Function follows form: ecological constraints on odor codes and olfactory percepts

Gottfried, Jay A.

doi:10.1016/j.conb.2009.07.012

Cited by 43 publications

(26 citation statements)

References 52 publications

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“…It may be that following fewer encounters with the odor the rats learned to ignore a more general quail odor, reducing the likelihood of the eggs attracting attention after their introduction. Black rats should have the olfactory capability to distinguish between quail odor and egg odor (25), but generalizing may be less cognitively costly and adequate for normal foraging activities (16,26). That rats required little spatial reinforcement to filter an unrewarding odor into their olfactory background suggests their cognitive processes are adapted for optimizing foraging efficiency in situations where encountering novel food is common.…”

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

“…Mammalian predators live in a rich olfactory world, able to detect and recognize immense numbers of odors and distinguish minute differences in complex mixtures (13,14). Such capabilities should hinder efficient foraging unless superfluous olfactory information can be quickly disregarded (15,16).Bird eggs and nestlings are readily found by scent-hunting predators, and predation by alien mammals, such as black rats, Rattus rattus, poses a major threat to the conservation of many avian species globally (17). Inducing populations of wild predators to ignore the cues of vulnerable prey could relax the risk faced by prey during critical times, such as nesting.…”

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Exploiting olfactory learning in alien rats to protect birds’ eggs

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Banks

2012

Proc. Natl. Acad. Sci. U.S.A.

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Predators must ignore unhelpful background "noise" within information-rich environments and focus on useful cues of prey activity to forage efficiently. Learning to disregard unrewarding cues should happen quickly, weakening future interest in the cue. Prey odor, which is rapidly investigated by predators, may be particularly appropriate for testing whether consistently unrewarded cues are ignored, and whether such behavior can be exploited to benefit prey. Using wild free-ranging populations of black rats, Rattus rattus, an alien predator of global concern, we tested whether the application of bird-nesting odors before the introduction of artificial nests (odor preexposure), enhanced the survival of birds eggs (prey) compared with areas where prey and nesting odors were introduced concurrently. In areas where predators had encountered prey odor before prey being available, the subsequently introduced eggs showed 62% greater survival than in areas where prey and odor were introduced together. We suggest that black rats preexposed to prey odor learned to ignore the unrewarding cue, leading to a significant improvement in prey survival that held for the 7-d monitoring period. Exploiting rapid learning that underpins foraging decisions by manipulating sensory contexts offers a nonlethal, but effective approach to reducing undesirable predatory impacts. Techniques based on olfactory preexposure may provide prey with protection during critical periods of vulnerability, such as immediately following a prey reintroduction. These results also highlight the potential benefits to species conservation to be gained from a greater understanding of the cognitive mechanisms driving alien predator behavior within ecological contexts.predation | sensory learning | habituation | foraging behavior | information use E fficient predators must identify and then pursue cues of profitable prey while ignoring stimuli that have proved unrewarding (1, 2). Such optimal foraging tactics rely on complex discrimination tasks being made rapidly and accurately within dynamic environments and benefit from attentional mechanisms, such as search images (3, 4), which assist the hunter to focus on useful information. How unrewarding prey cues are ignored remains unexplored in ecological contexts, despite the obvious fitness advantage for generalist predators switching between multiple prey. Being able to deceive predators into ignoring relevant cues may also have practical implications for assisting the survival of vulnerable prey that have ineffective defenses, such as some native prey facing alien predators (5).Optimal behavior models imply that previous experience influences whether a predator pursues or ignores prey cues (6, 7). In a study examining predatory behavior in wild red squirrels Tamiasciurus hudsonicus, Pelech et al. (8) showed that squirrels experienced in finding artificial nests containing food found nests quicker than nonexperienced animals. Successful foraging experience facilitated faster detection of nests and increased prey vu...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Exploiting olfactory learning in alien rats to protect birds’ eggs

