PhD, University of Maryland, as editor of the Journal of Counseling Psychology for a 6-year term beginning in 1994. As of January 1, 1993, manuscripts should be directed to Clara E. Hill, PhD Department of Psychology University of Maryland College Park, Maryland 20742 Manuscript submission patterns for the Journal of Counseling Psychology make the precise date of completion of the 1993 volume uncertain. The current editor, Lenore W. Harmon, PhD, will receive and consider manuscripts until December 31,1992. Should the 1993 volume be completed before that date, manuscripts will be redirected to Dr. Hill for consideration in the 1994 volume.