FRANKLIN D. MCMILLAN

Best Friends Animal Society, Kanab, Utah, USA

The knowledge that severe adversity can cause long-term psychological and physiological problems in humans has been recognized for centuries. ‘Trauma’, the ancient Greek word meaning ‘to wound’ or ‘pierce’, first referred to the bodily injury suffered by soldiers from the piercing of their armor (Spiers and Harrington, 2001). In the more recent use of the term, particularly in the human psychological and psychiatric literature, trauma is now understood as a wound inflicted upon the mind as well as the body (Ray, 2008). Despite the longstanding recognition of stress-induced changes, the characteristic syndrome of psychological trauma only attained formal recognition when, in 1980, the American Psychiatric Association included in the Diagnostic and Statistical Manual of Mental Disorders (DSM-III) a new category, called posttraumatic stress disorder (PTSD) (Nayback, 2009). From a retrospective viewpoint, the disorder that is now known as PTSD first appeared in the official nomenclature when the first edition of the DSM in 1952 described the syndrome under the name ‘gross stress reaction’ (Andreasen, 2010).

In general, physical and psychological processes of an organism return to a baseline state of homeostasis after disruption. Recent studies in humans and nonhuman animals (hereafter animals) have shown that following experiences of severe psychological stress a homeostatic psychological state may not be reestablished, especially with diversity that is prolonged or repetitive in nature (Wilson, 2004). Rather than return to homeostasis the mind-body undergoes persistent dysfunction, often continuing to operate as if the trauma were perpetual and ongoing in daily life (Wilson, 2004). The different forms that this enduring dysfunction can take are what constitute posttraumatic psychopathology.

14.1.1 Indistinct concepts and terminology

A major problem pervades the field of psychological trauma: the inherently indistinct lines between the most fundamental concepts, including pathological versus nonpathological, adaptive versus maladaptive, normal versus impaired function, and clinically significant versus not clinically significant changes (Marshall et al., 1998; Wakefield and Horwitz, 2010; Joseph, 2011). Questions persist as to whether firm lines exist to distinguish these basic concepts or if they each constitute a dimensional continuum.

14.1.2 What is psychological trauma?

In both scientific and everyday usage, psychological trauma has had two meanings. It is used to refer to the stressful stimulus or event, such as ‘the dog was exposed to trauma’, or to the response to the stressful stimulus or event, such as ‘the dog experienced psychological trauma’. This double meaning conflates the injury with the incident. When an event is deemed ‘traumatic’, the assumption is that the event, by definition, results in injury (Gist and Devilly, 2010). However, the well-established fact that multiple individuals exposed to the same aversive stimulus or event will experience a diverse array of psychological outcomes (Ruscio et al., 2002) demonstrates that trauma is not the event, but rather the response of individuals to that event. In this context it is important to stipulate that the aversive, stressful events are potentially traumatic and that trauma is what occurs within an individual during and after exposure to the event (O’Donnell et al., 2010). In this chapter the term ‘potentially traumatic event’ (PTE) will be used to maintain clarity that the event itself is not traumatic and the reactions of those exposed may for some individuals never reach a pathologic level of intensity or duration (Gist and Devilly 2010), and ‘trauma’ will be used to denote the response, not the stressor.

14.1.3 Psychological trauma: Considerations when comparing humans and animals

A large body of research has demonstrated that despite the influence of higher cognitive functions in humans, basic emotional processes are shared by humans and other mammals (Panksepp, 1998). Strong evidence also indicates commonalities across species in psychopathological processes. Brain structures and neuroendocrine mechanisms implicated in mood and anxiety disorders are shared across a wide range of vertebrates, and vulnerability, risk, and protective factors for stress- and trauma-related psychopathology also appear to operate similarly among higher animals (Panksepp, 1998). Nevertheless, despite the shared brain structures and emotional processes, a number of factors must be taken into consideration when comparing psychopathology in humans and animals.

