Learning and CRF-Induced Indecision during Escape and Submission in Rainbow Trout during Socially Aggressive Interactions in the Stress-Alternatives Model

Abstract

Socially stressful environments induce a phenotypic dichotomy of coping measures for populations in response to a dominant aggressor and given a route of egress. This submission- (Stay) or escape-oriented (Escape) dichotomy represents individual decision-making under the stressful influence of hostile social environments. We utilized the Stress-Alternatives Model (SAM) to explore behavioral factors which might predict behavioral phenotype in rainbow trout. The SAM is a compartmentalized tank, with smaller and larger trout separated by an opaque divider until social interaction, and another divider occluding a safety zone, accessible by way of an escape route only large enough for the smaller fish. We hypothesized that distinctive behavioral responses during the first social interaction would indicate a predisposition for one of the behavioral phenotypes in the subsequent interactions. Surprisingly, increased amount or intensity of aggression received had no significant effect on promoting escape in test fish. In fact, during the first day of interaction, fish that turned toward their larger opponent during attack eventually learned to escape. Escaping fish also learn to monitor the patrolling behavior of aggressors, and eventually escape primarily when they are not being observed. Escape per se, was also predicted in trout exhibiting increased movements directed toward the escape route. By contrast, fish that consistently remained in the tank with the aggressor (Stay) showed significantly higher frequency of swimming in subordinate positions, at the top or the bottom of the water column, as well as sitting at the bottom. In addition, a corticotropin-releasing factor (CRF)-induced behavior, snap-shake, was also displayed in untreated fish during aggressive social interaction, and blocked by a CRF1 receptor antagonist. Especially prevalent among the Stay phenotype, snap-shake indicates indecision regarding escape-related behaviors. Snap-shake was also exhibited by fish of the Escape phenotype, showing a positive correlation with latency to escape. These results demonstrate adaptive responses to stress that reflect evolutionarily conserved stress neurocircuitry which may translate to psychological disorders and decision-making across vertebrate taxa.

Coping styles in European sea bass: The link between boldness, stress response and neurogenesis

“…The transcription in the whole brain of gr2, mr and crf, which involved in the regulation of the HPI axis, was higher in shy than bold fish, whereas gr1 transcription did not differ between the two groups. Elevated gr2, mr or crf transcription in shy fish has also been reported in other fish species and contexts [80,[89][90][91]. For example, HR rainbow trout (considered as shy) displayed higher levels of crf than LR (considered as bold) in the forebrain of rainbow trout following confinement stress [80].…”

Orexin 2 receptor stimulation enhances resilience, while orexin 2 inhibition promotes susceptibility, to social stress, anxiety and depression

“…We defined the amount of time spent attentive to the hole as only including time when the test mouse was actively interested in and investigating the escape hole and tunnel directly (sniffing and placing head in the hole). This measure is a novel indicator of anxious behavior and decision-making unique to this model, which has been effectively used in SAM experiments on rainbow trout (Summers et al, 2017). We consider Escape and Stay behavioral outcomes to be the result of decision-making because early responses are variable, become stable with experience, and are modifiable by learning as well as anxiogenic or anxiolytic drugs (Carpenter and Summers, 2009; Smith et al, 2014; Smith et al, 2016; Summers et al, 2017; Yaeger et al, 2018).…”

“…It is important to note that both phenotypes readily discover and examine the escape routes, then learn how to escape, but only some (50% is average) choose to use this option (Carpenter and Summers, 2009; Robertson et al, 2015; Smith et al, 2014). Escaping during aggressive interactions behaviorally ameliorates the stress involved, and reverses rising stress hormone and gene expression levels (Carpenter and Summers, 2009; Robertson et al, 2017; Robertson et al, 2015; Smith et al, 2014; Smith et al, 2016; Summers et al, 2017). Animals that choose to remain with the larger aggressor (Stay) exhibit much higher elevated plasma corticosterone, behavioral Pavlovian fear conditioning, elevated anxiolytic neuropeptide S (NPS) gene expression in the central amygdala (CeA), and enhanced gene expression of cannabinoid 2 (Cb 2 ) receptors in the hippocampus (Robertson et al, 2017; Smith et al, 2014; Smith et al, 2016).…”

“…As such, the latency to escape is dramatically reduced, which is another reliable measure of diminished anxious behavior in the SAM (Robertson et al, 2015; Smith et al, 2014). Other anxiolytic factors, such as wheel-running exercise and icv NPS, reduce the initial latency to escape (Carpenter and Summers, 2009; Robertson et al, 2015; Smith et al, 2014; Smith et al, 2016; Summers et al, 2017; Yaeger et al, 2018). Alternatively, remaining submissively (Stay) leads to social defeat, which is the most stressful condition (Koolhaas et al, 1997) in our model.…”

Socio-Ecological Disruptions at Critical Periods During Development Alter Stress Responses and Hippocampal Dendritic Morphology of Prairie Voles: Implications for Social Monogamy

“…In real life, when individuals are challenged with physical threats or face uncertainty, neither humans nor other animals weigh all alternatives to choose the best strategy and their cognitive abilities can be affected by their stress responses (Giora, 1987;Lima, 1998;Porcelli and Delgado, 2017;Summers et al, 2017). Although several studies have examined the role of stress in monogamy, most have focused on how stress influences or is impacted by partner preference and paternal care (DeVries et al, 1996;Bosch et al, 2009;Hostetler and Ryabinin, 2013;Hyer and Glasper, 2017;Kowalczyk et al, 2018).…”