Post-traumatic stress disorder: evolutionary

perspectives

Chris Cantor

Fear is the key emotion of post-traumatic stress disorder (PTSD). Fear’s evolved function is
motivating survival via defensive behaviours. Defensive behaviours have been highly
conserved throughout mammalian species; hence much may be learned from ethology.
Predation pressure drove the early evolution of defences, laying foundations in the more
ancient brain structures. Conspecific (same species) pressure has been a more recent
evolutionary influence, but along with environmental threats it has dominated PTSD research.
Anti-predator responses involve both avoiding a predator’s sensory field and avoiding
detection if within it, as well as escape behaviours. More effective avoidance results in less
need for escape behaviours, suggesting that avoidance is biologically distinct from flight.
Recognizing the predation, environmental and conspecific origins of defence may result in
clearer definition of PTSD phenomena. Defence can also be viewed in the stages of no
threat, potential threat, encounter and circa strike. Specific defences are used sequentially
and according to contexts, loosely in the order: avoidance, attentive immobility, withdrawal,
aggressive defence, appeasement and tonic immobility. The DSM-IV criteria and PTSD
research show substantial congruence with the model proposed: that PTSD is a disorder of
heightened defence involving six key defences used in conjunction with vigilance and risk
assessment according to contexts. Human research is reviewed in this respect with reference
to laboratory and wild animal observations providing new insights. Understanding individual
perceptual issues (e.g. predictability and controllability) relevant to these phenomena,
combined with defence strategy recalibration and neuronal plasticity research goes some
way to explaining why some traumatized individuals develop PTSD when others do not.
Key words: defence, evolution, post-traumatic stress disorder.

Australian and New Zealand Journal of Psychiatry 2009; 43:1038–1048

Science is facts: just as houses are made of stones, Survival perspectives

so is science made of facts; but a pile of stones is
not a house and a collection of facts is not neces- Disordered emotions have been a key focus of psy-
sarily science. chiatry. Evolutionary psychology views emotions as
Henri Poincaré, 1842–1912. response patterns shaped by natural selection to offer selec-
tive advantages in certain situations [1]. Emotions moti-
vate survival behaviours. Fanselow and Lester described
‘..the organism as confronted with a series of environ-
mental problems that must be solved to insure future
reproduction’ [2].
Many features of anxiety disorder subtypes cor-
Chris Cantor, Adjunct Senior Lecturer respond to dangers encountered recurrently by our
Department of Psychiatry, University of Queensland, PO Box 1216, distant ancestors [1,3,4]. Anxiety is a response to
Noosa Heads, Qld 4567, Australia. Email: [email protected] potential threats, while fear relates to direct threats.
Received 17 February 2009; accepted 11 May 2009. Anxiety involves less organized behaviour than fear.