Language and cognitive barriers

Among the most formidable challenges we encounter in our attempts to understand psychological processes in nonhuman species involve the limitations in the animals’ capacities for introspection of their subjective experiences and the language barrier, which impair their ability to convey the content of their thought processes (and/or our ability to interpret their communications). These barriers greatly impair our ability to acquire two types of information highly relevant to the assessment of psychological trauma in any species: historical information and information about one’s subjective experiences. From a comparative perspective, the same challenge occurs in very young children, where research has shown that because of limited verbal expression capabilities, assessment criteria need to be more behaviorally anchored (Scheeringa, 2016).

Historical information

The histories of companion animals are almost always incomplete, since unless the current caregiver raised the animal from birth, the experiences that that animal was exposed to or deprived of may be omitted from the animal’s records or unknown altogether. This is true not just for the obvious cases of stray and shelter animals, but also for animals purchased as pets from reputable sources, since some stressful event may have occurred prior to the purchase, including the first 8 weeks of life. Moreover, due to the abundant research on the effects of maternal stress on the prenatal neuroendocrine development of mammalian fetuses (Braastad, 1998), an accurate history of adversity needs to also include maternal experiences throughout pregnancy.

The deficiencies in historical information create two major diagnostic problems. First, as will be discussed in more detail later, inadequate socialization ¹ in early life may result in later behaviors – predominantly fear-based – that often closely resemble those resulting from psychological trauma. Second, the diagnoses of certain trauma- and stressor-related disorders is contingent on historical information before and after a stressful event to distinguish pre-existing conditions from effects. Specifications in the diagnostic criteria, in particular ‘not present before trauma’ or ‘beginning after the traumatic event(s) occurred’ (American Psychiatric Association, 2013), cannot be met when the individual’s history prior to such an event is unknown. Child psychology research has shown that there is no feasible way to obtain information about traumatic events from the victims themselves if the children are too young to verbalize experiences (Scheeringa, 2016).

Information about subjective experiences

The current ‘gold standard’ for the diagnosis of posttraumatic disorders in humans is the diagnostic criteria set forth in the fifth edition of the DSM, which rely heavily on patients’ subjective reports of their experiences and internal states (Pitman et al., 2012). Clearly, the subjective experiences of some symptoms such as recurrent, involuntary, and intrusive distressing memories of the traumatic event(s); dissociative flashbacks; nightmares; and an inability to remember important aspects of the traumatic event(s) cannot be confirmed (or modeled) in animals and may only be inferred from nonverbal behavioral and other measures (e.g., physiological measurements, brain imaging) (Foa et al., 1992; Whitaker et al., 2014; Richter-Levin et al., 2018). This, as for incomplete histories, is not exclusive to animals, for although inaccessibility to subjective states applies to all animals it also applies to some humans, such as infants, some mentally disabled individuals, and persons with dementia (Ferdowsian et al., 2011).

14.2 Adaptive Fear Responses

The emotion of fear – consisting of physiological, perceptual, and psychological elements – elicits highly adaptive behavioral responses when real or perceived threats endanger the life or well-being of the individual (Rosen and Schulkin, 1998). Behavioral responses are traditionally grouped into three categories: flight, fight, or freeze (Wiedenmayer, 2004). Lang (1977) has described the concept of a fear structure, which is conceived of as a neural program for escape or avoidance behavior containing information about the feared stimulus, the behavioral responses, and the appraised meanings of both stimulus and responses. Activation of a fear structure occurs when the animal perceives environmental cues that correspond to information represented in the structure, which coordinates and monopolizes brain resources for the purpose of enhancing the animal’s ability to defend against a challenge (LeDoux, 2012). When a fear structure accurately represents threats in the world it serves as a blueprint for effective action, which, in conjunction with its motivational function, results in the production of self-protective behavior (Rosen and Schulkin, 1998; Cahill and Foa, 2007; LeDoux, 2012).

