Lasting recognition of threatening people by wild American crows

Marzluff, John M.; Walls, Jeff; Cornell, Heather N; Withey, John C.; Craig, David P.

doi:10.1016/j.anbehav.2009.12.022

Cited by 172 publications

(156 citation statements)

References 40 publications

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“…We demonstrated previously that free-ranging American crows (Corvus brachyrhynchos) discriminate among humans based on facial characteristics, but we could only speculate on the neural basis for this behavior (1,6). Because birds and mammals share some common sensory and motor circuits (7), we hypothesized that recognition of humans by crows might involve a distributed set of interactive brain regions.…”

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confidence: 99%

“…American crow | cognition | facial recognition | [F-18]fluorodeoxyglucose-PET imaging | learned fear A variety of species are able to discriminate between human faces (1)(2)(3), and this ability appears to be linked to neural integration of perception, emotion, and memory. Brain imaging studies have revealed that humans use a core recognition system in their sensory cortex (the posterior superior temporal sulcus, the inferior occipital gyrus, and the fusiform gyrus) networked with two extended systems that convey the historical (anterior paracingulate, posterior superior temporal sulcus/temporoparietal junction, anterior temporal cortex, precuneus, and posterior cingulate) and emotional (amygdala, insula, and striatum) significance of the person (4).…”

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Brain imaging reveals neuronal circuitry underlying the crow’s perception of human faces

Marzluff¹,

Miyaoka

Minoshima

et al. 2012

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

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Crows pay close attention to people and can remember specific faces for several years after a single encounter. In mammals, including humans, faces are evaluated by an integrated neural system involving the sensory cortex, limbic system, and striatum. Here we test the hypothesis that birds use a similar system by providing an imaging analysis of an awake, wild animal's brain as it performs an adaptive, complex cognitive task. We show that in vivo imaging of crow brain activity during exposure to familiar human faces previously associated with either capture (threatening) or caretaking (caring) activated several brain regions that allow birds to discriminate, associate, and remember visual stimuli, including the rostral hyperpallium, nidopallium, mesopallium, and lateral striatum. Perception of threatening faces activated circuitry including amygdalar, thalamic, and brainstem regions, known in humans and other vertebrates to be related to emotion, motivation, and conditioned fear learning. In contrast, perception of caring faces activated motivation and striatal regions. In our experiments and in nature, when perceiving a threatening face, crows froze and fixed their gaze (decreased blink rate), which was associated with activation of brain regions known in birds to regulate perception, attention, fear, and escape behavior. These findings indicate that, similar to humans, crows use sophisticated visual sensory systems to recognize faces and modulate behavioral responses by integrating visual information with expectation and emotion. Our approach has wide applicability and potential to improve our understanding of the neural basis for animal behavior.A variety of species are able to discriminate between human faces (1-3), and this ability appears to be linked to neural integration of perception, emotion, and memory. Brain imaging studies have revealed that humans use a core recognition system in their sensory cortex (the posterior superior temporal sulcus, the inferior occipital gyrus, and the fusiform gyrus) networked with two extended systems that convey the historical (anterior paracingulate, posterior superior temporal sulcus/temporoparietal junction, anterior temporal cortex, precuneus, and posterior cingulate) and emotional (amygdala, insula, and striatum) significance of the person (4). This network of brain regions that perceive and analyze faces is informed by ventral and dorsal visual pathways-the ventral enabling fine discrimination and the dorsal providing rapid, but coarse, emotional assessment (3). Brain mapping investigations on other species capable of human recognition are extremely limited; however, electrophysiological recordings in the visual cortex of domestic sheep and nonhuman primates have indicated the presence of neurons that respond to human facial information (5).We demonstrated previously that free-ranging American crows (Corvus brachyrhynchos) discriminate among humans based on facial characteristics, but we could only speculate on the neural basis for this behavior (1, 6). Because bi...

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Brain imaging reveals neuronal circuitry underlying the crow’s perception of human faces

Marzluff¹,

Miyaoka

Minoshima

et al. 2012

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

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“…This focus has demonstrated that a number of different species are able to use visual cues to distinguish between individual humans that present varying levels of threat (4,5,(14)(15)(16). However, acoustic cues could potentially provide a more effective means of classifying human predators by virtue of enabling categories of particularly dangerous humans to be identified.…”

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“…animal cognition | communication | social behavior | predator recognition | vocalization T he ability to recognize predators and assess the level of threat that they pose is a crucial cognitive skill for many wild animals that has very direct and obvious fitness consequences (1)(2)(3)(4)(5). Until recently, most research in this area focused on how a range of birds and mammals classify other animal predators, demonstrating complex abilities to differentiate between predators with different hunting styles and respond with appropriate escape tactics (2,3,(6)(7)(8).…”

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Elephants can determine ethnicity, gender, and age from acoustic cues in human voices

McComb

Shannon

Sayialel

et al. 2014

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

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Animals can accrue direct fitness benefits by accurately classifying predatory threat according to the species of predator and the magnitude of risk associated with an encounter. Human predators present a particularly interesting cognitive challenge, as it is typically the case that different human subgroups pose radically different levels of danger to animals living around them. Although a number of prey species have proved able to discriminate between certain human categories on the basis of visual and olfactory cues, vocalizations potentially provide a much richer source of information. We now use controlled playback experiments to investigate whether family groups of free-ranging African elephants (Loxodonta africana) in Amboseli National Park, Kenya can use acoustic characteristics of speech to make functionally relevant distinctions between human subcategories differing not only in ethnicity but also in sex and age. Our results demonstrate that elephants can reliably discriminate between two different ethnic groups that differ in the level of threat they represent, significantly increasing their probability of defensive bunching and investigative smelling following playbacks of Maasai voices. Moreover, these responses were specific to the sex and age of Maasai presented, with the voices of Maasai women and boys, subcategories that would generally pose little threat, significantly less likely to produce these behavioral responses. Considering the long history and often pervasive predatory threat associated with humans across the globe, it is likely that abilities to precisely identify dangerous subcategories of humans on the basis of subtle voice characteristics could have been selected for in other cognitively advanced animal species.T he ability to recognize predators and assess the level of threat that they pose is a crucial cognitive skill for many wild animals that has very direct and obvious fitness consequences (1-5). Until recently, most research in this area focused on how a range of birds and mammals classify other animal predators, demonstrating complex abilities to differentiate between predators with different hunting styles and respond with appropriate escape tactics (2, 3, 6-8). However, for many wild populations, humans represent a significant predatory threat (5, 9, 10) and this threat is rapidly increasing as areas for wildlife decrease and humananimal conflict grows. Moreover, as it is typically the case that not all humans pose the same risk to prey species, distinguishing between different human subgroups to identify those associated with genuinely threatening situations could present a major cognitive challenge. The extent of behavioral flexibility that different species may exhibit in correctly classifying human predators-and the degree of sophistication possible in such abilities-is therefore of considerable interest.Most research on the abilities of animals to classify human predators has focused on discrimination through facial features or general differences in behavior and appear...

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“…The study of how animals first identify threats from other species constitutes a growing body of literature, including the different alarm calls for different predators in vervet monkeys (6) and prairie dogs (7) and the ability of wild corvids to recognize individual humans by their faces (8,9). Such fine discriminatory abilities may help distinguish dangerous from nondangerous encounters with one of the most threatening species on the planet: ours.…”

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confidence: 99%