© 2009 The Royal Australian and New Zealand College of Psychiatrists

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 C. CANTOR 1039

Phobias, despite being listed in DSM-IV as anxiety decision-making has been demonstrated in both verte-
disorders, relate to direct threats [5,6]. The neural cir- brates and invertebrates [14]. Even simple prey such as
cuits of anxiety and fear are distinct. Fear involves insects make defensive decisions and respond accord-
primitive structures in the hind-brain, for example the ingly. In the journey from early unicellular organisms of
periaqueductal grey. Anxiety, unlike fear, activates the 3000 million years ago to modern Homo a few hundred
hypothalamo-pituitary–adrenal axis [7]. Fear is the key thousand years ago milestones included the arrival of
emotion in post-traumatic stress disorder (PTSD) and early reptiles and mammals 300 and 200 million years
its function is motivating defence. Therefore, might ago, respectively. Primary motivational neural circuits
PTSD be a disorder of defence? in the brain developed early in evolutionary history, in
That PTSD is noxious and disabling does not automa- primitive cortical, subcortical and midbrain structures
tically negate a potentially adaptive function. People born mediating largely unconditioned essential survival
without capacity for pain die early. Diarrhoea and vom- behaviours [5]. These primitive structures include
iting are unpleasant but their aversiveness drives future the amygdala and its projections. For a review of
avoidance. The clinician’s illusion is that symptoms are the relevant neuroanatomy and neurophysiology see
the problem [8]. Importantly for understanding evolution Davis [15].
and PTSD, what is adaptive in one environment may not Neurologist Paul MacLean developed the ‘triune
be so in another. brain’ concept, which suggests that both anatomically
The more essential a characteristic is for survival the and functionally the human brain reflects three ances-
more it will be conserved over evolutionary time. The tral eras of development: the reptilian; palaeo-(old)
basic skeletal design of a vertebral column, ribs and four mammalian; and the neo-(new) mammalian eras, with
limbs has persisted over many millions of years in virtu- the latter emerging 65 million years ago following the
ally all higher animals. Significant qualitative changes in mass extinction of large reptiles and dinosaurs [16]. The
design would tend to be fatal, although there has been corresponding brain regions and functions essentially
scope for adjustments. Fundamental survival behaviours are reptilian behaviours, palaeo-mammalian emotions
include breathing, eating and sexual reproduction, with and neo-mammalian reasoning. The triune regions may
remarkable similarities throughout the animal world. operate in isolation or concurrently.
Defence is another fundamental of survival; hence it too Defence can be viewed as having three foundations:
is highly conserved [3], although the defence repertoire threats posed by predators; conspecifics (same species);
of higher primates is more complex [9]. and the environment. Predation laid the essential foun-
This paper explores ethological research for insights dations and has also been a major driver of general
into defence and PTSD. The framework of an evolution- organismic complexity [17]. Predators may influence
ary theory of PTSD integrating existing behavioural, prey populations by stimulating costly defensive strate-
information processing and neuroscientific theories is gies, with intimidation affecting prey numbers at least as
presented. Not only is evolutionary theory unfamiliar to much as prey consumption [18]. Conspecific pressure is
some researchers and clinicians, but the topic of evolu- relevant to more recent defence evolution.
tion and PTSD is also very recent. Marks’ landmark 1987 Most PTSD literature is based on conspecific research,
work on evolution and anxiety disorders paid only mod- particularly of war veterans, and the results may not be
est attention to PTSD, which was then in its infancy [10]. representative of other PTSD populations. Might predator-
Subsequent PTSD-specific work has included Silove induced PTSD differ from conspecific-induced PTSD?
(1998) [11], Cantor (2005) [3], Bracha et al. (2005) [12] This could be studied using large cat or shark attack file
and Cantor and Price (2007) [13]. The basic principles data sources. Might shark attack victims display less
of the evolution of defences will be considered before generalized avoidance, particularly less fear of conspe-
examining their relevance to the psychopathology of cifics, but a more specific sea phobia? Although PTSD
PTSD and briefly presenting insights arising from a studies to date have not addressed the predator question,
defence perspective. Potential explanations for the enduring rates of conspecific-induced PTSD (assaults) tend to
nature of PTSD will be suggested. be higher than environmental PTSD [19]. Although it
has been suggested that this may relate to disillusion-
ment with humanity and loss of trust, the subcortical
Predation and the evolution of defences brain structures involved in PTSD suggest alternative
explanations.
All current life on earth originated from unicellu- Successful predation requires five components: detec-
lar organisms that, despite the absence of nervous sys- tion, identification, approach, subjugation, and consumption
tems, could learn defensive strategies [10]. Adaptive [20]. Prey anti-predator responses mirror these. Reptiles

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1040 POST-TRAUMATIC STRESS AND EVOLUTION