Fears are either innate (hard-wired) or learned. Most relevant to the phenomenon of psychological trauma is the latter, for, as we will see, trauma commonly (though not always) occurs as a result of a fearful experience and then manifests as a fear or anxiety disorder. Evidence indicates that the evolutionary development of fear-learning mechanisms was guided by the fact that the likelihood of injury or death is strongly linked to the speed, strength, and duration of learned fears. In situations where the animal perceives a high risk of injury, subsequent exposure to this stimulus or situation could have fatal consequences and therefore fast-learning mechanisms that can immediately alter behavioral responses, as occurs in one-trial learning, are of high fitness priority (Wiedenmayer, 2004). In a recent review of research on the formation of learned fears in animals, Wiedenmayer (2004) presented findings from studies with rats demonstrating that a single aversive experience may alter synaptic transmission in components of the fear pathway such as the amygdala, hippocampus, and periaqueductal gray, and profoundly affect an animal’s behavioral, psychological, and physiological responsivity. Such neural alterations may persist for extended periods of time and appear to underlie long-term behavioral changes after the threat.

The paradigm of fear conditioning has become the first choice for studying the neural basis of fear learning and, more recently, the memory-related aspects of PTSD-like symptoms (Siegmund and Wotjak, 2006). In this particular form of classical conditioning, a biologically neutral stimulus (conditioned stimulus, CS) acquires threat status when it occurs in association with a biologically significant threat (unconditioned stimulus, US) (LeDoux, 2012).

Crucial for the understanding of psychological trauma is that the learning involved with an aversive experience involves two processes: generalization and sensitization. In fear conditioning neural connections form to associate not only the CS, but also the contextual cues of the environment, with the US (Wiedenmayer, 2004). The process of generalization accounts for how traumatic reactions can broaden to involve not only stimuli clearly related to the traumatic event (trauma-related cues, TRCs), but also to stimuli seemingly unrelated (Monson et al., 2007). Sensitization, on the other hand, is a nonassociative form of learning that refers to an increased responsivity after an aversive event to the TRCs and in some cases to other, even harmless, stimuli (Wiedenmayer, 2004). Through sensitization, the animal becomes more reactive each time a nonthreatening stimulus is encountered, which can result in problematic responses such as hyperexcitability and exaggerated fear responses (Mills, 2009). Both generalization and sensitization appear to contribute to the emotional disturbances in posttraumatic distress (Parsons and Ressler, 2013).

For situations and stimuli which continue to pose a potential risk for an individual, retention of fear memories and responses is adaptive. However, when the risk subsides it is biologically costly to retain highly reactive fear responses for nonthreats, and in such situations memory-modulating mechanisms – e.g., fear extinction, habituation, de-sensitization, or forgetting – serve to restrict the duration of memory storage and ensure that only relevant features are retained (Wiedenmayer, 2004). Memory-modulating mechanisms may allow animals to gradually trade off threat-related behaviors with other activities more relevant to current needs. The phenomenology and neurocircuitry of fear conditioning and extinction are highly conserved among humans and many other animal species (Bonne et al., 2004; LeDoux, 2012; VanElzakker et al., 2014).

14.3 Posttraumatic Psychopathology in Humans and Animals

The changed behavior elicited by normal fear responses is of clear survival value in protecting animals from danger. However, fear mechanisms, like any other biological process, are vulnerable to dysfunction. When this occurs, adaptive, nonpathological responses cross over to become maladaptive and pathological. What is not at all clear is at what ‘level’ this occurs; that is, where any line might exist that distinguishes pathologic behavior and adaptive, high levels of fear (Marshall et al., 1998; Wakefield and Horwitz, 2010). In addition, many gaps remain in our understanding of how traumatic events produce the changes constituting longer-lasting and pathologic sequelae, including reduced thresholds for activation and hyperexcitability in fear circuits and disruption of memory-modulating mechanisms regulating the balance between learning and forgetting, resulting in an emotional event being stored for an excessive period of time (Rosen and Schulkin, 1998; Wiedenmayer, 2004). The work in this area will be discussed in the section on the pathophysiology of PTSD.

