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Foraging Latencies to Ceiling Looming Stimuli (A) Group average latencies GSEM to retrieve food pellet. (B) A number of rats who failed to retrieve the pellet on Expanding Disc trial (did not retrieve pellet within 180 s). (C) Representative position plots of a female rat that failed to retrieve a pellet on the first day of Expanding Disc exposure. (D) Position plot from the same rat demonstrating rapid habituation to Expanding Disc during the second day of expanding disc exposure.
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Rodents in the wild are under nearly constant threat of aerial predation and thus have evolved adaptive innate defensive behaviors, such as freezing or fleeing, in response to a perceived looming threat. Here we employed an ethologically relevant paradigm to study innate fear of aerial predators in male and female rats during a goal-oriented task....
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Context 1
... sweeping block stimulus elicited fewer fleeing responses in both sexes (4/8 females; 2/7 males), whereas almost none of the animals (1/7 females; 0/8 males) fled in response to the overhead, sweeping bar stimulus. Once again, none of the male and female rats displayed freezing in the arena when looming stimuli were presented and quickly habituated to the stimuli ( Figure 4B-4D). Hence, our sweeping stimuli results in rats contrast with a previous study conducted in mice that reported freezing responses to a similar stimulus (De Franceschi et al., 2016). ...
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Resumo: O presente artigo tem como objetivo apresentar um pouco da evolução da ciência que estuda o comportamento animal comparado-Etologia-, destacando a teoria de Lorenz (1937), considerado um dos fundadores dessa ciência. O texto inicia-se fazendo referência às diversas relações existentes entre os seres humanos e os demais animais, desde os pri...
Resumo: O presente artigo tem como objetivo apresentar um pouco da evolução da ciência que estuda o comportamento animal comparado-Etologia-, destacando a teoria de Lorenz (1937), considerado um dos fundadores dessa ciência. O texto inicia-se fazendo referência às diversas relações existentes entre os seres humanos e os demais animais, desde os pri...
Citations
... CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made Previous research in laboratory rats observed sex differences in foraging strategy involving male rats spending more time in open, novel environments compared to female rats [32,44,46,47]. We found no sex differences in mice across foraging success, foraging latency, time spent in the foraging zone, and nest exits. ...
Foraging is a universal behavior that has co-evolved with predation pressure. We investigated the role of bed nucleus of the stria terminalis (BNST) GABA neurons in robotic and live predator threat processing and their consequences in post-threat encounter foraging. Mice were trained to procure food in a laboratory-based foraging apparatus in which food pellets were placed at discrete and incrementally greater distances from a nest zone. After mice learned to forage, they were exposed to either a robotic or live predator threat, while BNST GABA neurons were chemogenetically inhibited. Post-robotic threat encounter, mice spent more time in the nest zone, but other foraging parameters were unchanged compared to pre-encounter behavior. Inhibition of BNST GABA neurons had no effect on foraging behavior post-robotic threat encounter. Following live predator exposure, control mice spent significantly more time in the nest zone, increased their latency to successfully forage, and their overall foraging performance was significantly altered. Inhibition of BNST GABA neurons during live predator exposure prevented changes in foraging behavior from developing after live predator threat. BNST GABA neuron inhibition did not alter foraging behavior during robotic or live predator threat. We conclude that while both robotic and live predator encounter effectively intrude on foraging behavior, the perceived risk and behavioral consequence of the threats are distinguishable. Additionally, BNST GABA neurons may play a role in the integration of prior innate predator threat experience that results in hypervigilance during post-encounter foraging behavior.
... In a similar vein, Orsini and colleagues (2016) measured rats' preferences between a large food reward that was sometimes accompanied by a shock and a smaller amount of food that carried no risk of shock, and found that female rats had a stronger preference for the smaller and safer option compared with male rats. Indeed, even a simulated predator cue (Zambetti et al., 2019) had a stronger impact on food-seeking behavior in female rats despite the absence of any actual painful outcome. ...