use more diverse, less energy-demanding responses than hierarchy [2,3,26,27]. Prey defensive decision-making
mammals, which have greater energy capacity [21]. Mam- is determined by the distance from predator, the preda-
malian defences are less diverse but are more widely distributed tor’s behaviour and cost–benefit calculations regarding
throughout mammalian species [22]. Nevertheless, because access to food or mates [28]. The combination of physi-
reptiles preceded the advent of early mammals by 100 mil- cal and psychological distance variables is referred to as
lion years the foundations of some mammalian defences have ‘predatory imminence’ [2].
reptilian origins, with more automatic and rapid, as opposed Stage 1 of the distance-dependent hierarchy involves
to consciously calculated responses [16,23]. prey engaging in its preferred activity in the absence of
Anti-predator traits span behaviour, morphology, physi- predation (or other threat). Stage 2 is a pre-encounter
ology, chemistry and life history [24]. There are two main scenario involving potential threat. Stage 3, after encoun-
behavioural strategies: predator avoidance and predator ter, involves predator detection. Stage 4 is circa-strike
escape from being consumed. Avoidance involves avoid- defensive behaviour [2,26,29]. A fifth stage, recuperation
ing a predator’s sensory field, the latter evading detection from wounds by lying low until the period of threat has
within a predator’s sensory field and escape. Avoidance passed, has been suggested [30].
and escape are separate functional entities. Avoiding a The hierarchical approach positions avoidance in the
predator’s sensory field involves some prey spending much first and second stages – preferred activity and poten-
of their lives in refuges and/or reduced activity, such as tial predation threat – whereas flight belongs in stage
emerging at particular times of the day. 3: after encounter. An important implication is that the
Avoiding detection within a predator’s sensory more successfully an early strategy is used, the less
field may entail morphological or behavioural crypsis the need to rely on later strategies. Nowhere is this more
(concealment) [24]. Prey can recognize predators and apparent than in the tortoise whose unusual withdrawal of
change their behaviours accordingly. Rodents may for- body parts into its carapace has eliminated the need for
age around shrubs when under threat from owls, but energy-demanding flight or fight. Avoidance and flight
switch to the open when under threat from snakes [25]. have been driven by distinct selection pressures and their
Following predator detection more active defences biology will reflect this. Understanding this is impor-
such as withdrawal or aggressive defence may be used tant for considering the confused DSM-IV avoidance-
for capture deterrence. Let us now examine the key behaviour criteria that reflect true avoidance, withdrawal
defences. and numbing phenomena.
Marks was clear that the two immobilities – attentive and
tonic – are different physiologically and functionally [10].
Defence hierarchy Brandao et al. claim to have identified the neural substrates
of at least four different types of immobility, but their work
Marks described four fundamental mammalian is difficult to incorporate with functional research [7]. It
defences: withdrawal, immobility, aggressive defence, and is sufficient to recognize that attentive immobility occurs
appeasement [10]. He described two types of immobility – early in the defence sequence, whereas tonic immobility
attentive and tonic – with little in common except immo- is the last defence prior to consumption.
bility. He noted that avoidance, withdrawal, flight and The post-encounter stage of flight or fight is associated
other escape behaviours comprised a broader avoidance with sympathetic activation [31]. Flight or other with-
strategy. For reasons that will later become clear I shall drawal will generally be preferred to aggressive defence
follow Langerhans’ separation of avoidance from with- because it carries less risk of injuries that may hamper
drawal [24]. Hence, the traditional oversimplistic ‘fight or foraging or predation, decreasing survival.
flight’ should be re-conceptualized as six key defences in a Appeasement is primarily a defence for conspecific
specific sequence: avoidance, attentive immobility, with- encounters with more dominant individuals. It involves
drawal, aggressive defence, appeasement, and tonic immo- pacification, conciliation and submission [3].
bility [3]. All six defences are routinely complemented The final circa-strike defence is tonic immobility. It
by vigilance and risk assessment. involves a sudden prolonged stillness with preservation
Studies of US, Brazilian and Welsh students have dem- of awareness. It is initiated by inescapable situations,
onstrated that people use similar defences to rats, the often with physical contact, particularly restraint [31].
most convenient laboratory research animal. Defence, It involves zero or near zero distance and immediate
however, is less conditioned and more innate in less predatory imminence.
encephalized mammals [6]. While I refer to the six key defences as avoidance, atten-
The notion of six key defences is usefully comple- tive immobility, withdrawal, aggressive defence, appease-
mented by the concept of a distance-dependent defence ment, and tonic immobility, all these defences involve