Acknowledging the indeterminacy of any line separating normal from pathological fear, Foa and Kozak (1986) have proposed criteria for such a distinction. They suggested that a fear structure is pathological or maladaptive when the following characteristics are present: (i) associations among stimulus elements are inaccurate or unrealistic; (ii) harmless stimuli and response elements are erroneously associated with threat meaning; (iii) physiological and escape/avoidance responses are evoked by harmless stimuli; and (iv) excessive and easily triggered response elements interfere with normal, adaptive behavior.

Transitioning from a discussion on pathological fear to posttraumatic psychopathology in general requires a brief explanation. Historically, a large proportion of pathophysiology research on psychological trauma, and in particular PTSD, has focused on fear mechanisms, and hence there is much overlap between fear research and PTSD research. However, as Friedman et al. (2007b) have noted, since other emotions, such as sadness, grief, anger, guilt, shame, and disgust, are also associated with PTSD, it would be inappropriate to conceptualize this disorder entirely within the context of fear-based appraisals and reactions. Reflecting the emphasis of the trauma literature on fear, the discussions of psychological trauma in this chapter will be predominantly about this particular emotion. Throughout, however, it bears keeping in mind that while pathological fear constitutes much of posttraumatic psychopathology, the two phenomena are not equivalents.

The challenge of identifying lines between adaptive and pathologic fear can be broadened to psychopathology in general. As is the case for fear specifically, while a definitive line dividing nonpathological and pathological may be not be possible for mental disorders as a whole, there is little debate that at some point nonpathological crosses over to pathological. The DSM-5 (American Psychiatric Association, 2013) approaches this by defining mental disorder as:

The formal recognition of PTSD (defined below) in 1980 was accompanied by the realization that PTSD fell short of capturing the full range of posttraumatic responses and psychological injuries, which vary in both type and severity. Epidemiological studies have shown that PTSD symptoms are not the only, indeed not even the most likely, type of posttraumatic reactions; other types include specific phobia, generalized anxiety disorder (GAD), and mood disorders (O’Donnell et al., 2004; Rosen et al., 2010a). It is now accepted that the reactions to overwhelming psychological stressors are best understood as a spectrum of conditions rather than as a single disorder (Herman, 1997; Briere and Spinazzola, 2005; Bryant, 2010), and in this chapter ‘spectrum’ will refer to this array of different types of posttraumatic pathologic responses.

14.3.1 Posttraumatic stress

In addition to the diagnosis of PTSD referring to just one type of response to trauma, it also represents only one level of severity, namely, very severe. This de-emphasizes, if not ignores, the less severe forms of this particular type of posttraumatic response (Norris and Slone, 2007). On this issue of severity, a major point of debate is whether PTSD is a dimensional condition differing only quantitatively from milder and normal reactions to stressful events or whether it is a discrete syndrome qualitatively different from less severe and normative stress reactions (Ruscio et al., 2002). It is known that not everyone exposed to a PTE will develop the full complement of symptoms of PTSD, but most people will develop some emotional distress following the adversity (Joseph, 2011). To address this question Ruscio et al. (2002) conducted multiple taxometric procedures in a large sample of male combat veterans to determine the latent structure of PTSD. They found that PTSD was best characterized as a dimensional disorder rather than as a categorical structure that views PTSD as a qualitatively distinct clinical syndrome served by a dichotomous diagnostic breakdown of ‘PTSD’ and ‘no PTSD’ (Ruscio et al., 2002).

This dimensional view suggests that posttraumatic distress symptoms are distributed along a mild-to-severe continuum and individuals who meet current PTSD diagnostic criteria generally represent those affected most severely (Briere and Spinazzola, 2005; Friedman et al., 2007b). However, there would be no distinct line that would qualitatively separate these individuals from those exhibiting less severe signs (see Fig. 14.1). It has been proposed that this continuum be referred to by the term posttraumatic stress (PTS, and will be used in this chapter), and that once posttraumatic stress reaches a certain level of intensity the individual experiencing it is said to have PTSD (Joseph, 2011). This chapter will espouse the dimensional interpretation of PTS and PTSD, and will use the term PTSD when referring to research that has used a categorical view. In addition, ‘continuum’ will refer to the gradations of severity of PTS responses as depicted in Fig. 14.1.