The ubiquity, importance, and sophistication of foraging behavior makes it an ideal platform for studying naturalistic decision making in animals. We developed a spatial patch-foraging task for rats, in which subjects chose how long to remain in one foraging patch as the rate of food earnings steadily decreased. The cost of seeking out a new location was varied across sessions. The behavioral task was designed to mimic the structure of natural foraging problems, where distinct spatial locations are associated with different reward statistics, and decisions require navigation and movement through space. Male and female rats generally followed the predictions of theoretical models of foraging, albeit with a consistent tendency to persist with patches for too long compared with behavioral strategies that maximize food intake rate. The tendency to choose overly-long patch residence times was stronger in male rats. We also observed sex differences in locomotion as rats performed the task, but these differences in movement only partially accounted for the differences in patch residence durations observed between male and female rats. Together, these results suggest a nuanced relationship between movement, sex, and foraging decisions.
... To maximize individual survival probability, animals should optimally have innate behaviors to cope with environmental threats and to fulfill internal demands. Evidence has shown that rodents prioritize loomingstimuli-evoked defensive behavior over sleeping [68] and foraging [85]. Furthermore, mice can rapidly learn that repeated stimuli is non-threatening and then adapt, which induces cognitively controlled suppression of escape behavior following looming stimuli [86]. ...
Background
Sex differences ranging from physiological functions to pathological disorders are developmentally hard-wired in a broad range of animals, from invertebrates to humans. These differences ensure that animals can display appropriate behaviors under a variety of circumstances, such as aggression, hunting, sleep, mating, and parental care, which are often thought to be important in the acquisition of resources, including territory, food, and mates. Although there are reports of an absence of sexual dimorphism in the context of innate fear, the question of whether there is sexual dimorphism of innate defensive behavior is still an open question. Therefore, an in-depth investigation to determine whether there are sex differences in developmentally hard-wired innate defensive behaviors in life-threatening circumstances is warranted.
Results
We found that innate defensive behavioral responses to potentially life-threatening stimuli between males and females were indistinguishable over their lifespan. However, by using 3 dimensional (3D)-motion learning framework analysis, we found that males and females showed different behavioral patterns after escaping to the refuge. Specifically, the defensive “freezing” occurred primarily in males, whereas females were more likely to return directly to exploration. Moreover, there were also no estrous phase differences in innate defensive behavioral responses after looming stimuli.
Conclusions
Our results demonstrate that visually-evoked innate fear behavior is highly conserved throughout the lifespan in both males and females, while specific post-threat coping strategies depend on sex. These findings indicate that innate fear behavior is essential to both sexes and as such, there are no evolutionary-driven sex differences in defensive ability.
... In fact, some researchers have questioned the evolutionary logic underlying fear conditioning; "No owl hoots or whistles 5 seconds before pouncing on a mouse…Nor will the owl give the mouse enough trials for the necessary learning to occur…What keeps animals alive in the wild is that they have very effective innate defensive reactions which occur when they encounter any kind of new or sudden stimulus" 32 . Consistent with this contrarian view are findings that laboratory rodents exhibit unlearned, instinctive fear responses to advancing artificial terrestrial and aerial predators 33,34 , overhead looming stimuli 35 , and predator odors 36 . ...
... Prior to placing each animal, the arena was wiped with 70% ethanol. The ANY-maze software and Ami interface system (Stoelting) connected to a PC automatically tracked the animal's position in the arena, via a ceiling mounted camera, and triggered the tone, shock, and aerial predator stimuli: (i) 3 kHz, 80 dB tone CS (measured from the trigger location; 81 dB within the nest area) was produced using ANY-maze (Stoelting) and presented through two speakers mounted on the nest-foraging border; (ii) 1 s, 2.5 mA shock US was delivered to the animal's dorsal neck/back region via a headstage tethered to a stimulus-isolator (Bak); (iii) A life-like model owl 34 , mounted onto a 92 cm pneumatic air cylinder (Bimba) at the opposite end of the foraging arena and hidden behind a black curtain, plunged downward towards the rat (46 cm/s), then retracted back to it starting position. ...