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 C. CANTOR 1041

the vital co-phenomena of vigilance and risk assess- C7, a sense of foreshortened future, appears depres-
ment. Whereas psychiatry has tended to equate hyper- sive. A shortcoming of the current approach to PTSD
vigilance with physiological overarousal, ethologists is the non-specificity of the word ‘trauma’ that includes
view hypervigilance more in terms of watchfulness. fear, loss and other noxious emotions. PTSD might be
Vigilance increases as risks are assessed as greater more useful if it was restricted to the emotion fear; loss
or ambiguous [32]. In primates much vigilance may is adequately catered for by depression.
relate to defence against conspecifics as opposed to The D overarousal symptoms [34] are sometimes
predators [33]. referred to as hypervigilance phenomena, and criterion
D4 is just that. D5 relates to startle reactions, which
involve rapid automatic withdrawal and aggressive
Post-traumatic stress disorder and DSM-IV defence responses from lower brain areas. They are con-
sidered reliable indicators of fear in fear research [5].
Let us now examine the relevance of these issues to Delays associated with emotions and reasoning may
the clinical phenomena of PTSD. The DSM-IV stres- prove fatal so primitive rapid reptilian functions are
sor criteria involve threat of death, physical injury highly represented in defensive behaviour.
or a threat to the bodily integrity of oneself or others Criterion D1, sleep disturbance, is consistent with
[34]. Hence, defence is highly relevant to the stressor hypervigilance but would be more useful if described
criteria. specifically as a sleep disturbance associated with safety
All five re-experiencing criteria (intrusive recollec- concerns, differentiating it from depressive insomnia.
tions, nightmares, and the three criteria relating to height- D3, difficulty concentrating, is similarly problematic,
ened reactions to trauma memories) [34] reflect enhanced involving concentration on safety at the expense of other
memory for threats. Re-experiencing phenomena keeps issues. This leaves D2, anger/irritability, which clearly
defence in the foreground of concerns. Sullivan and relates to aggressive defence.
Gorman have suggested that PTSD is a disorder of fear Hence, the still evolving criteria due for revision
memory circuitry [35]. Silove described survival benefits for DSM-V include the theory’s memory component
from a rapid and enduring fear learning system with cor- for a heightened state of defence; the vigilance aspect
tical and subcortical pathways [11]. In mice memory of and, in a muddled way, avoidance, flight, numbing and
electric shocks in the immediate aftermath predicted re- aggressive defence phenomena. There is a remarkable
experiencing symptoms but not avoidance or overarousal degree of fit with the evolutionary theory. But what
symptoms [36]. about appeasement and the immobilities? The theory
The DSM-IV avoidance C criteria [34] sound more is jeopardized if these are not found in PTSD. Can-
encouraging for the theory than they actually are, but tor and Price have suggested that appeasement is the
there remains considerable congruence. Criterion C1, foundation of complex PTSD [13]. The paradoxical
avoiding thoughts, feelings or conversations associated attachments of abused children and spouses to their
with the trauma, is more consistent with psychological abusers and those of Stockholm syndrome victims are
flight than avoidance. Criterion C2, avoiding activities, understandable when viewed from the perspective of
places or people arousing recollections of threats is appeasement.
clearly consistent with defence. Strictly interpreted it is This leaves attentive and tonic immobilities. The next
unclear whether this criterion would include flight, but section briefly provides some insights from this defence
most patients fleeing from trauma reminders will also perspective, prioritizing tonic immobility because it is
avoid them. C3, psychogenic amnesia, also represents unfamiliar to many clinicians.
psychological avoidance/flight.
C4, diminished interest or participation in significant
activities, C5, feelings of detachment from others, and
C6, restricted range of affect, are somewhat problematic. Clinical insights from defences
Foa et al. suggested that these are numbing symptoms
that should be separated from avoidance behaviours [37]. Avoidance
Numbing involves the opioid system and relates to the
stage 3 post-predator encounter [2]. Numbing of injuries Avoidance of predators, conspecific and environmental
inflicted by predators facilitates flight or fight, flight to a hazards involves avoidance of entering the relevant field:
refuge and avoidance of coming out. Hence, numbing is stage 2, a pre-encounter scenario [2]. Avoidance was the
more an adjunct to these defences than an independent dominant defence in the energy-limited reptilian era, flight
entity. and fight being energy demanding. Hence, avoidance