New terminology to describe the forms of PTS exhibited by victims who experience substantial psychological impairment and distress but fall below the diagnostic threshold of PTSD is not consistent among researchers; the terms include subthreshold, subsyndromal, and partial PTSD (Bergman et al., 2017). In a recent review, Bergman et al. (2017) found that the majority of articles used the term subthreshold PTSD, which will be used in this chapter. As the term implies, subthreshold PTSD denotes a condition consisting of the presence of some symptoms of PTSD, but the number and intensity of the symptoms fail to reach the diagnostic threshold for the disorder as described in the DSM (Ruscio et al., 2002; Cukor et al., 2010). In contrast to subthreshold forms of PTS, the condition in which all the diagnostic criteria have been met is referred to most commonly as simply PTSD, but has also been termed full and full-threshold PTSD (Friedman et al., 2007b; American Psychiatric Association, 2013) as well as full-blown PTSD (Bergman et al., 2017). Other methods of describing the PTS continuum have been used, such as the notion that subthreshold PTSD be considered an ‘intermediate phenotype’ of the disorder, and individuals would be ‘affected, intermediate, and non-affected’ (Richter-Levin et al., 2018).

The validity and clinical relevance of subthreshold PTSD has been questioned since it was first used with the Vietnam veteran population (Cukor et al., 2010), but lending credence to the concept is the clinically significant difference between those with PTSD, subthreshold PTSD, and no symptoms (Cukor et al., 2010). By multiple measures – functional impairment, severity of symptoms, wanting or needing treatment, healthcare utilization, distress, psychological well-being, psychological impairment, and quality of life – subthreshold PTSD falls between full PTSD and having no disorder (Norris and Slone, 2007; Cukor et al., 2010; Brancu et al., 2016; Bergman et al., 2017).

Subthreshold PTSD consists of different conditions and courses. Subthreshold PTSD groups may include individuals with PTSD who have partially remitted to subthreshold status, vulnerable patients whose symptoms will develop into late-onset full PTSD, and individuals who will remain at chronic, subthreshold levels (Cukor et al., 2010; Brancu et al., 2016; Bergman et al., 2017).

Studies investigating the prevalence of subthreshold PTSD have been hampered by the variability of diagnostic criteria among researchers, but it is clear that subthreshold PTSD is prevalent among PTE-exposed individuals (Cukor et al., 2010; Brancu et al., 2016). Norris and Slone (2007) summarized the epidemiology of PTSD by noting that at any one point of time there are at least one to two times as many individuals in the current population with severe subthreshold PTSD as those with full PTSD. The recognition of the concept of subthreshold PTSD has engendered ongoing debate among human mental health professionals, as the concern about the possibility that creating a subthreshold diagnosis may pathologize normal responses to extreme adversity must be continually weighed against the possibility of ignoring the needs of a crucial subpopulation of individuals who experience significant psychopathology and functional impairment (Cukor et al., 2010; Bergman et al., 2015).

Posttraumatic stress disorder

Posttraumatic stress disorder is one of the most severe outcomes of exposure to a severely aversive event. At present, PTSD is not a well-defined disorder. The definition and diagnosis of PTSD in humans is based on behavioral symptoms and self-reports, without any objective parameters (Richter-Levin et al., 2018). PTSD is not defined by or composed of the immediate responses to trauma exposure: it is rather a disorder of the more chronic, lingering symptoms.

