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      Human Analogue Safe Haven Effect of the Owner: Behavioural and Heart Rate Response to Stressful Social Stimuli in Dogs

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          Abstract

          The secure base and safe haven effects of the attachment figure are central features of the human attachment theory. Recently, conclusive evidence for human analogue attachment behaviours in dogs has been provided, however, the owner’s security-providing role in danger has not been directly supported. We investigated the relationship between the behavioural and cardiac response in dogs (N = 30) while being approached by a threatening stranger in separation vs. in the presence of the owner, presented in a balanced order. Non-invasive telemetric measures of heart rate (HR) and heart rate variability (HRV) data during the threatening approaches was compared to periods before and after the encounters. Dogs that showed distress vocalisation during separation (N = 18) and that growled or barked at the stranger during the threatening approach (N = 17) were defined as behaviourally reactive in the given situation. While characteristic stress vocalisations were emitted during separations, the absence of the owner did not have an effect on dogs’ mean HR, but significantly increased the HRV. The threatening approach increased dogs’ mean HR, with a parallel decrease in the HRV, particularly in dogs that were behaviourally reactive to the encounter. Importantly, the HR increase was significantly less pronounced when dogs faced the stranger in the presence of the owner. Moreover, the test order, whether the dog encountered the stranger first with or without its owner, also proved important: HR increase associated with the encounter in separation seemed to be attenuated in dogs that faced the stranger first in the presence of their owner. We provided evidence for human analogue safe haven effect of the owner in a potentially dangerous situation. Similarly to parents of infants, owners can provide a buffer against stress in dogs, which can even reduce the effect of a subsequent encounter with the same threatening stimuli later when the owner is not present.

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          Most cited references13

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          Heart-rate change as a component of the orienting response.

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            Effects of controlled breathing, mental activity and mental stress with or without verbalization on heart rate variability.

            To assess whether talking or reading (silently or aloud) could affect heart rate variability (HRV) and to what extent these changes require a simultaneous recording of respiratory activity to be correctly interpreted. Sympathetic predominance in the power spectrum obtained from short- and long-term HRV recordings predicts a poor prognosis in a number of cardiac diseases. Heart rate variability is often recorded without measuring respiration; slow breaths might artefactually increase low frequency power in RR interval (RR) and falsely mimic sympathetic activation. In 12 healthy volunteers we evaluated the effect of free talking and reading, silently and aloud, on respiration, RR and blood pressure (BP). We also compared spontaneous breathing to controlled breathing and mental arithmetic, silent or aloud. The power in the so called low- (LF) and high-frequency (HF) bands in RR and BP was obtained from autoregressive power spectrum analysis. Compared with spontaneous breathing, reading silently increased the speed of breathing (p < 0.05), decreased mean RR and RR variability and increased BP. Reading aloud, free talking and mental arithmetic aloud shifted the respiratory frequency into the LF band, thus increasing LF% and decreasing HF% to a similar degree in both RR and respiration, with decrease in mean RR but with minor differences in crude RR variability. Simple mental and verbal activities markedly affect HRV through changes in respiratory frequency. This possibility should be taken into account when analyzing HRV without simultaneous acquisition and analysis of respiration.
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              Cardiac vagal tone: a physiological index of stress.

              S Porges (1994)
              Cardiac vagal tone is proposed as a novel index of stress and stress vulnerability in mammals. A model is described that emphasizes the role of the parasympathetic nervous system and particularly the vagus nerve in defining stress. The model details the importance of a branch of the vagus originating in the nucleus ambiguus. In mammals the nucleus ambiguus not only coordinates sucking, swallowing, and breathing, but it also regulates heart rate and vocalizations in response to stressors. In mammals it is possible, by quantifying the amplitude of respiratory sinus arrhythmia, to assess the tonic and phasic regulation of the vagal pathways originating in the nucleus ambiguus. Measurement of this component of vagal tone is proposed as a method to assess, on an individual basis, both stress and the vulnerability to stress.
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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, USA )
                1932-6203
                2013
                4 March 2013
                : 8
                : 3
                : e58475
                Affiliations
                [1 ]MTA-ELTE Comparative Ethology Research Group, Budapest, Hungary
                [2 ]Department of Agri-Environmental Management, Szent István University. Gödöllő, Hungary
                [3 ]Department of Ethology, Eötvös Loránd University, Budapest, Hungary
                Tulane University Medical School, United States of America
                Author notes

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

                Conceived and designed the experiments: MG SS TF KM ÁM. Performed the experiments: MG SS KM. Analyzed the data: MG SS TF KM. Wrote the paper: MG SS TF KM ÁM.

                Article
                PONE-D-12-33091
                10.1371/journal.pone.0058475
                3587610
                23469283
                677d541b-d88f-4305-bf0b-8ab3c088f574
                Copyright @ 2013

                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
                : 24 October 2012
                : 5 February 2013
                Page count
                Pages: 9
                Funding
                The Hungarian Science Foundation (OTKA TO43763), and the Hungarian Academy of Sciences (F01/031) supported this work. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Animal Management
                Animal Behavior
                Biology
                Evolutionary Biology
                Animal Behavior
                Zoology
                Animal Behavior
                Medicine
                Mental Health
                Psychology
                Psychological Stress
                Social and Behavioral Sciences
                Psychology
                Behavior
                Psychological Stress
                Veterinary Science
                Animal Management
                Animal Behavior

                Uncategorized
                Uncategorized

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