Pavlovian fear conditioning, which offers the advantage of simplicity in both the control of conditional and unconditional stimuli (CS, US) presentation and the analysis of specific conditional and unconditional responses (CR, UR) in a controlled laboratory setting, has been the standard model in basic and translational fear research. Despite 100 years of experiments, the utility of fear conditioning has not been trans-situationally validated in real-life contexts. We thus investigated whether fear conditioning readily occurs and guides the animal’s future behavior in an ecologically-relevant environment. To do so, Long-Evans rats foraging for food in an open arena were presented with a tone CS paired with electric shock US to their dorsal neck/body that instinctively elicited escape UR to the safe nest. On subsequent test days, the tone-shock paired animals failed to exhibit fear CR to the CS. In contrast, animals that encountered a realistic agent of danger (a looming artificial owl) paired with a shock, simulating a plausible predatory strike, instantly fled to the nest when presented with a tone for the first time. These results highlight the possibility of a nonassociative, rather than standard associative, fear process providing survival function in life-threatening situations that animals are likely to encounter in nature.
... There is a long history of studying sex differences in discounting (in both human and non-human species), and while evidence is mixed, some studies have reported sex differences on intertemporal choice paradigms (Doidge et al., 2021;Grissom & Reyes, 2019;Haaren et al., 1988;Hernandez et al., 2020;Perry et al., 2005;Weafer & de Wit, 2014). The prospect of reliable sex differences in delay discounting, raises the possibility of sex differences in foraging strategies (Chaby et al., 2016;Zambetti et al., 2019). While more work is necessary (Orsini & Setlow, 2017;Shansky, 2018;Shansky & Murphy, 2021;Shansky & Woolley, 2016), these results could have interesting theoretical implications for models of foraging. ...
... For instance, prey species like rats and mice devote considerable resources to detecting and avoiding potential predators. This is critical in natural settings (Beauchamp, 2015) and occurs in the laboratory as well (Wallace et al., 2013;Yilmaz & Meister, 2013;Zambetti et al., 2019), yet it is unclear how goals like predator avoidance are balanced with foraging efficiency. Those who work with rodents have likely witnessed an unexpected noise interrupt ongoing behavior. ...
... Knowing how foraging computations are affected by interruptions may be critical to interpreting foraging decisions. Experiments that program the occurrence of startling events or introduce artificial predators during foraging could examine how these factors interact with foraging decisions (Amir et al., 2015;Chaby et al., 2016;Kim & Jung, 2018;Mobbs et al., 2018;Pellman & Kim, 2016;Walters et al., 2019;Zambetti et al., 2019). Recent years have also seen great advances in computational techniques for identifying statistical structure in animal behavior (Calhoun et al., 2019;Gris et al., 2017;Hsu & Yttri, 2021;McCullough & Goodhill, 2021;Wiltschko et al., 2015). ...
Theoretical models of foraging are based on the maximization of food intake rate. Remarkably, foragers often hew close to the predictions of rate maximization, except for a frequently observed bias to remain in patches for too long. By sticking with depleting options beyond the optimal patch residence time-a phenomenon referred to as overharvesting or overstaying-foragers miss out on food they could have earned had they sought a new option elsewhere. Here, we review potential causes of overstaying and consider the role that temporal cognition might play in this phenomenon. We first consider how an explicit, internal sense of time might inform foraging behaviors, and next examine patch-leaving choices from the perspective of intertemporal decision-making. Finally, we identify promising areas for future research that will provide a better understanding of how foraging decisions are made, and what factors drive the tendency to overharvest patches. (PsycInfo Database Record (c) 2022 APA, all rights reserved).