The clinical diagnosis of PTSD is made only if an individual exhibits a certain number of symptoms from each of four well-defined symptom clusters for a certain period of time. As specified in the DSM-5 (American Psychiatric Association, 2013), in addition to the history of exposure to actual or threatened death, serious injury, or sexual violence, the four symptom clusters that distinguish PTSD from other posttraumatic psychological disturbances are unwanted intrusions of memories of the traumatic event, often in the form of dissociation, flashbacks, and nightmares; avoidance of anything reminiscent of the traumatic event; negative alterations in cognition and mood; and alterations in arousal and reactivity, including hyperarousal symptoms such as hypervigilance and increased startle response. Additional diagnostic elements include: the components within these symptom clusters must begin or worsen after the traumatic event(s) occurred, the duration of symptoms is greater than 1 month, and the disturbance causes clinically significant distress or impairment in social, occupational, or other important areas of functioning. On the basis of several decades of research demonstrating that children and adolescents can develop PTSD (Scheeringa et al., 2003), the fifth edition of the DSM has introduced a set of diagnostic criteria for children 6 years of age and younger, which require fewer and slightly recategorized symptoms than is set forth for humans over 6 years of age. Generally speaking, the diagnosis of PTSD is used in children and adolescents when intrusive memories, avoidance, and arousal symptoms are serious, continue, and interfere with daily functioning (Fairbank et al., 2007). Table 14.1 summarizes the criteria for children 6 years of age or less and is given the most attention in this chapter because of the similar challenges in animals and very young humans regarding documenting adult symptoms, such as the problem of obtaining reliable verbal self-reports.

Interindividual variability of PTSD symptom profiles is characteristic for the disorder in humans (Wilson, 2004). For example, in some individuals avoidance reactions may predominate, while others may experience mostly hyperarousal and reactivity. Any one symptom prominent in one individual may be minor or even absent in another.

The course of posttraumatic distress has been well characterized in humans. For the large majority of the population the distress after exposure to a PTE is limited to an acute, transient disturbance followed by complete recovery as neurobiological effects extinguish over time (Marshall et al., 1998; Friedman et al., 2007a; Rosen et al., 2010a; Sherin and Nemeroff, 2011). However, a substantial minority of traumatized individuals do not fully recover but go on to develop clinical problems that create ongoing distress of varying severity. Studies in human populations exposed to a PTE have been relatively consistent in showing that the incidence of PTSD falls between 15% and 35% for most types of trauma, including sexual assault, military combat, natural disaster, motor vehicle accident, captivity, or witnessing the death or serious injury of another individual (Santiago et al., 2013; VanElzakker et al., 2014). Thus, there are two trajectories following traumatic stress: normal transient distress (i.e., resilience; successful coping response) or chronic clinical morbidity/distress (unsuccessful or partially successful coping response). This does not mean that the transiently affected individuals are completely free of long-term effects, as memories of the event are likely to remain, but these memories do not significantly impair the individual’s functioning and enjoyment of life.

NEUROBIOLOGY AND PATHOPHYSIOLOGY OF PTSD The neurobiological mechanisms underlying PTSD are incompletely understood and have been recently reviewed (Southwick et al., 2007; Sherin and Nemeroff, 2011; Shalev et al., 2017). The following is a brief synopsis of some of the disorder’s key dysfunctional elements currently known or hypothesized.

Shalev et al. (2017) have suggested that four brain functions play a prominent role in the psychopathology of PTSD: (i) threat detection; (ii) contextual processing; (iii) fear learning; and (iv) emotion regulation and executive function. It is well accepted that, broadly conceived, the primary dysfunction in the disorder involves fear mechanisms; fear conditioning as well as fear sensitization and generalization processes contribute to both the development and maintenance of the disorder (Thoeringer and Wotjak, 2013; VanElzakker et al., 2014).

Classical fear conditioning has been a leading paradigm for research on the neural processes of PTSD. Fear conditioning is a normal learning process critical for animal survival, and its use in modeling PTSD is based on the assumption that the underlying neurobiology of PTSD is similar in principle to that of classical fear conditioning, only more intense (Richter-Levin et al., 2018). However, until this assumption is confirmed it remains possible that that PTSD is a result of the failure of the normal fear responses following exposure to a severe stressor, resulting in the development of an alternative, pathological process (Richter-Levin et al., 2018). Accordingly, Richter-Levin et al. (2018) have stressed the importance of efforts to differentiate the mechanisms underlying adaptive fear memory formation from those that contribute to the development of pathology.