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Banks

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Many factors may influence the perception of a mixture such as chemical structure, intensity or salience of the components and mixture complexity (Gottfried 2009;Riffell 2012;Thomas-Danguin et al 2014). Interactions between odor molecules occur at the receptor level of the olfactory system (e.g., Bell et al 1987;DuchampViret et al 2003;Kay et al 2003), in the olfactory bulb (antennal lobe in insects; e.g., Linster et al 2001;Deisig et al 2006;Dulac 2006) and/or in higher brain areas (e.g., Boyle et al 2009;Gottfried 2010;Wilson and Sullivan 2011).…”

Section: Introductionmentioning

confidence: 99%

Brain processing of a configural vs elemental odor mixture in the newborn rabbit

et al. 2015

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Organisms are surrounded throughout life by chemically complex odors. How individuals process an odorant within a mixture or a mixture as a whole is a key question in neuroethology and chemical senses. This question is addressed here by using newborn rabbits, which can be rapidly conditioned to a new stimulus by single association with the mammary pheromone. After conditioning to ethyl maltol (odorant B), pups behaviorally respond to B and an A'B' mixture (68/32 ratio) but not to ethyl isobutyrate (odorant A) or an AB mixture (30/70 ratio). This suggests elemental and configural perception of A'B' and AB, respectively. We then explored the neural substrates underlying the processing of these mixtures with the hypothesis that processing varies according to perception. Pups were pseudoconditioned or conditioned to B on postnatal day 3 before exposure to B, A'B' or AB on day 4. Fos expression was not similar between groups (mainly in the olfactory bulb and posterior piriform cortex) suggesting a differential processing of the stimuli that might reflect either stimulus complexity or conditioning effect. Thus, the ratio of components in A'B' vs AB leads to differential activation of the olfactory system which may contribute to elemental and configural percepts of these mixtures. In addition, together with recent behavioral data, this highlights that configural perception occurs even in relatively immature animals, emphasizing the value of the newborn rabbit for exploration of odor mixture processing from molecules to brain and behavior.

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“…bee, catfish, human, spiny lobster, moth and rat), with different approaches (e.g. [9][10][11][12][13][14][15][16]). For instance, data in human adults revealed that a mixture of two odorants (AB), one smelling like strawberry (A: ethyl isobutyrate) and the other like caramel (B: ethyl maltol), generates the configural perception of a pineapple odour at a specific ratio of A/B [17,18].…”

Section: Introductionmentioning

confidence: 99%

Neonatal representation of odour objects: distinct memories of the whole and its parts

et al. 2014

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Extraction of relevant information from highly complex environments is a prerequisite to survival. Within odour mixtures, such information is contained in the odours of specific elements or in the mixture configuration perceived as a whole unique odour. For instance, an AB mixture of the element A (ethyl isobutyrate) and the element B (ethyl maltol) generates a configural AB percept in humans and apparently in another species, the rabbit. Here, we examined whether the memory of such a configuration is distinct from the memory of the individual odorants. Taking advantage of the newborn rabbit's ability to learn odour mixtures, we combined behavioural and pharmacological tools to specifically eliminate elemental memory of A and B after conditioning to the AB mixture and evaluate consequences on configural memory of AB. The amnesic treatment suppressed responsiveness to A and B but not to AB. Two other experiments confirmed the specific perception and particular memory of the AB mixture. These data demonstrate the existence of configurations in certain odour mixtures and their representation as unique objects: after learning, animals form a configural memory of these mixtures, which coexists with, but is relatively dissociated from, memory of their elements. This capability emerges very early in life.

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Function follows form: ecological constraints on odor codes and olfactory percepts

Cited by 43 publications

References 52 publications

Exploiting olfactory learning in alien rats to protect birds’ eggs

Exploiting olfactory learning in alien rats to protect birds’ eggs

Brain processing of a configural vs elemental odor mixture in the newborn rabbit

Neonatal representation of odour objects: distinct memories of the whole and its parts

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