Abstract
Predator-induced fear is both, one of the most common stressors employed in animal model studies of post-traumatic stress disorder (PTSD), and a major focus of research in ecology. There has been a growing discourse between these disciplines but no direct empirical linkage. We endeavoured to provide this empirical linkage by conducting experiments drawing upon the strengths of both disciplines. Exposure to a natural cue of predator danger (predator vocalizations), had enduring effects of at least 7 days duration involving both, a heightened sensitivity to predator danger (indicative of an enduring memory of fear), and elevated neuronal activation in both the amygdala and hippocampus – in wild birds (black-capped chickadees, Poecile atricapillus), exposed to natural environmental and social experiences in the 7 days following predator exposure. Our results demonstrate enduring effects on the brain and behaviour, meeting the criteria to be considered an animal model of PTSD – in a wild animal, which are of a nature and degree which can be anticipated could affect fecundity and survival in free-living wildlife. We suggest our findings support both the proposition that PTSD is not unnatural, and that long-lasting effects of predator-induced fear, with likely effects on fecundity and survival, are the norm in nature.
Highlights
Biomedical scientists studying post-traumatic stress disorder (PTSD), and ecologists, have independently developed an interest in the impacts of predator-induced fear in the last two decades[1,2]
We experimentally tested for these enduring effects by employing a well-established predator-fear protocol used in animal model studies of PTSD (2 days experimental predator cue exposure followed by 7 days without30,31), and subsequently measuring both, a behavioural reaction to danger (‘freezing’, i.e., time spent ‘vigilant and immobile’15,16) commonly assessed in animal model studies of PTSD19, and a well-studied marker of long-term neuronal activation (∆FosB30–32)
On the “fear-circuit” involving the amygdala[19] and the hippocampus, are criteria which our results meet[1,12,19,20]. That these enduring effects on the amygdala and hippocampus were directly attributable to the fear induced by hearing predator cues 7 days previously, is clear from the immediate activation of these brain areas resulting from hearing these cues, as shown in our subsidiary experiment
Summary
Biomedical scientists studying post-traumatic stress disorder (PTSD), and ecologists, have independently developed an interest in the impacts of predator-induced fear in the last two decades[1,2]. In light of the many PTSD-like changes manifest in laboratory rodents in response to predator-induced fear[19], has prompted a growing number of biomedical researchers to propose[3,5,6,7,9,10,11] that “PTSD is the cost of inheriting an evolutionarily primitive mechanism that considers survival more important than the quality of one’s life”[12] In this view, PTSD-like changes in the brain and behaviour are not unnatural or “maladaptive”, but are rather evolutionary adaptations which entail costs, such as “hypervigilance”[12,19,20] and the avoidance of trauma-related cues[19], that provide the benefit of increasing the probability of survival, by increasing the likelihood of detecting a life-threatening danger (hypervigilance), and reducing the probability of encountering one (avoidance). Our results demonstrate that PTSD-like changes in the brain and behaviour can occur in wild animals; which we suggest supports both the proposition that PTSD is not unnatural[3,5,6,7,9,10,11,12], and that long-lasting effects of predator-induced fear, with likely effects on fecundity and survival, are the norm in nature[2,3,4,8,21,25,29]
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