Predator-induced fear causes PTSD-like changes in the brains and behaviour of wild animals

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.

Telencephalic regulation of the HPA axis in birds

“…More neurons express immediate early genes in TnA when pigeons are exposed to unpredictable foot shocks, than if those shocks are predicted by tones (or than tones alone) ( Brito et al, 2019 ); and when black-capped chickadees (Poecile atricapilllus) are exposed to the stress of predator cues, such as calls of a predator or high-urgency alarm calls. This activation lasts for at least 7 days after repeated exposure ( Zanette et al, 2019 ). The structures identified in these two studies are equivalent to those identified in ring doves and starlings by Cheng et al (1999) , which had similar connectivity to each other.…”

“…Indeed, exposure to stress also activates areas in the avian HF, as it does in the mammalian hippocampus. Exposure to stressful stimuli (predator calls and alarm calls) increase activation in the (caudal) HF of black-capped chickadees, both immediately, and over the next 7 days ( Zanette et al, 2019 ). No evidence was found for HF activation in crows exposed to different types of threatening stimuli, though ( Cross et al, 2013 ).…”

Rationale, Relevance, and Limits of Stress-Induced Psychopathology in Rodents as Models for Psychiatry Research: An Introductory Overview

“…However, psychological stress can also be related to wildlife survival, where predation represents one of the more dangerous sources of life-threatening paradigms [ 64 ]. Consistently, predator perception induces heightened vigilance and fear, triggering neuroendocrine and behavioral responses and prototypical psychological stress responses [ 65 ].…”

Can the mammalian dive response override posttraumatic stress disorder?

“…While PTSD itself is a disorder, the stress physiology involved in PTSD is considered to be an evolutionary mechanism that makes use of the fight or flight response and functions by reinforcing organismal fear, hypervigilance, and threat avoidance, after experiencing a real or perceived threat [8][9][10][11]. Pertinent to the scope of the hypothesis that will be proposed in this article, the stress response is partially characterized by hyperactivity of the hypothalamic-pituitary-adrenal (HPA) axis, amygdala, and sympathetic nervous system (SNS) [4,12].…”