Environmental Enrichment Facilitates Anxiety in Conflict-Based Tests but Inhibits Predator Threat-Induced Defensive Behaviour in Male Mice

<b><i>Introduction:</i></b> Environmental enrichment (EE) is a useful and sophisticated tool that improves rodents’ well-being by stimulating social behaviour and cognitive, motor, and sensory functions. Exposure to EE induces neuroplasticity in different brain areas, including the limbic system, which has been implicated in the control of anxiety and fear. However, the effects of EE on ethologically relevant naturalistic behaviours, such as those displayed by prey in the presence of predators, remain largely unexplored. <b><i>Material and Methods:</i></b> In the present study, we investigated anxiety- and panic attack-like behaviours in a predator (cat)-prey confrontation paradigm and compared them with those in classical assays, such as the elevated plus-maze (EPM), marble-burying, and open field tests (OFTs), using C57BL/6J male mice housed in enriched or standard environments for 6 weeks. <b><i>Results:</i></b> We observed that EE exposure caused enhancement of the levels of anxiety-like behaviours in the EPM and OFTs, increasing risk assessment (an anxiety-related response), and decreasing escape (a panic attack-like response) behaviours during exposure to the predator versus prey confrontation paradigm. <b><i>Conclusion:</i></b> Taken together, our findings suggest that enriched external environments can modify the processing of fear- and anxiety-related stimuli in dangerous situations, changing the decision-making defensive strategy.

The anterior cingulate cortex and its role in controlling contextual fear memory to predatory threats

Predator exposure is a life-threatening experience and elicits learned fear responses to the context in which the predator was encountered. The anterior cingulate area (ACA) occupies a pivotal position in a cortical network responsive to predatory threats, and it exerts a critical role in processing fear memory. The experiments were made in mice and revealed that the ACA is involved in both the acquisition and expression of contextual fear to predatory threat. Overall, the ACA can provide predictive relationships between the context and the predator threat and influences fear memory acquisition through projections to the basolateral amygdala and perirhinal region and the expression of contextual fear through projections to the dorsolateral periaqueductal gray. Our results expand previous studies based on classical fear conditioning and open interesting perspectives for understanding how the ACA is involved in processing contextual fear memory to ethologic threatening conditions that entrain specific medial hypothalamic fear circuits.

A hypothalamic-thalamostriatal circuit that controls approach-avoidance conflict in rats

Survival depends on a balance between seeking rewards and avoiding potential threats, but the neural circuits that regulate this motivational conflict remain largely unknown. Using an approach-food vs. avoid-predator threat conflict test in rats, we identified a subpopulation of neurons in the anterior portion of the paraventricular thalamic nucleus (aPVT) which express corticotrophin-releasing factor (CRF) and are preferentially recruited during conflict. Inactivation of aPVTCRF neurons during conflict biases animal’s response toward food, whereas activation of these cells recapitulates the food-seeking suppression observed during conflict. aPVTCRF neurons project densely to the nucleus accumbens (NAc), and activity in this pathway reduces food seeking and increases avoidance. In addition, we identified the ventromedial hypothalamus (VMH) as a critical input to aPVTCRF neurons, and demonstrated that VMH-aPVT neurons mediate defensive behaviors exclusively during conflict. Together, our findings describe a hypothalamic-thalamostriatal circuit that suppresses reward-seeking behavior under the competing demands of avoiding threats.

The anterior cingulate cortex and its role in controlling contextual fear memory to predatory threats

ABSTRACTPredator exposure is a life-threatening experience and elicits learned fear responses to the context in which the predator was encountered. The anterior cingulate area (ACA) occupies a pivotal position in a cortical network responsive to predatory threats, and it exerts a critical role in processing fear memory. Ours results revealed that the ACA is involved in both the acquisition and expression of contextual fear to predatory threat. Overall, the ACA can provide predictive relationships between the context and the predator threat and influences fear memory acquisition through projections to the basolateral amygdala and perirhinal region and the expression of contextual fear through projections to the dorsolateral periaqueductal gray. Our results expand previous studies based on classical fear conditioning and open interesting perspectives for understanding how the ACA is involved in processing contextual fear memory to ethologic threatening conditions that entrain specific medial hypothalamic fear circuits (i.e., predator- and conspecific-responsive circuits).

Impact of continuous predator threat on telomere dynamics in parent and nestling pied flycatchers

In addition to direct mortality, predators can have indirect effects on prey populations by affecting prey behaviour or physiology. For example, predator presence can increase stress hormone levels, which can have physiological costs. Stress exposure accelerates the shortening of telomeres (i.e. the protective caps of chromosomes) and shorter telomeres have been linked to increased mortality risk. However, the effect of perceived predation risk on telomeres is not known. We investigated the effects of continuous predator threat (nesting Eurasian pygmy owl Glaucidium passerinum) on telomere dynamics of both adult and partially cross-fostered nestling pied flycatchers (Ficedula hypoleuca) in the wild. Females nesting at owl-inhabited sites showed impaired telomere maintenance between incubation and chick rearing compared to controls, and both males and females ended up with shorter telomeres at owl-inhabited sites in the end of chick rearing. On the contrary, both original and cross-fostered chicks reared in owl sites had consistently longer telomeres during growth than chicks reared at control sites. Thus, predation risk may cause a long-term cost in terms of telomeres for parents but not for their offspring. Predators may therefore affect telomere dynamics of their preys, which could have implications for their ageing rate and consequently for population dynamics.

The association between evidence of a predator threat and responsiveness to alarm calls in Western Australian magpies (Cracticus tibicen dorsalis)

Alarm calls are a widespread form of antipredator defence and being alerted to the presence of predators by the alarm calls of conspecifics is considered one of the benefits of group living. However, while social information can allow an individual to gain additional information, it can also at times be inaccurate or irrelevant. Such variation in the accuracy of social information is predicted to select for receivers to discriminate between sources of social information. In this study, we used playback experiments to determine whether Western Australian magpies (Cracticus tibicen dorsalis) respond to the predator information associated with alarm calls. Magpies were exposed to the alarm calls of two group members that differed in the threat associated with the alarm call: one call was played in the presence of a predator model while the other was not—in order to establish differences in the predator information provided by each caller. We then played back the alarm calls of the same group members in the absence of the predator model to determine whether magpies responded differently to signallers in response to the previous association between the alarm call and a predator threat. We found that receivers showed significantly greater levels of responsiveness to signallers that previously gave alarm calls in the appropriate context. Thus, the accuracy of threat-based information influenced subsequent receiver response.

Predator recognition and anti-predatory behaviour in a recent aquatic invader, the killer shrimp (Dikerogammarus villosus)

The killer shrimp (Dikerogammarus villosus) is one of the most recent, but also most damaging, aquatic invasive species in Europe, but information on how the species responds to novel predation pressures in recently invaded areas is very limited. We employed an open test arena to examine predator recognition and anti-predatory behaviour in killer shrimp exposed to either blank water or water conditioned with fish kairomones to simulate a predator threat. Within five years after their introduction, killer shrimp spent much more time hiding in the presence of fish kairomones than when they were exposed to blank water. However, no significant difference was found in aggregation behaviour, and killer shrimp were strongly attracted to the scent of conspecifics regardless of predator threat. Given the strong selective pressures that fish predators can exert on native and invasive gammarids, our findings highlight the need to consider prey-predator interactions to better predict the dispersal and likely impact of killer shrimp into invaded ecosystems.