Fox urine exposure induces avoidance behavior in rats and activates the amygdalar olfactory cortex

Wernecke, Kerstin E.A.; Vincenz, Daniel; Storsberg, Silke D; D'Hanis, Wolfgang; Goldschmidt, Jürgen; Fendt, Markus

doi:10.1016/j.bbr.2014.11.020

Cited by 22 publications

(15 citation statements)

References 66 publications

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“…Mice mainly rely on their sense of smell to avoid danger. Thus, when given the opportunity, they readily avoid spots containing predator kairomones (Root et al, 2014 ; Wernecke et al, 2015 ). Our results in female CD1 mice, showing that they avoid a zone containing TMT, a putative kairomone, are in agreement with this view.…”

Section: Discussionmentioning

confidence: 99%

Avoidance and contextual learning induced by a kairomone, a pheromone and a common odorant in female CD1 mice

et al. 2015

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Chemosignals mediate both intra- and inter-specific communication in most mammals. Pheromones elicit stereotyped reactions in conspecifics, whereas kairomones provoke a reaction in an allospecific animal. For instance, predator kairomones elicit anticipated defensive responses in preys. The aim of this work was to test the behavioral responses of female mice to two chemosignals: 2-heptanone (2-HP), a putative alarm pheromone, and 2,4,5-trimethylthiazoline (TMT), a fox-derived putative kairomone, widely used to investigate fear and anxiety in rodents. The banana-like odorant isoamyl acetate (IA), unlikely to act as a chemosignal, served as a control odorant. We first presented increasing amounts of these odorants in consecutive days, in a test box in which mice could explore or avoid them. Female mice avoided the highest amounts of all three compounds, with TMT and IA eliciting avoidance at lower amounts (3.8 pmol and 0.35 μmol, respectively) than 2-HP (35 μmol). All three compounds induced minimal effects in global locomotion and immobility in this set up. Further, mice detected 3.5 pmol of TMT and IA in a habituation–dishabituation test, so avoidance of IA started well beyond the detection threshold. Finally, both TMT and IA, but not 2-HP, induced conditioned place avoidance and increased immobility in the neutral compartment during a contextual memory test. These data suggest that intense odors can induce contextual learning irrespective of their putative biological significance. Our results support that synthetic predator-related compounds (like TMT) or other intense odorants are useful to investigate the neurobiological basis of emotional behaviors in rodents. Since intense odorants unlikely to act as chemosignals can elicit similar behavioral reactions than chemosignals, we stress the importance of using behavioral measures in combination with other physiological (e.g., hormonal levels) or neural measures (e.g., immediate early gene expression) to establish the ethological significance of odorants.

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Section: Discussionmentioning

confidence: 99%

Avoidance and contextual learning induced by a kairomone, a pheromone and a common odorant in female CD1 mice

et al. 2015

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“…In contrast to this, we wanted to mainly investigate how hole visits are influenced by aversive odors. Based on previous studies from our laboratory ( Fendt, 2006 ; Ferrero et al, 2011 ; Wernecke et al, 2015 ), we expected that holes with aversive odors will be visited less often, i.e., avoided. Such avoidance is much easier to observe when holes are very often visited under control conditions.…”

Section: Methodsmentioning

confidence: 99%

“…For instance, Osada et al (2013) observed that mice similarly avoided the short arm of a Y-maze when it contained wolf urine. Using an open-field test we previously showed that rats avoid the quadrant or corner of the testing arena containing carnivore urine, e.g., from foxes, bobcats, pumas, coyotes, or lions ( Fendt, 2006 ; Ferrero et al, 2011 ; Wernecke et al, 2015 ). This is confirmed by field studies demonstrating that carnivore urine samples (e.g., dingo, coyote, bobcat, wolf) are effective repellents protecting forestry and agricultural areas from feeding-related damage ( Nolte et al, 1994 ; Bramley and Waas, 2001 ; Parsons et al, 2007 ).…”