... Results revealed an amygdala dependent modulation of circadian rhythms can be elicited when the fear is timed to circadian cues (Pellman et al., 2015). In addition, realistic predator stimuli such as a plastic owl that surges from behind a hidden curtain while a hungry rat is foraging for food elicits opposite habituation to the fear related cues and willingness to enter a fear context in males and females than what is observed when using footshock and freezing as measures (Zambetti et al., 2019). Specifically, female rats are much less likely to approach the zone in which the owl surges than male rats. ...
In this Perspective review, we highlight some of the less explored aspects of lateral habenula (LHb) function in contextual memory, sleep, and behavioral flexibility. We provide evidence that LHb is well-situated to integrate different internal state and multimodal sensory information from memory-, stress-, motivational-, and reward-related circuits essential for both survival and decision making. We further discuss the impact of early life stress (ELS) on LHb function as an example of stress-induced hyperactivity and dysregulation of neuromodulatory systems within the LHb that promote anhedonia and motivational deficits following ELS. We acknowledge that recent technological advancements in manipulation and recording of neural circuits in simplified and well-controlled behavioral paradigms have been invaluable in our understanding of the critical role of LHb in motivation and emotional regulation as well as the involvement of LHb dysfunction in stress-induced psychopathology. However, we also argue that the use of ethologically-relevant behaviors with consideration of complex aspects of decision-making is warranted for future studies of LHb contributions in a wide range of psychiatric illnesses. We conclude this Perspective with some of the outstanding issues for the field to consider where a multi-systems approach is needed to investigate the complex nature of LHb circuitry interactions with environmental stimuli that predisposes psychiatric disorders.
... In rats in the laboratory setting a number of stimuli have been identified that evoke innate defensive escape behaviors that include emission of 22 kHz USVs. These include mild restraint stress (153) (Figure 2); air puff (154,155); forced swimming (156); overhead looming stimuli simulating aerial attack (157) and unavoidable acute or repeated footshocks (158). The 22 kHz USVs emitted in these settings are widely believed to reflect a negative affective state akin to anxiety and fear (159). ...
Anxiety disorders are more prevalent in women than in men. In women the menstrual cycle introduces another variable; indeed, some conditions e.g., premenstrual syndrome, are menstrual cycle specific. Animal models of fear and anxiety, which form the basis for research into drug treatments, have been developed almost exclusively, using males. There remains a paucity of work using females and the available literature presents a confusing picture. One confound is the estrous cycle in females, which some authors consider, but many do not. Importantly, there are no accepted standardized criteria for defining cycle phase, which is important given the rapidly changing hormonal profile during the 4-day cycle of rodents. Moreover, since many behavioral tests that involve a learning component or that consider extinction of a previously acquired association require several days to complete; the outcome may depend on the phase of the cycle on the days of training as well as on test days. In this article we consider responsiveness of females compared to males in a number of commonly used behavioral tests of anxiety and fear that were developed in male rodents. We conclude that females perform in a qualitatively similar manner to males in most tests although there may be sex and strain differences in sensitivity. Tests based on unconditioned threatening stimuli are significantly influenced by estrous cycle phase with animals displaying increased responsiveness in the late diestrus phase of the cycle (similar to the premenstrual phase in women). Tests that utilize conditioned fear paradigms, which involve a learning component appear to be less impacted by the estrous cycle although sex and cycle-related differences in responding can still be detected. Ethologically-relevant tests appear to have more translational value in females. However, even when sex differences in behavior are not detected, the same outward behavioral response may be mediated by different brain mechanisms. In order to progress basic research in the field of female psychiatry and psychopharmacology, there is a pressing need to validate and standardize experimental protocols for using female animal models of anxiety-related states.