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1042 POST-TRAUMATIC STRESS AND EVOLUTION

should have significant neurodevelopmental represen- distance decreased, suggesting an increase in muscle ten-
tation in the human ‘reptilian’ brain. Sure enough, the sion with attentive immobility [22,40]. Attentive immo-
brainstem basal ganglia and extrapyramidal motor sys- bility is mediated by the lateral projections of the central
tems control a number of automatic behaviours [38]. grey that also mediates stress-induced analgesia [41].
The reptilian quality of avoidance in PTSD may result
in patients defaulting on exposure challenges for rea-
sons lying outside of awareness (although palaeo- and Withdrawal
neo-mammalian correlates may co-occur).
Asking potential PTSD patients how they cope with Reptiles have limited energy reserves for energy-
supermarkets and crowded shopping centres is useful. demanding defences such as flight and aggressive
They frequently avoid them. What are the contextual defence. When reptiles do use flight it requires augmen-
implications of this? Environmental dangers seem irrel- tation by withdrawal to refuges such as cracks in rocks
evant. Predation threat would be only symbolically rele- inaccessible to predators [21]. Aquatic insects, gastro-
vant; many noisy people may alert predators. Conspecific pods, crustaceans, fish, reptiles and mammals have all
fear of strangers appears more relevant. been observed to use refuging [42]. Refuging increases
Avoidance involves modification of behaviour accord- with rising predation risk [14] and is likely to similarly
ing to the perceived likelihood of a threat encounter: a increase with conspecific risks.
cost–benefit calculation. This has been explored experi- Although human refuging may have ancient reptilian
mentally using the size and frequency of rat meals. Fre- origins, it could also have arisen through evolutionary
quent small meals are preferred because they are digested convergence, which involves a shared solution to an evo-
more efficiently, but carry risks associated with time away lutionary challenge, without shared ancestral inheritance
from the burrow. As the perceived risks experimentally of the strategy. The hovering long-tongued humming bird
rose, rats switched to larger, less frequent, less digestible and humming bird hawk moth use the same solutions for
meals with the benefit of less exposure to predators [2]. reaching nectar in deep flowers without suitable perches.
The pregnant female of some species take more risks One is a bird, the other an insect. The slow flight of pri-
with predators compared with the stronger male [37] mates has been a recent development from our faster
because they have greater nutritional requirements, again mammalian ancestors, suggesting possible refuging by
illustrating cost–benefit calculations [14]. Well-nourished convergence. Fast-footed mammals that can outrun pred-
pregnant humans with PTSD are unlikely to display less ators utilize open spaces for defence. Refuging includes
avoidance in the absence of predators, but the hypothesis both flight to refuges and avoidance of emerging for
would be readily testable. extended periods, to ensure that dangers have passed.
Patients with PTSD often talk more about refuging
than about flight. They gain a greater understanding of
Attentive immobility their withdrawn, often near-housebound states when
they understand that this relates to not only avoidance
Attentive immobility is a transitional state of high in the DSM sense, but also in the defensive sense.
arousal and hypervigilance that follows detection of a Non-human primates seek refuges up trees; humans use
possible immediate threat [38], that is, stage 3 – after their homes.
encounter – and is a prelude to definitive defence deci- Refuging lends itself well to research because different
sion-making [14]. Attentive immobility keeps the head PTSD sample groups may present different activity
still for careful assessment of threat, provides crypsis schedules. Comparing environmental- versus conspecific-
and primes the individual for flight or aggressive defence induced PTSD with respect to proportion of time spent
[21]. Attentive immobility involves focused attention, within the home would be simple, but ethological hypoth-
cardiac deceleration, analgesia and potentiated startle eses are preferable to intuition.
[32]. Bradycardia is sufficiently reliable that along with Flight initiation distances from predators were found
measurements of body sway (an index of immobility) to increase with distance from burrows in woodchucks
it has been used in human investigations of attentive and took into account the positioning of the predator
immobility [39]. with respect to the woodchuck and the burrow [43]. This
Attentive immobility is particularly pronounced in rats, again illustrates cost–benefit calculations with respect to
making them useful research subjects, but it is a familiar interrupting foraging and the use of energy-demanding
human experience, unlike the unfamiliar tonic immobil- defences. Risk assessment is pharmacologically distinct
ity. Defensive aggressive behaviours, including startle, from flight: flight decreases selectively with anti-panic
in wild rats were found to rise abruptly as predator–prey drugs while risk assessment responds to anxiolytics [6].