Evidence indicates that disturbances in PTSD occur in several interacting brain regions involved in the regulation and integration of stress and fear responses, including the amygdala, hippocampus, anterior cingulate cortex, and prefrontal cortical regions (Heim and Nemeroff, 2009; Shalev et al., 2017). The pathophysiology of PTSD involves both sustained hyperactivity of the sympathetic branch of the autonomic nervous system and dysregulation and sensitization of the hypothalamic–pituitary–adrenocortical (HPA) axis (Friedman et al., 2007b; Heim and Nemeroff, 2009). The dysfunction in this system may be associated with changes in perception, memory, motivation, personality, cognitive processing, and interpersonal relations (Wilson, 2004).

A major conceptualization of PTSD highlights the role of the amygdala in processing threatening or fearful stimuli. The amygdala in PTSD becomes hyperresponsive to stimuli (trauma-related as well as non-trauma-related) and this excessive activation is accompanied by an abnormally low response in the brain regions, such as the medial prefrontal cortex, that exert inhibitory control on amygdala activity (Charney, 2004; Yehuda and LeDoux, 2007; VanElzakker et al., 2014). These changes are supported by neuroimaging studies in human patients with PTSD, which demonstrate that structures involved in fear expression over-activate while structures involved in fear inhibition under-activate or deactivate (VanElzakker et al., 2014). For most individuals, extinction learning causes fear responses to trauma-related stimuli to diminish over time, such that repeated exposure to TRCs in the absence of threat forms a new and less excitatory association that competes with the original fear memory (Quirk, 2002). However, in individuals with PTSD the extinction deficit associated with the inhibition failure of the amygdala permits conditioned fears, and the symptoms they elicit, to persist for months or years beyond the point that they would normally be extinguished (VanElzakker et al., 2014).

These two effects on fear – enhanced acquisition and impaired extinction – together result in a lowering of the threshold for fearful reactivity and prolongation of fear memories. In addition to this, PTSD is associated with an increased propensity for fear generalization (VanElzakker et al., 2014), which diminishes the individual’s capability to distinguish between safe and unsafe stimuli and to clearly identify danger (Bonne et al., 2004; Sherin and Nemeroff, 2011). The threatening context thereby expands to the extent that perceived danger becomes both imminent and unpredictable and almost every place is believed to be unsafe. Ultimately there is an overall loss of one’s sense of security – ‘the world is completely dangerous’ (Bonne et al., 2004; Cahill and Foa, 2007; Hembree and Foa, 2010; American Psychiatric Association, 2013).

The combined effect of these neurophysiological changes is an emotional appraisal process that is biased toward the perception of threat rather than safety, producing a response bias of overreaction rather than underreaction (Friedman, 2001). Rather than a normal level of alertness with relaxed attention, individuals with PTSD have an elevated baseline of arousal: the individual continues to function in a ‘red alert’ status of readiness – hypervigilant, hyperreactive, and primed for another stressful event (Wilson et al., 2001a; Wilson, 2004). Patients display an exaggerated startle response to unexpected stimuli (‘jumpiness’) and a pronounced reaction to TRCs, are often irritable, and they experience difficulties in sleep and concentration (Bonne et al., 2004; Wilson, 2004; Segman et al., 2007; American Psychiatric Association, 2013).

POSTTRAUMATIC STRESS DISORDER IN ANIMALS

Animal – Experimental. Extensive effort over many decades has been put forth to develop an animal model of PTSD. The specific emotional state that is the primary focus of investigation for many of these proposed models is conditioned fear (Siegmund and Wotjak, 2007) and these studies overlap with, and use the same stressors (e.g., restraint stress, exposure to predators, being held underwater, and foot- and tailshocks [Siegmund and Wotjak, 2006]) as are used in studies on fear conditioning (Southwick et al., 2007). Most animal models of PTSD are based on exposure to stressors that the victim cannot control, that are unpredictable, or are both (Mallonée, 2004). There is substantial agreement that in many of the animal models the physiological and behavioral disturbances following experimental psychological trauma often match the most prominent and cardinal features of PTSD in humans (Foa et al., 1992; Mallonée, 2004; Southwick et al., 2007). Specific psychobehavioral signs produced in these models include trauma-associated contextual fear, increased anxiety-like behaviors, exaggerated startle responses, hyperarousal, avoidance behavior, cognitive impairment, and reduced social interaction (Thoeringer and Wotjak, 2013).

