Stressor controllability modulates the stress response in fish

Marco Cerqueira,Sandie Millot,Simon Mackenzie,Catarina C V Oliveira,Rui F Oliveira,Maria Filipa Castanheira,Tomé Silva,Sonia Rey,Gonçalo A Oliveira,Ana S Félix

doi:10.1186/s12868-021-00653-0

Abstract

BackgroundIn humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax).ResultsFish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used.ConclusionsThese results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).

Highlights

In humans the stress response is known to be modulated to a great extent by psychological factors, by the predictability and the perceived control that the subject has of the stressor
The hypothalamic– pituitary–adrenal (HPA) axis response to stress has been shown to be influenced by controllability in humans, where in response to laboratory tasks, cortisol levels are lower in groups where stressor control is perceived than in groups where stressor control is not perceived [14] and perceived control is negatively correlated with cortisol [16, 17]
In rodents the HPA stress response seems insensitive to stressor controllability, but repeated exposure to controllable stressors leads to a lower response [18,19,20]

Summary

Introduction

In humans the stress response is known to be modulated to a great extent by psychological factors, by the predictability and the perceived control that the subject has of the stressor This psychological dimension of the stress response has been demonstrated in animals phylogenetically closer to humans (i.e. mammals). Given the central role of the mPFC on stressor controllability, it could be questioned whether this psychological moderation of the stress response is present in non-mammals that lack a cerebral cortex In this respect, querying its occurrence in fish, which represent a phylogenetically divergent vertebrate lineage from that of mammals [21], whose brains lack a mPFC homologue [22], is of major relevance. This has recently been shown by the involvement of the mesopallium and nidopallium in the complex cognitive abilities of birds [23,24,25]

Results

Discussion

Conclusion