Section: Methodsmentioning

confidence: 99%

“…In this context, predator odors warn prey animals of a potential confrontation with a predator. For example, odors derived from cats or other carnivorous species (e.g., urine samples from foxes, bobcats, pumas, and coyotes) elicit a range of innate defensive behaviors in rodents including avoidance and hiding behavior, an increase in risk assessment behaviors and the suppression of non-defensive behaviors such as foraging, sexual behavior and overall locomotor activity ( Blanchard and Blanchard, 1989 ; Apfelbach et al, 2005 ; Endres et al, 2005 ; Masini et al, 2005 ; Fendt, 2006 ; Wernecke et al, 2015 ).…”

Section: General Introductionmentioning

confidence: 99%

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The olfactory hole-board test in rats: a new paradigm to study aversion and preferences to odors

Wernecke

Fendt

2015

Front. Behav. Neurosci.

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Odors of biological relevance (e.g., predator odors, sex odors) are known to effectively influence basic survival needs of rodents such as anti-predatory defensiveness and mating behaviors. Research focused on the effects of these odors on rats’ behavior mostly includes multi-trial paradigms where animals experience single odor exposures in subsequent, separated experimental sessions. In the present study, we introduce a modification of the olfactory hole-board test that allows studying the effects of different odors on rats’ behavior within single trials. First, we demonstrated that the corner holes of the hole-board were preferentially visited by rats. The placement of different odors under the corner holes changed this hole preference. We showed that holes with carnivore urine samples were avoided, while corner holes with female rat urine samples were preferred. Furthermore, corner holes with urine samples from a carnivore, herbivore, and omnivore were differentially visited indicating that rats can discriminate these odors. To test whether anxiolytic treatment specifically modulates the avoidance of carnivore urine holes, we treated rats with buspirone. Buspirone treatment completely abolished the avoidance of carnivore urine holes. Taken together, our findings indicate that the olfactory hole-board test is a valuable tool for measuring avoidance and preference responses to biologically relevant odors.

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“…Semiochemicals are divided into two major groups: pheromones (for conspecific communication) and allelochemicals (for interspecific communication) (Nielsen et al, 2015 ). Kairomones are allelochemicals that transfer unidirectionally from an emitter to a receiver and provide a benefit to the receiver organism (Brown et al, 1970 ; Liberles, 2014 ; Nielsen et al, 2015 ; Wernecke et al, 2015 ). Therefore, when a prey animal benefits, the chemical signal produced by a predator is a kairomone.…”

Section: Introductionmentioning

confidence: 99%

The scent of wolves: pyrazine analogs induce avoidance and vigilance behaviors in prey

2015

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The common gray wolf (Canis lupus) is an apex predator located at the top of the food chain in the Northern Hemisphere. It preys on rodents, rabbits, ungulates, and many other kinds of mammal. However, the behavioral evidence for, and the chemical basis of, the fear-inducing impact of wolf urine on prey are unclear. Recently, the pyrazine analogs 2, 6-dimethylpyrazine, 2, 3, 5-trimethylpyrazine and 3-ethyl-2, 5-dimethyl pyrazine were identified as kairomones in the urine of wolves. When mice were confronted with a mixture of purified pyrazine analogs, vigilance behaviors, including freezing and excitation of neurons at the accessory olfactory bulb, were markedly increased. Additionally, the odor of the pyrazine cocktail effectively suppressed the approach of deer to a feeding area, and for those close to the feeding area elicited fear-related behaviors such as the “tail-flag,” “flight,” and “jump” actions. In this review, we discuss the transfer of chemical information from wolf to prey through the novel kairomones identified in wolf urine and also compare the characteristics of wolf kairomones with other predator-produced kairomones that affect rodents.

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Fox urine exposure induces avoidance behavior in rats and activates the amygdalar olfactory cortex

Cited by 22 publications

References 66 publications

Avoidance and contextual learning induced by a kairomone, a pheromone and a common odorant in female CD1 mice

Avoidance and contextual learning induced by a kairomone, a pheromone and a common odorant in female CD1 mice

The olfactory hole-board test in rats: a new paradigm to study aversion and preferences to odors

The scent of wolves: pyrazine analogs induce avoidance and vigilance behaviors in prey

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