Some of the models include re-exposure to TRCs at a later time, which appears to replicate the events in PTSD in which the person’s functional impairments and distress persist as a result of periodical encounters with reminders of the trauma (e.g., a car backfiring, which resembles the sound of gunfire during military combat). For example, in one study with rats (Louvart et al., 2005) an intense and prolonged footshock was followed by three weekly reminders of the event using stimuli present during the event (excluding the UC, i.e., electric shock). The rats demonstrated several long-term alterations: increased anxiety behavior, reduced time spent in an ‘aversive-like’ context, altered social behavior, and a blunted corticosterone response to stress.

Similarly, recent studies with cows have shown that a simulated wolf encounter in wolf-experienced, but not in wolf-naïve, cows elicited behavioral and physiological changes (Cooke et al., 2013) as well as selected brain–blood biomarkers (brain-derived neurotrophic factor and c-Fos proto-oncogene mRNA regulation) (Cooke et al., 2017) comparable with changes documented in humans and rodent models with stress- and fear-related psychological disorders, including PTSD symptoms (Sherin and Nemeroff, 2011). These findings suggest that exposure to wolves in cows leads to the formulation of fear memories that may be elicited at a later time upon re-encountering the earlier fear-inducing stimulus.

As mentioned above, approximately 15% to 35% of humans exposed to a severe stressor will develop PTSD. Similar information about the course of psychological trauma in animals living natural lives (i.e., outside the laboratory setting) is lacking. However, in a series of laboratory studies Cohen et al. (2006) investigated the prevalence rates of rats displaying an extreme magnitude of behavioral response to a predator stress paradigm. They reported that after exposure to the stressor almost all animals responded ‘extremely’, but over the next 30 days the incidence of individuals showing extreme behavioral responses dropped to an unvarying 25%, closely conforming to the human data.

Overall, in terms of posttraumatic physiological and behavioral alterations, experimental studies in clinical populations of many human survivors with PTSD are consistent with animal studies (Anda et al., 2006). However, there is, to date, no single accepted animal model of PTSD; each model has its pros and cons (Whitaker et al., 2014; Richter-Levin et al., 2018). The validity and limitations of existing animal models of PTSD have been recently reviewed (Schöner et al., 2017; Deslauriers et al., 2018; Cabib et al., 2019). Importantly, while animal models have produced neuroendocrine alterations and phenomenology that closely resembles specific aspects of PTSD, none has replicated the human condition in its entirety (Whitaker et al., 2014). This is not surprising, since, as mentioned earlier, many subjective features of PTSD cannot be confirmed with certainty in animals.

Animal – Clinical. The study of posttraumatic psychopathology in animals has been almost exclusively in the laboratory setting. However, there have been a small number of cases of PTSD in a clinical context reported in peer-reviewed and non-reviewed publications.

Peer-reviewed reports

Without using the term posttraumatic stress, Loeffler et al. (2009) reported on impaired psychological health following prolonged severe stress in bears. The practice of farming bears for bile extraction is legal in China, where bear bile is used in traditional Chinese medicine (despite the fact that it is unnecessary, as more than 50 alternative herbal products with equal or greater medicinal efficacy exist [Liu, 2004]). The Asiatic black bear (Ursus thibetanus) comprises most of the estimated 10,000 to 12,000 bears used in these farming operations; some are born in captivity and some are captured from the wild as adults. The bears are confined for their entire lives to very small cages that are only marginally bigger than the bears themselves during which they encounter the following stressors: extreme spatial restrictions, severe restriction of species-typical behavior, adverse substrate for sleeping and standing, deprivation of social needs, loss of the sense of control, extreme understimulation, and unpleasant interactions with humans (the bile extraction procedure is painful) (see Fig. 14.2a–d).

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