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We asked the owners about their health condition and that of their dogs before starting the experiment. Dogs with behavioral or physical problems were excluded. The experiment took place in an experimental room at Azabu University.
An experimental setting is shown in Figure 1A. To inhibit the stimulus given to dogs other than the owner, a partition was placed between the audience and the dog, and the dog could only see the owner. The dog was loosely tied with a leash and could not exit the compartment 1. The owner and the audience sat on chairs and did not walk or stand during the experiment. Figure 1. The schematic draw of the experimental setting and the time course of the experiments.
A The owner sat on the chair in front of the audience, and dog only could watch the owner in the sessions. In cases, if the dogs showing separation distress from the owner, the owner sat on the chair close to the dogs. B In the stress session, 5 min of explanation of the document to the audience, followed by 5 min arithmetic tasks were given to the owner. In the control session, the owner just read the document. The audience was not allowed to give voice communication to the owner in either session.
The schematic procedure was illustrated in Figure 1B. After informing owners with the experiment contents, the owners who signed the Informed Consent participated in the experiment. Next, the dog and owner were equipped with electrocardiogram ECG devices. Then, the dog and the owner were given 40 min of waiting time in a waiting room together. At that time, the owner was asked to fill out a questionnaire State-Trait Anxiety Inventory STAI and to rest reading books or using the smartphone, etc.
The owners filled out the STAI again after the test to evaluate the stress levels after the experiment. After the min resting period, the dog tied with a loose leash and the owner entered the experimental room. The experiment was conducted in three steps: 1 filling out the questionnaire pretest and resting time for 40 min, 2 participation in the experimental condition for 30 min, and 3 filling out the post-test questionnaire Figure 1B.
All dog—owner pairs participated both in Control and Stress conditions on different days, at least 1 week apart. The time of the experiment was fixed to avoid diurnal changes of autonomic activity, and the sequence of two conditions was pseudo-randomly controlled: half of them were given the Control condition first, and the rest were given the Stress condition first.
The standard methods were slightly modified: the original method of 10 min presentation was replaced with a 5-min period to read a document for explanation, and 5-min to explain the document. Subsequently, the participants were asked to conduct verbal mental arithmetic for 5 min. Thus, the stress session consisted of a 5-min speech preparation, 5-min oral explanation of the document, and 5-min verbal mental arithmetic in front of an audience one experimenter.
Repeat the calculation again. The owner was asked merely to read the same documents, but the owner did not need to explanation it. Regarding the control condition of arithmetic, the owners were asked to read loud the formulas and answers written on the paper. ECG measurement was conducted according to our previous report Katayama et al. The electrocardiogram induction of each dog was an M-X lead.
Ultrasound gel Aquasonic clear, Parker, United States was applied on the surface of the skin. The owner was asked to fix three electrodes along with the fifth costa.
Both ECG sampling rates were set to Hz. The ECG data for each dog and owner were recorded on the compact multifunction sensor. We excluded 20 out of 34 data from the further analysis.
The reasons for exclusion were as follows. We analyzed these data using statistical software SPSS ver. Finally, the effects of these parameters on the correlation coefficients of HRVs were examined by generalized linear model GLM. The behavior of the dogs in each condition was shown in Table 1.
Other behavior was not different between the conditions. Other STAI scores were not different between conditions. Comparisons of each HRV parameter between conditions did not show any significant difference either in dogs or owners Figure 2. Figure 2. The comparison of HRV parameters between sessions. An example of the changes of HRV parameters during the session was shown in Figure 3.
Some pairs showed similar time-dependent changes of HRV. Correlation coefficients of RRI in the stress condition tended to be higher than that of the control condition Figure 4. GLM revealed that 5 out of 6 correlation coefficients of HRV parameters were positively influenced by the duration of the ownership Table 2. In addition, daily duration of time spent with dogs also had two positive influences but one negative on the correlation coefficients of HRV parameters Table 2.
In the control condition, GLM revealed the effect of sex on correlation coefficients of all three HRV parameters; female dogs showed stronger correlation coefficients as compared to male Table 2 and Supplementary Figure S2.
Figure 3. Tentative examples of the HRV parameters changes of a dog and its owner in the sessions. The HRV parameters of the control session were on the left, and those of the stress sessions were on the right panels. The parameters of the dogs were on the first Y axis and presented in solid lines with diamond, and the parameters of the owners were on the second Y axis and presented in dotted lines with triangle.
HRV parameters were calculated in each s time bin. Figure 4. Figure 5. The duration of the ownership had a positive correlation with the correlation coefficient of RMSSD in stress condition, but not in the control condition. Table 2. In this study, we examined the emotional contagion between humans and dogs by accessing the autonomic responses. It was found that emotional contagion can be transferred from the owner to the dogs, and the efficacy of the emotional contagion was depending of the duration of the time sharing with dog and owners.
The existence of emotional contagion between human and dogs, an inter-species dyad, can contribute to the cohabitation.
