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      Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

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          Abstract

          Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs ( Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.

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          Most cited references34

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          The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety.

          The dynamic interactions between the amygdala and the medial prefrontal cortex (mPFC) are usefully conceptualized as a circuit that both allows us to react automatically to biologically relevant predictive stimuli as well as regulate these reactions when the situation calls for it. In this review, we will begin by discussing the role of this amygdala-mPFC circuitry in the conditioning and extinction of aversive learning in animals. We will then relate these data to emotional regulation paradigms in humans. Finally, we will consider how these processes are compromised in normal and pathological anxiety. We conclude that the capacity for efficient crosstalk between the amygdala and the mPFC, which is represented as the strength of the amygdala-mPFC circuitry, is crucial to beneficial outcomes in terms of reported anxiety. Copyright © 2011 Elsevier B.V. All rights reserved.
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            Facial Expressions of Emotion: Are Angry Faces Detected More Efficiently?

            The rapid detection of facial expressions of anger or threat has obvious adaptive value. In this study, we examined the efficiency of facial processing by means of a visual search task. Participants searched displays of schematic faces and were required to determine whether the faces displayed were all the same or whether one was different. Four main results were found: (1) When displays contained the same faces, people were slower in detecting the absence of a discrepant face when the faces displayed angry (or sad/angry) rather than happy expressions. (2) When displays contained a discrepant face people were faster in detecting this when the discrepant face displayed an angry rather than a happy expression. (3) Neither of these patterns for same and different displays was apparent when face displays were inverted, or when just the mouth was presented in isolation. (4) The search slopes for angry targets were significantly lower than for happy targets. These results suggest that detection of angry facial expressions is fast and efficient, although does not "pop-out" in the traditional sense.
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              What does it take to become 'best friends'? Evolutionary changes in canine social competence.

              The traditional and relatively narrow-focused research on ape-human comparisons has recently been significantly extended by investigations of different clades of animals, including the domestic dog (Canis familiaris). Here, we provide a short overview of how the comparative investigation of canine social behaviour advances our understanding of the evolution of social skills and argue that a system-level approach to dog social cognition provides a broader view on the 'human-likeness' of canine social competence. We introduce the concept of evolutionary social competence as a collateral notion of developmental social competence. We argue that such an extended perspective on social competence provides a useful tool for conceptualising wolf-dog differences in socio-cognitive functioning, as well as for considering specific social skills not in isolation, but as a part of a system. Copyright © 2013 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                13 January 2016
                2016
                : 11
                : 1
                : e0143047
                Affiliations
                [1 ]Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
                [2 ]Cognitive Science, Faculty of Behavioural Sciences, University of Helsinki, Helsinki, Finland
                [3 ]Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland
                [4 ]Department of Production Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
                University of Lincoln, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SS HT LH CMK OV. Performed the experiments: SS HT. Analyzed the data: SS LH. Contributed reagents/materials/analysis tools: OV CMK MVK. Wrote the paper: SS MVK LH OV CMK HT.

                Article
                PONE-D-14-56588
                10.1371/journal.pone.0143047
                4711950
                26761433
                a1f46b31-7e04-4be5-8a04-56611522252e
                © 2016 Somppi et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 17 December 2014
                : 30 October 2015
                Page count
                Figures: 4, Tables: 1, Pages: 16
                Funding
                Academy of Finland ( http://www.aka.fi) project #137931 to OV; Emil Aaltonen Foundation ( http://www.emilaaltonen.fi/) to SS; The Brain Research at Aalto University and University of Helsinki BRAHE consortium ( http://www.brain-mind.fi) to MVK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                All relevant data are within the paper and its Supporting Information files.

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