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 C. CANTOR 1043

Aggressive defence animal world in insects, crustaceans, fish, amphibians,

reptiles, mammals and birds [27,31]. It arises in situations
Aggressive defence is subdivided into aggressive sig- of immediate ‘predatory imminence’ (and its conspecific
nalling and the more dangerous ‘fight’. Anger is an emo- or environmental counterparts). It is an involuntary state
tion with exceptionally effective signalling functions [44]. of profound motor inhibition despite fully preserved con-
Only if signalling fails is the more energy-demanding sciousness, activated by extreme fear, perceived inescap-
and hazardous fight response likely to be initiated [3,10]. able circumstances, usually involving an obviously more
Prey may alert predators that they have been detected powerful predator or conspecific [3,48]. In animals it
by attempts to frighten, confuse or intimidate them [24]. usually involves restraint. On termination of tonic immo-
Prey may use aggressive signalling as part of an escape bility sudden recovery and flight may occur but this is
response, combining fight with flight. Aggressors signal neither as precipitous nor as reliable as that following
aggression with conspecific encounters but not when attentive immobility [10]. Tonic immobility may persist
attacking prey as they strive to remain undetected. beyond release [27] and in chickens has been observed
to last up to 5¾ h [49].
Appeasement It may promote survival through inhibition of preda-
tor killing reflexes, confusion of predators, deterrence
Cantor and Price recently published in this Journal a through raising the possibility of diseased dead meat
detailed review of appeasement reactions, providing ani- and lowering of blood pressure, which reduces blood
mal and human observations suggesting that appease- loss from injuries [3,31]. With conspecifics its submis-
ment is the foundation of complex PTSD [13], and so I sive aspects may serve also as appeasement to deter more
only make brief mention of it here. Appeasement’s asso- serious assault.
ciation with conspecifics suggests a more recent triune During tonic immobility animals remain largely
brain heritage than defences evolving from predation. unresponsive to external stimuli. The immobility
De-escalation is one of appeasement’s core functions involves either muscular hypo- or hyper-tonicity, waxy
[45]. Defeated primates have been observed to retreat, flexibility, suppression of vocal behaviour, intermittent
only to return to the dominant conspecific and protest eye closure, Parkinsonian-like tremors with changes
until signals of acceptance are elicited, a phenomenon in heart rate, decreased temperature, increased respi-
known as ‘reverted escape’ [46]. It involves flight to ratory rate and electrocardiogram changes [27,49,50].
the source of the threat. The dominant may engage in Experimental pre-induction shocks stimulating fear
further coercion, with the subordinate responding with and/or adrenalin injections can greatly extend tonic
more appeasement, reinforcing their social bond with immobility, whereas increasing familiarity with the
due recognition of status. This is commonly observed threat decreases it.
with abused spouses and children [13]. From an evolu- Waxy flexibility in combat victims presenting with
tionary perspective subordinates often have to maintain tonic immobility may be misdiagnosed as psychotic cata-
group membership for survival, and dominants need to tonia [51]. There are many similarities and differences
maintain group cohesion. between tonic immobility and catatonia [52]. Tonic
A specific traumatic context, traumatic defeat plus immobility evolved as a fear response for present threats.
an inescapable relationship with a dominant oppres- With humans such responses may be activated by fear
sor, resulting in specific PTSD symptoms, suggests that but maintained by a cognitive focus on potential (i.e.
PTSD research may benefit from greater consideration of future) threats, with those threats remaining undetected,
contexts: predator, conspecific and environmental, com- resulting in a protracted state of immobility commonly
bined with other contextual characteristics. This might described as catatonic stupor. The linkage of catatonia
lead to greater understandability and predictability of with defence against ill-defined threats is further sup-
treatment responses. It contrasts with a general malfunc- ported by catatonic excitement being associated with
tioning disease-based approach. ‘PTSD’ may be better undirected assaultativeness.
viewed as the ‘PTSDs’ (plural). Some conversion reactions may reflect animal defence
behaviours [12,53]. Accounts of the immobility invol-
ved in World War I shell shock are often difficult to
Tonic immobility differentiate between catatonia, conversion or tonic
immobility. Some support for this arises from neurophysi-
Tonic immobility is the final defence in the chain of ological findings of hyperactive monitoring during motor-
anti-predator responses: nature has one last desperate initiating decisions in subjects with conversion paresis
measure [47]. It is widely represented throughout the of one arm [54].