Previous studies of emotional contagion between dogs and humans evaluated behavioral or hormonal changes Jones and Josephs, ; Romero et al. Therefore, there was still a concern whether the behavioral changes were results of specific emotional changes or not. For example, emotional changes such as fear can be expressed by various behaviors with large individual differences, but the autonomic fear responses were similar among individuals Ogata et al.
Second, the hormonal changes took a relatively longer time, such as minutes to hours, to occur. Instead, emotional changes were more rapid, taking such as 5 to 20 s. Therefore, the higher time-resolution and neuro-physiological measurements are needed to address the question of the existence of emotional contagions between dogs and humans. For these reasons, we focused on HRV. Measurement of HRV has some advantages. For example, HRV reflects the state of the sympathetic and parasympathetic nervous systems in a short time period Von Borell et al.
Moreover, HRV parameters are associated with emotion both in humans and animals. The present study confirmed previous studies in dogs in demonstrating an association between the HRV and emotional responses such as affiliation Romero et al.
In the present study, the analysis time window was set as 15 sec, which was suitable for accessing the autonomic changes and for accessing the correlation of HRV between humans and dogs. Our results found that some pairs of owners and dogs showed positive correlation of HRV changes in the control and stress sessions. This is the first study, as far as we know, showing correlations of a short-time window HRV between dogs and their owners.
In the stress condition, STAI State anxiety scores tended to be higher than that of the control condition. However, we could not find the effects of stress in human HRV.
This suggests that the stress experience by our modified TSST was moderate, even the protocol was the similar to previously described ones. One possible reason for this is that existence of the dog brought social buffering effects to the owners. In humans, the existence of the dog was reported to decrease stress responses, such as autonomic responses Allen et al. Although the reasons were not clear, some participants showed no change in scores of state anxiety before and after the stress session, indicating that some owners were not stressed.
Therefore, the group comparison would not suitable for the evaluation of emotional contagion due to the lack of emotional changes in some owners, and it was needed to access the individual correlation coefficients for the efficacy of the emotional contagion.
As a result, correlation coefficients, especially RRI, increased in the stress condition as compared to the control condition. This suggests that when the owners had higher negative emotions, the dogs had similar emotional changes, and it supports previous studies in which emotional contagion is well observed in negative conditions de Waal, One of the most notable findings was that the correlation coefficients of HRV were positively correlated with duration of ownership in both control and stress conditions.
In addition, daily duration of the time spent with dogs has positive influence on the correlation coefficients of HRV between dogs and owners. The present results fully support this hypothesis; the dogs and their owners, as stated above, are genetically distant, but there was emotional contagion; moreover, the sharing environment was a key factor in facilitating emotional contagion. For example, emotional contagion may help group members to escape from predators, to find food resources, and even to fight against outgroup individuals, all of which are frequently proposed merits of group living Preston and de Waal, Therefore, the present results constitute the first empirical data for supporting their theoretical model.
We have started this experiment of 34 pairs of the owner and dog. However, due to the technical, especially instability of continuous monitoring of HR, 20 pairs were excluded from the analysis.
More sophisticated methods are needed in future. Another interesting point was that, in the control condition, female dogs showed stronger correlation coefficients of HRV parameters with the owners as compared to male. Females animals, including humans, show higher capability in empathy de Waal, ; Ben-Ami Bartal et al.
The mechanisms underlying the sex differences in the capability of empathy were not discovered yet, one candidate molecule is oxytocin, which showed sex differences in response to administration in dogs Nagasawa et al.
One unsolved question concerns the mechanisms underlying the facilitating effect of sharing environments on the expression of emotional contagion between dogs and owners. Living with humans can bring many social experiences to dogs. While living together, dogs and their owners can form a bond that can facilitate the emotional contagion.
Oxytocin is a candidate molecule for explaining this possibility. Therefore, the bonding between dog and owner was facilitated by oxytocin acting on the central nervous system Young and Wang, Therefore, longer ownership would lead to a tighter bond between dogs and owners, thereby facilitating the oxytocin-mediated positive loop in the experimental context.
However, the gazing behavior directed by dogs toward their owners had negative influences to the correlation of coefficients of HRV between dogs and owners. Measuring oxytocin both in dogs and humans is needed to clarify this unsolved issue. The dog is a unique animal, which is the oldest domesticated species. Dogs have coexisted with humans for more than 35, years and are woven into human society as partners who bond with humans Skoglund et al.
Dogs have acquired human-like communication skills during the domestication process; therefore, they can understand human gestures and facial expressions and can refer to human information in their decision-making. They have come to live together with humans in a group and share the same environment.
In this context, emotional contagion can be beneficial to both dogs and humans, such as when a dog alarms the owner to the approach of a predator. Therefore, the emotional contagion found in this study can be the gift of the long cohabitation history.
The raw data supporting the conclusions of this manuscript will be made available by the authors, without undue reservation, to any qualified researcher. MK involved in all steps of the process, and was the primary conductor of the experiments. MK and MN performed the statistical analysis. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank all dogs, their owners, and laboratory members helped the experiments.
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