... Several prior studies have compared males and female rodents' performance in contextual fear conditioning and collectively the results are ambivalent. Some studies have reported males showing stronger context fear conditioning (Maren et al., 1994;Wiltgen et al., 2001;Chang et al., 2009;Gresack et al., 2009;Barker and Galea, 2010;Mizuno et al., 2012;Colon et al., 2018;Colon and Poulos, 2020) whereas others showed equivalent levels of contextual fear in males and females (Kosten et al., 2006;Dachtler et al., 2011;Keiser et al., 2017), and some studies have even reported stronger context fear conditioning in females (Fenton et al., 2016;Blume et al., 2017;Zambetti et al., 2019). Nearly all of these prior studies have used freezing behavior to assess learning, meaning that the discrepant results are not simply because these studies used different measures of fear. ...
The study of fear conditioning has led to a better understanding of fear and anxiety-based disorders such as post-traumatic stress disorder (PTSD). Despite the fact many of these disorders are more common in women than in men, the vast majority of work investigating fear conditioning in rodents has been conducted in males. The goal of the work presented here was to better understand how biological sex affects contextual fear conditioning and expression. To this end, rats of both sexes were trained to fear a specific context and fear responses were measured upon re-exposure to the conditioning context. In the first experiment, male and female rats were given context fear conditioning and tested the next day during which freezing behavior was measured. In the second experiment, rats were trained and tested in a similar fashion while fear-potentiated startle and defecation were measured. We found that males showed more freezing behavior than females during a fear expression test. The expression of fear-potentiated startle did not differ between sexes, while males exhibited more defecation during a test in a novel context. These data suggest that the expression of defensive behavior differs between sexes and highlight the importance of using multiple measures of fear when comparing between sexes.
... To evaluate threat related changes in foraging, the animals are confronted with a threat stimulus in the foraging area, such as the smell of a predator [9] or an electric shock [8]. In response to such threat encounter animals show an increase in risk assessment behaviors, e.g., attentive head-scanning [10], an inhibition of appetitive behavior [11], an increased latency in the procurement of food pellets [12] as well as a reduction in number of meals accompanied by an increase of the size of portions to maintain caloric intake [8]. ...
The spreading of COVID-19 has led to panic buying all over the world. In this study, we applied an animal model framework to elucidate changes in human purchasing behavior under COVID-19 pandemic conditions. Purchasing behavior and potential predictors were assessed in an online questionnaire format ( N = 813). Multiple regression analyses were used to evaluate the role of individually Perceived Threat of COVID-19 , anxiety related personality traits (trait-anxiety, intolerance of uncertainty) and the role of media exposure in predicting quantity and frequency of purchasing behavior. High levels of Perceived Threat of COVID-19 were associated significantly with a reported reduction in purchasing frequency ( b = -.24, p < .001) and an increase in the quantity of products bought per purchase ( b = .22, p < .001). These results are comparable to observed changes in foraging behavior in rodents under threat conditions. Higher levels of intolerance of uncertainty ( b = .19, p < .001) and high extend of media exposure ( b = .27, p < .001) were positively associated with Perceived Threat of COVID-19 and an increase in purchasing quantity. This study contributes to our understanding of aberrated human purchasing behavior and aims to link findings from animal research to human behavior beyond experimental investigations.
Women are more likely to develop an anxiety disorder than men. Yet, preclinical models of anxiety were largely developed in male rodents, with poorly understood predictive validity for sex differences. Here, we investigate whether commonly used anxiety-like behavior tests, elevated plus maze (EPM) and open field (OF), represent the human sex difference in adult Sprague-Dawley rats. When interpreted by EPM or OF, female rats displayed less anxiety-like behavior compared to males, as they spent twice as much time in the open arm of the EPM or the center of the OF compared to males. However, they also displayed vastly different levels of locomotor activity, possibly confounding interpretation of these locomotion-dependent tests. To exclude locomotion from the assessment, the acoustic startle response (ASR) test was used. When interpreted by the ASR test, females displayed more anxiety-like behavior compared to males, as indicated by a nearly two-fold higher startle amplitude. The observed sex differences were not driven by gonadal steroids. Overall, all but one of the tests fail to mirror the sex difference in anxiety reported in humans. Our findings suggest that the ASR might be a better fit in modelling female anxiety-like behavior.