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1044 POST-TRAUMATIC STRESS AND EVOLUTION

In contemporary humans tonic immobility is com- Enduring defensive reorientation

monly experienced with conspecific encounters in rape-
induced paralysis [27,30,55]. A total of 37% of 35 rape PTSD involves an enduring heightened defensive
victims were found to have experienced tonic immo- orientation. What causes this in some trauma victims but
bility [56]. It also has been found in victims of other not others?
sexual abuse and some non-sexual violence. Heidt et al.
found that 52% of women with histories of childhood Perception, controllability/predictability
sexual abuse reported tonic immobility in response to the and contexts
abuse [57]. Older perpetrators and greater age differen-
tials (suggesting perceived inescapability) between the The significance of traumatic events differs for differ-
abusers and children were both associated with greater ent individuals. The traditional model of PTSD linking
tonic immobility, which was associated with greater threat exposure to psychopathology neglects the appraisal
distress, peritraumatic dissociation, depression, anxiety process in humans that links an objective event to a sub-
and PTSD. Similarly, 41.7% of survivors of adult sexual jective response [61]. How a traumatic event is processed
assault reported significant immobility during their most [3,62,63] depends on complex interactions between an
recent assault, and 10.4% reported extreme immobility individual’s psychological makeup, the traumatic event
[58]. Rape victims may be insensitive to pain during and the context in which it occurs.
tonic immobility [27]. Conditioning research has tended to overlook the
Tonic immobility may be a key determinant of PTSD contexts in which aversive stimuli have been applied
outcome following sexual assault. Tonic immobility was [63]. Aversive stimulation in laboratories is associated
found to partially mediate the relationship between fear with longer lasting changes than in the wild, possibly
and both overall PTSD symptom severity and PTSD because wild animals have trade-offs to consider: the
avoidance/numbing [49]. Further, the relationship bet- costs and benefits of strategies in complex and danger-
ween perceived inescapability and PTSD symptom sever- ous environments [64]. Bearing in mind that PTSD in
ity and avoidance/numbing was fully mediated by tonic war veterans often becomes more overt following repa-
immobility. No relationship was found between tonic triation, might the cost of avoidance for combat veter-
immobility and hyperarousal symptoms, suggesting that, ans be too great until they have left the war zone? In
like appeasement, tonic immobility may generate specific laboratory animals environmental variables predispose
PTSD symptomatology and that tonic immobility-driven and increase responsivity, and lack of social interac-
PTSD may be less responsive to arousal-lowering treat- tions may increase the consequences of aversive expe-
ments. riences and inescapability [64]. This is akin to child
Non-sexual conspecific assaults have also involved abuse and neglect being risk factors for adult human
tonic immobility, with 43% of victims of urban violence PTSD.
reporting peritraumatic tonic immobility, which emerged Trauma processing will be influenced by gene-neural
as a marker for poorer responses to psychotropics [59]. variance, life histories, predictability, controllability, and
Tonic immobility, but not dissociation or panic, predicted other individual and contextual variables [3]. There is
PTSD symptom severity after controlling for potential strong evidence that controllability and predictability are
confounders in urban violence victims [60]. crucial psychological variables [65]. Studies of labora-
The preservation of awareness with an inability to tory animals and torture victims have shown that even
voluntarily respond implies dissociation [3]. Deperson- an illusion of control can be protective [66]. PTSD may
alization (detachment from self) but not derealization even occur with the deprivation of control in prisoners in
(detachment from environment) was found to be asso- the absence of actual physical torture [67].
ciated with tonic immobility, but the reverse occurred Overlapping with controllability/predictability issues
with fear [58]. This fits with depersonalization having is that of mental defeat, which is the perceived loss of
an internal focus on why one is not responding, whereas all autonomy, a state of giving up efforts to retain one’s
in derealization the focus is more external. Dissocia- identity with an independent will [19]. It represents the
tive identity disorder patients often become immobile, complete breakdown of resistance to the oppressor. Tor-
enter trance-like states and report out-of-body experi- ture victims may face uncontrollable external circum-
ences or dissociative amnesia [30]. While tonic immo- stances yet remain mentally undefeated: ‘I’m going to
bility is not associated with all types of dissociation, die — so be it.’ Mental defeat in East German political
might there be a subtype of dissociation specific to tonic prisoners was correlated with both the development and
immobility? severity of PTSD.

