Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Nov;28(11):4719-4728.
doi: 10.1038/s41380-023-02240-7. Epub 2023 Sep 6.

Sounds of danger and post-traumatic stress responses in wild rodents: ecological validity of a translational model of post-traumatic stress disorder

Hagit Cohen  1   2 , Michael A Matar  3 , Doron Todder  3 , Carmit Cohen  3 , Joseph Zohar  4 , Hadas Hawlena  5 , Zvika Abramsky  6
Affiliations

Sounds of danger and post-traumatic stress responses in wild rodents: ecological validity of a translational model of post-traumatic stress disorder

Hagit Cohen et al. Mol Psychiatry. 2023 Nov.

Abstract

In the wild, animals face a highly variable world full of predators. Most predator attacks are unsuccessful, and the prey survives. According to the conventional perspective, the fear responses elicited by predators are acute and transient in nature. However, the long-term, non-lethal effects of predator exposure on prey behavioral stress sequelae, such as anxiety and post-traumatic symptoms, remain poorly understood. Most experiments on animal models of anxiety-related behavior or post-traumatic stress disorder have been carried out using commercial strains of rats and mice. A fundamental question is whether laboratory rodents appropriately express the behavioral responses of wild species in their natural environment; in other words, whether behavioral responses to stress observed in the laboratory can be generalized to natural behavior. To further elucidate the relative contributions of the natural selection pressures influences, this study investigated the bio-behavioral and morphological effects of auditory predator cues (owl territorial calls) in males and females of three wild rodent species in a laboratory set-up: Acomys cahirinus; Gerbillus henleyi; and Gerbillus gerbillus. Our results indicate that owl territorial calls elicited not only "fight or flight" behavioral responses but caused PTSD-like behavioral responses in wild rodents that have never encountered owls in nature and could cause, in some individuals, enduring physiological and morphological responses that parallel those seen in laboratory rodents or traumatized people. In all rodent species, the PTSD phenotype was characterized by a blunting of fecal cortisol metabolite response early after exposure and by a lower hypothalamic orexin-A level and lower total dendritic length and number in the dentate gyrus granule cells eight days after predator exposure. Phenotypically, this refers to a significant functional impairment that could affect reproduction and survival and thus fitness and population dynamics.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. The long-term effects of predator cue exposure on behavior.
The top panel (1) depicts the experimental protocol. The red circle signifies the behavioral test performed, for which the results are shown. A Anxiety Index which integrates the measured EPM behavioral measures. B Startle amplitude in the acoustic startle response (ASR) paradigm. C Percentage of startle habituation in the ASR paradigm. D Prevalence of extreme behavioral response (EBR) (in percentages), E Prevalence of minimal behavioral response (MBR) (in percentages), F Prevalence of partial behavioral response (PBR) (in percentages). Owl territory calls had long-lasting influences on rodent behavior; all species reacted significantly to predator cue stress in terms of anxiety-related behavior in the EPM and ASR paradigms 7 days after exposure. In addition, predator cue exposure causes post-traumatic stress disorder (PTSD)-like behavioral responses in wild rodents that have never encountered owls. Data are presented as data points and mean ± SEM and percentage.
Fig. 2
Fig. 2. The effects of predator cue exposure on fecal cortisol metabolite (FCM) levels.
The top panel (1) depicts the experimental protocol. The red circle signifies the behavioral test performed, for which the results are shown. A The FCM levels, collected 1–2 h after predator stress exposure, in female and male Acomys cahirinus. B The FCM levels in Acomys cahirinus according to the affected groups (classified using the cut-off behavioral criteria (CBC) method). C The FCM levels, collected 1–2 h after predator stress exposure, in female and male Gerbillus henleyi. D The FCM levels in Gerbillus henleyi according to the affected groups (classified using the CBC method). E The FCM levels, collected 1–2 h after predator stress exposure, in female and male Gerbillus gerbillus. F The FCM levels in Gerbillus gerbillus according to the affected groups (classified using the CBC method). Although we tested basal FCM concentrations in G. gerbillus before predator exposure and found that the FCM concentrations were relatively low and significantly elevated in response to the stressor compared to their baseline levels, it is still unclear whether the poor FCM response to predator stress and the dysregulation observed in the acute aftermath of trauma represent an existing pre-trauma vulnerability trait or develops from the exposure to the trauma itself. Data are presented as data points and mean ± SEM.
Fig. 3
Fig. 3. The long-term effects of predator cue exposure on hypothalamic levels of orexin A.
(1) The top panel depicts the experimental protocol. The red circle signifies the test performed whose results are shown. A Hypothalamic levels of orexin-A (ORX-A) in females and males Acomys cahirinus species. B Hypothalamic levels of ORX-A in Acomys cahirinus species according to the affected groups (according to the cut-off behavioral criteria (CBC) method). C Hypothalamic levels of ORX-A in females and males Gerbillus henleyi species. D Hypothalamic levels of ORX-A in Gerbillus henleyi species according to the affected groups (according to the CBC method). E Hypothalamic levels of ORX-A in females and males Gerbillus gerbillus species. F Hypothalamic levels of ORX-A in Gerbillus gerbillus species according to the affected groups (according to the CBC method). Data are presented as data points and mean ± SEM.
Fig. 4
Fig. 4. The long-term effects of predator cue exposure on morphology of dentate gyrus (DG) granular neurons.
(1) The top panel depicts the experimental protocol. The red circle signifies the test performed, for which the results are shown. A Quantitative analysis of total dendritic length (μm), and (C) total dendritic number of dentate gyrus granule cells from the suprapyramidal blade in female and male Acomys cahirinus, Gerbillus henleyi (E, G, respectively), and Gerbillus gerbillus (I, K, respectively). B Quantitative analysis of total dendritic length (μm), and (D) total dendritic number of dentate gyrus granule cells according to the affected groups in Acomys cahirinus, Gerbillus henleyi (F, H respectively), and Gerbillus gerbillus (J, L, respectively). Data are presented as data points and mean ± SEM.
Fig. 5
Fig. 5
Computer-generated plots of reconstructions of the dendritic trees from granule cells of female and male Acomys cahirinus, Gerbillus henleyi, and Gerbillus gerbillus.
See this image and copyright information in PMC

Similar articles

See all similar articles

References

    1. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders (5th Edition) - DSM-5. 5 ed ed. Washington, DC,: American Psychiatric Association (2013).
    1. Brown JS, Kotler BP, Bouskila A. Ecology of fear: Foraging games between predators and prey with pulsed resources. Annales Zoologici Fennici. 2001;38:71–87.
    1. Houston A, McNamara J, Hutchinson J. General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc Lond. 1993;341:375–97.
    1. Hugie DM. The waiting game: a “battle of waits” between predator and prey. Behav Ecol. 2003;14:807–17.
    1. Katz MW, Abramsky Z, Kotler BP, Rosenzweig ML, Alteshtein O, Vasserman G. Optimal foraging of little egrets and their prey in a foraging game in a patchy environment. Am Naturalist. 2013;181:381–95. - PubMed