The oldest and strongest emotion of mankind is fear, and the oldest and strongest kind of fear is fear of the unknown. – H.P. Lovecraft
Exposure to danger can cause severe psychological problems like post-traumatic stress disorder (PTSD). Not everyone exposed to risk acquires PTSD, but it commonly occurs after experiencing military combat or assault. It is estimated to affect around 5% of people in North America at any given time. Symptoms include social withdrawal, intense nervousness and hypervigilance, and fear of the unexpected.
From an evolutionary perspective, these symptoms can be highly beneficial when real danger exists. The symptoms have costs, of course, but they can save your life. Hypervigilance keeps you prepared for an attack, and withdrawal can keep you away from one. In fact, some experts no longer consider PTSD as a disorder because of its adaptive nature. The symptoms can become a debilitating problem, however, upon a sudden return to a safe environment where the costs of the symptoms accumulate without any benefit.
Minnow predation by pike. Credit: Adam Crane
Ecologists have shown that animals, including humans, generally show fear in similar ways, especially in the context of attacks from predators. While neuroanatomy varies substantially across animal taxa, the underlying neural pathways and behaviors associated with “fear” are quite similar. Hence, our understanding of the acquisition and treatment of PTSD has benefited greatly from animal models, as performing controlled and randomized experiments on humans are often not ethically viable.
For decades, prey fishes have been a classic model for understanding fear reactions. Many fishes have a chemical alarm substance in their skin, originally described as “Schreckstoff” (meaning “fright stuff” in German), that is only released when their skin is damaged by a predator. Therefore, this substance reliably indicates predation risk, and it elicits antipredator behaviors such as increased shelter use and decreased foraging. Repeated exposure to this alarm substance can induce a fearful state that includes chronic freezing and hypervigilant pacing, even in the absence of any threat. Fish in this fearful state also become neophobic, a characteristic where they show fear toward novel stimuli that would normally be perceived as nonthreatening.
Many fish species are highly social and learn from one another. Social learning of predation risk has been a focus of our work where a naïve “observer” individual learns about a specific predator from an experienced “model.” However, prior exposure to extreme risk can disrupt this transfer of information. After an observer has been exposed to risk repeatedly, it has difficulty learning from its social model about the safety of a stimulus. Instead, the social model indirectly acquires the fearful state from the observer. This socially-transmitted state of fear appears to parallel what is often referred to as “secondary trauma” among humans (figure 1). In secondary trauma, a person can acquire trauma symptoms simply by interacting with a victim of direct trauma. Such can occur among family members of PTSD sufferers and the health professionals that treat them.
Figure 1. Transfer of information about fear and safety. Credit: Adam Crane
We recently conducted experiments with fish on what is known as “social buffering,” where the presence of others alleviates stress for social animals. Specifically, we used calm models to weaken the neophobia of observers that had been exposed to repeated risk from a predator attack. The goal of this research was to better understand social learning of safety in fish, while also seeking to apply experimental outcomes to dimensions of PTSD.
First, we exposed observer fish to repeated risk either in isolation or in a group of fish. After an observer had experienced risk in a group, a group of five calm models was persuasive enough to facilitate a modest reduction of the fearful state of the observer. In comparison, interacting with only one calm model had no influence, with the model instead acquiring the socially-transmitted state of fear.
When observers had been exposed to risk in isolation, they showed higher levels of fear compared to those exposed to risk in a group. Surprisingly, however, even the presence of a single calm model substantially weakened fear in these observers. Thus, when the fearful state was acquired in a group, it was more difficult to override, apparently because it had been socially reinforced. These outcomes parallel anecdotal observations of humans that have acquired PTSD from group combat compared to victims of isolated trauma. Generally, PTSD from isolated trauma is more severe than that from group trauma, but behavioral therapy for victims of group trauma appears less effective.
In a second experiment, we periodically removed a model after it had experienced socially-transmitted fear, and then we replaced it with a new calm model. We did this replacement three times. The technique significantly weakened fear in observers, while also reducing socially-transmitted fear in models. We speculated that this outcome could parallel how the periodic replacement of therapists with secondary trauma might reduce the trauma symptoms of both themselves and their patients.
The idea that some fishes can be considered valid for exploring dimensions of PTSD has been met with a mix of support and criticism from other scientists. Fishes do meet some of the criteria required to be considered valid for modeling dimensions of PTSD, but other criteria still need to be tested. We argue that prey fishes may be a good model organism for several reasons, one of which being their abundance. We can conduct complex and controlled experiments where we manipulate several factors and still have large enough sample sizes for sufficient statistical power.
The best way to understand PTSD may be to combine what we learn from multiple animal models. Studies on fishes could potentially either fortify or challenge our current views on PTSD and possibly stimulate new ideas for recovery strategies.
These findings are described in the articles entitled Learning of safety in social fish: applications for studying post-traumatic stress in humans, recently published in the journal Animal Behaviour. This work was conducted by Adam Crane from Concordia University and Maud Ferrari from the University of Saskatchewan. These findings are also described in the article entitled The socially mediated recovery of fearful fish paired with periodically replaced calm models, recently published in the journal Proceedings of the Royal Society: Biological Sciences. This work was conducted by Adam Crane from Concordia University, and , Maud Ferrari from the University of Saskatchewan.