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 C. CANTOR 1045

Unconditioned behaviours and preparedness alarms are inexpensive compared with dire consequences
in the absence of alarms. An optimal defence system
Newborn infants do not learn to breath, they simply involves a lower cost of using a defence than the cost of
do it. Breathing is an unconditioned behaviour funda- not using it. Recalibration may occur according to the
mental to survival. Laboratory-bred rodents that have frequency and/or severity of threats, and control systems
never met predators respond on first exposure to preda- do not necessarily return to their previous levels.
tor cues with risk assessment behaviours, freezing and Enduring agonic switching would be expected to have
withdrawal [64]. some physiological representation. Langerhans observed
Other defensive behaviour may be rapidly learnt or the following [24].
activated by a process that Seligman called ‘prepared-
Many prey organisms have evolved adaptive
ness’ [68]. Laboratory-reared monkeys were initially
predator-induced phenotypic plasticity, where
unafraid of snakes, but rapidly became fearful follow-
particular phenotypes are only produced under the
ing viewing wild adult monkeys responding fearfully to
threat of predation, thus avoiding fitness costs in
snakes [69]. Their rapid fear learning was prepared by
the absence of particular predators. Others have
evolution.
fixed phenotypes. Plasticity will be favoured in
Short aversive stimulation increases defensive behav-
changeable environments, where environmental
iour in animals including risk assessment, freezing,
cues permit predicting cost-benefits.
escape, withdrawal, general activity and social behav-
iours. A single aversive event may result in lasting shifts Neural plasticity in afferent projections to and efferent
in response patterns. Inescapable shocks were found to projections from the amygdala seem to mediate lasting
increase defensive behaviour for up to 10 weeks [65]. consequences of aversive stimulation. Neurotransmitter
Exposure of rats to cats resulted in changes of up to at gastrin-releasing peptide (GRP) increases GABAergic
least 12 days in anxiety-like behaviour, potentiated star- inhibition in lateral amygdala during extinction of condi-
tle and amygdala hyperexcitability [70]. Animals may tioned fear. When GRP release is prevented, fear memory
associate both the aversive stimuli and the contextual persists [64]. In the generation of psychopathology over-
cues with threats, resulting in generalization as seen in activation of such circuits with resulting sensitization is
PTSD [63]. one possibility, memory modulation is another. PTSD
might result when the extinction of an aversive event’s
psychobehavioural response is impaired. Memory sup-
pressor genes and other molecular and cellular mecha-
Agonic switching and plasticity nisms might operate. Different experience-dependent
synaptic plasticity may be associated with outcome.
Defensive reorientation following threats may also
occur at a social systems level. Humans usually operate
under a ‘hedonic’ orientation. The hedonic mode involves Ethology
affiliative relationships with cooperation and facilitation
of exploratory behaviour [44]. The latter facilitates mate- Ethological studies of wild animals are important for
seeking and food-gathering but is the opposite of defence. exploring evolution and PTSD. The absence of PTSD in
At times of heightened threat a switch to the agonic mode animals would cast doubt on the theory proposed. Dem-
may be adaptive. This involves interactions based on com- onstrating its existence may clarify the core features of
petition with resolution based on dominant subordinate PTSD. Laboratory animal models generally involve ele-
polarities. Some social animals such as wolves are more ments of PTSD-like states without true PTSD. Etholo-
routinely orientated to the agonic mode. Populations of gists have barely considered PTSD in wild animals. There
individuals with genetic makeups allowing for flexibility has been a recent report, however, of possible PTSD in
in these regards will have survival advantages. While the elephants [71]. It is difficult from the description of the
agonic orientation of PTSD may be mostly unhelpful in disturbed behaviour – both fearful and aggressive – to
contemporary humans for whom the frequency of threats be sure that it represents PTSD, but it seems a possibil-
is usually low, if the environment were to become more ity. There also has been a convincing report of complex
threatening, constitutional flexibility for switching to a PTSD in chimpanzees rescued from years of traumatic
more defensive mode might be adaptive. entrapment in research laboratories [72]. Our relatedness
An optimal defence system will involve many false to elephants is relatively distant but we are close to chim-
alarms [8]. The smoke detector principle notes that false panzees. Elephants, like humans, however, are socially

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1046 POST-TRAUMATIC STRESS AND EVOLUTION

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