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      Chronic stress influences attentional and judgement bias and the activity of the HPA axis in sheep

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          Abstract

          Introduction

          Environmental challenges are part of everyday life for most domestic animals. However, very little is known about how animals cope emotionally and physiologically with cumulative challenges. This experiment aimed to determine the impact of long-term exposure to environmental challenges on the affective state and hypothalamic-pituitary-adrenal (HPA) axis responses to a subsequent additional acute shearing challenge.

          Methods

          Sheep were exposed to either a long-term environmental challenge (rest disruption and individual housing) in order to induce chronic stress (chronic stress group) or control conditions (group housing in a field with low stress handling and daily feed rewards, control group). Judgement and attention bias were assessed as measures of the emotional state following several days of the challenge or control treatment (pre-shearing tests). In addition, the responsiveness of the HPA-axis was evaluated using a combined Corticotropin Releasing Hormone and Arginine Vasopressin (CRH/AVP) challenge. Finally, all animals were exposed to an acute shearing challenge, then judgement bias (post-shearing test), HPA-axis and internal body temperature responses were determined.

          Results

          In the pre-shearing judgement bias test, the chronic stress group slightly increased optimism compared to the control treatment. In the attention bias test, the chronic stress group showed reduced vigilance behaviour towards a predator threat and a quicker approach to the food compared to the control treatment. The chronic stress group also had lower plasma ACTH concentrations in response to the CRH/AVP challenge compared to the control group, no differences in cortisol concentrations were found. In the post-shearing judgement bias test, differences in optimism were no longer evident between the chronic stress and control groups. Plasma ACTH concentrations and body temperatures showed a greater increase in response to shearing in the chronic stress group compared to the control group.

          Conclusion

          Our results suggest that long-term exposure to challenges biased cognitive measures of the affective state towards an increased expectation of a reward and reduced attention towards a threat. The exaggerated ACTH responses in the chronic stress group may be indicative of HPA-axis dysregulation. Despite a period of challenge exposure in the chronic stress group, judgement bias responses to the shearing challenge were similar in the chronic stress and control groups; the reasons for this need further investigation. The altered affective state together with signs of HPA-axis dysregulation may indicate an increased risk of compromised welfare in animals exposed to long-term environmental challenges.

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          Most cited references63

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          Emotion, cognition, and behavior.

          R J Dolan (2002)
          Emotion is central to the quality and range of everyday human experience. The neurobiological substrates of human emotion are now attracting increasing interest within the neurosciences motivated, to a considerable extent, by advances in functional neuroimaging techniques. An emerging theme is the question of how emotion interacts with and influences other domains of cognition, in particular attention, memory, and reasoning. The psychological consequences and mechanisms underlying the emotional modulation of cognition provide the focus of this article.
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            Stress revisited: a critical evaluation of the stress concept.

            With the steadily increasing number of publications in the field of stress research it has become evident that the conventional usage of the stress concept bears considerable problems. The use of the term 'stress' to conditions ranging from even the mildest challenging stimulation to severely aversive conditions, is in our view inappropriate. Review of the literature reveals that the physiological 'stress' response to appetitive, rewarding stimuli that are often not considered to be stressors can be as large as the response to negative stimuli. Analysis of the physiological response during exercise supports the view that the magnitude of the neuroendocrine response reflects the metabolic and physiological demands required for behavioural activity. We propose that the term 'stress' should be restricted to conditions where an environmental demand exceeds the natural regulatory capacity of an organism, in particular situations that include unpredictability and uncontrollability. Physiologically, stress seems to be characterized by either the absence of an anticipatory response (unpredictable) or a reduced recovery (uncontrollable) of the neuroendocrine reaction. The consequences of this restricted definition for stress research and the interpretation of results in terms of the adaptive and/or maladaptive nature of the response are discussed. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Animal behaviour: cognitive bias and affective state.

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 January 2019
                2019
                : 14
                : 1
                : e0211363
                Affiliations
                [1 ] CSIRO, Agriculture and Food, Locked Bag 1, Armidale NSW, Australia
                [2 ] School of Agriculture and Environment and the University of Western Australia Institute of Agriculture, The University of Western Australia, Crawley WA, Australia
                Radboud University Medical Centre, NETHERLANDS
                Author notes

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

                Author information
                http://orcid.org/0000-0002-1223-3480
                Article
                PONE-D-18-24829
                10.1371/journal.pone.0211363
                6353200
                30699168
                8e9fcc5d-be6f-484b-8304-c3f70116cc5f
                © 2019 Verbeek 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
                : 23 August 2018
                : 12 January 2019
                Page count
                Figures: 5, Tables: 2, Pages: 23
                Funding
                This work was supported by an Office of the Chief Executive Postdoctoral Fellowship Award, awarded by the Commonwealth Scientific and Industry Research Organization to CL, Australia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Sheep
                Medicine and Health Sciences
                Mental Health and Psychiatry
                Psychological Stress
                Biology and Life Sciences
                Psychology
                Psychological Stress
                Social Sciences
                Psychology
                Psychological Stress
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Body Temperature
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Body Temperature
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Cortisol
                Biology and Life Sciences
                Biochemistry
                Hormones
                Steroid Hormones
                Cortisol
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Biology and Life Sciences
                Psychology
                Behavior
                Social Sciences
                Psychology
                Behavior
                Biology and Life Sciences
                Psychology
                Emotions
                Social Sciences
                Psychology
                Emotions
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognitive Psychology
                Attention
                Biology and Life Sciences
                Psychology
                Cognitive Psychology
                Attention
                Social Sciences
                Psychology
                Cognitive Psychology
                Attention
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                All relevant data are within the manuscript and its Supporting Information files.

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