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We have previously shown that dog–owner interaction results in increasing oxytocin levels in owners and dogs, decreasing cortisol levels in owners but increasing cortisol levels in dogs. The present study aimed to further investigate whether oxytocin and cortisol levels in the previously tested owners and dogs were associated with their behaviors during the interaction experiment. Ten female volunteer dog–owners and their male Labrador dogs participated in a 60 min interaction experiment with interaction taking place during 0–3 min and blood samples for analysis of oxytocin and cortisol were collected at 0, 1, 3, 5, 15, 30, and 60 min. The entire experiment was videotaped and the following variables were noted; the different types (stroking, scratching, patting and activating touch, i.e., scratching and patting combined) as well as the frequency of touch applied by the owner, the number of times the owner touched her dog, the dog’s positions and time spent in each position. Correlations were analyzed between the behavioral variables and basal oxytocin levels, maximum oxytocin levels, delta oxytocin levels, basal cortisol levels and cortisol levels at 15 min. Owners with low oxytocin levels before and during the interaction touched their dogs more frequently (0 min:
In some human societies dogs have become a central part to family life and can even be considered as family members (
The neuropeptide oxytocin is produced in the paraventricular and supraoptic nuclei in the hypothalamus and is known to stimulate milk ejection during breastfeeding and uterine contractions during labor (
In addition, non-noxious sensory stimulation in the context of intraspecies friendly social interaction, as for example in pair bonding, maternal behavior and attachment, is associated with activation of the oxytocinergic system (e.g.,
Studies in humans have shown that oxytocin, when applied through nasal spray, can stimulate certain aspects of social interactions, such as increase the ability to interpret tone of voice (
Also interaction between humans and dogs, which include pleasant non-noxious sensory stimulation, can induce oxytocin release in both humans and dogs and generate effects such as decreased cortisol levels and blood pressure (
We have previously shown that interaction between dog owners and their dogs results in increasing levels of oxytocin in both owners and dogs, whereas cortisol levels decrease in the owners but increase in the dogs (
The results of the present paper is based on data described in detail in previous manuscripts (see
Ten privately owned male Labrador retrievers, older than 1 year (mean age = 4.7 years;
The study was conducted in an ordinary room (∼4 by 5 m) with four chairs, a desk and a bookcase. Dogs had
The owner was sitting in a chair with her dog lying or sitting beside her before the start of the experiment. At time-point zero the owner approached her dog and started to interact with him by talking to the dog and by touching different parts of the dog’s body for 3 min. The owner was instructed to interact with her dog in the same way as they usually do at home. After the 3 min of interaction the owner was instructed not to touch or talk to the dog for the rest of the experiment and to remain seated in her chair. The whole experiment lasted for 60 min. However, in most cases, the owner occasionally touched and talked to her dog in order to correct his behavior during the remaining part of the experiment.
As previously described in
Thirty minutes after insertion of the catheters and immediately before the owner started to interact with her dog the first blood sample (representing basal levels) was collected. The following samples were collected at 1, 3, 5, 15, 30, and 60 min after start of interaction. All blood samples were collected by an experienced nurse and an animal caretaker, respectively. They were both present in the room during the entire experiment but were instructed to ignore the participants except during the blood sampling. When not performing blood sampling they were sitting in chairs placed in one of the corners of the room.
All blood samples were collected into EDTA tubes (4 mL) containing Trasylol® (aprotinin) (Bayer AB) and they were taken simultaneously from dog and owner. The samples were immediately put on ice, centrifuged, and the plasma was collected and stored at -20°C until analysis.
Plasma levels of oxytocin in both the dogs and the owners were determined using Correlate-EIA TM Oxytocin Enzyme Immunoassay kit (sensitivity 11.7 pg/mL, Intra Assay precision 9.1% and Inter Assay precision 14.5%) (Assay designs, Inc. Ann Arbor, MI, United States). Cortisol levels were determined using DSL-10-2000 ACTIVE Cortisol Enzyme Immunoassay kit (sensitivity 2.76 nmol/L, Intra Assay precision 10.3% and Inter Assay precision 8.0%) (Diagnostic Systems Laboratories, Inc., Webster, TX, United States). The procedures were performed according to the manufacturers’ instructions and the recommended standards and controls were always included. Extraction of blood samples prior to oxytocin analysis was not performed instead the samples were diluted five times in the assay buffer before analysis. The samples from the dogs were diluted two times in the zero standard buffer before analysis of cortisol levels.
An Anthos Fluido microplate washer (Anthos Labtec Instruments GmbH) was used for all washing procedures, a Multiskan Ex microplate photometer (Thermo Electron Corporation) was used for reading the absorbance. The color development was read at 405 nm with background correction at 580 nm for oxytocin, and at 450 nm with background correction at 620 nm for cortisol. Creation of standard curves, curve fitting, and calculation of concentrations was done by using Ascent software (Ascent software ver. 2.6 for iEMS Reader MF and multiskan).
One dog was excluded from the analysis of oxytocin levels, since oxtocin levels in all samples were below the range of detection for this dog.
The entire experiment (60 min) was videotaped and the dogs’ behaviors were analyzed from the tapes. The ethogram is presented in
Ethogram describing the behaviors observed in the present study.
| Behavior | Definition | Sampling method |
|---|---|---|
| Owner stroking | Owner strokes the dog using her palm | Continuousa |
| Owner scratching | Owner scratches the dog | Continuousa |
| Owner patting | Owner pats the dog | Continuousa |
| Owner touching | The owners’ total amount of touch (Stroking + scratching + patting) | Continuousa |
| Activating touch | The total amount of scratching and patting | Continuousa |
| Verbal rewarding | Owner reward the dog verbally (e.g., “good dog”) | Continuousa |
| Verbal reprimanding | Owner reprimands the dog verbally (e.g., “here”) | Continuousa |
| Verbal instructions | Owner give the dog verbal instructions (e.g., “sit”) | Continuousa |
| Dog sitting | Dog is sitting with front legs extended and hind legs curved | Continuousb |
| Dog standing | Dog is standing up on all four paws | Continuousb |
| Dog lying down | Dog is lying down | Continuousb |
| Dog changing position | Dog changing position (changing from sitting, lying down, and standing) | Continuousa |
The frequency of the interaction behaviors studied.
| Total touch (number of times/time period) | Stroking (number of times/time period) | Petting (number of times/time period) | Scratching (number of times/time period) | Activating touch∗ (number of times/time period) | |
|---|---|---|---|---|---|
| 0–3 min | 170 (146–206) | 84 (26–111) | 22 (5–55) | 88 (47–141) | 94 (34-150) |
| 4–60 min | 6 (1–11.5) | – | – | – | – |
Before start of the experiment, the owners were once more informed about the study. They were then given the opportunity to ask questions and were informed that they could end their participation in the study at any time. Written consent was obtained from all subjects in accordance with the Declaration of Helsinki.
The protocol was approved by the Local Ethics Board in Uppsala (ref. number. 2005/377).
This study was carried out in accordance with the recommendations of the Swedish Board of Agriculture. The protocol was approved by the Animal Ethics Committee in Uppsala (ref. number. 296-2005). The National Board of Agriculture approved the use of privately owned dogs.
The Statistical Package for the Social Sciences (SPSS, version 22.0, IBM software) was used for performing statistical calculations.
The data was not normally distributed and hence the Spearman rank coefficient was used for calculating correlations between hormone levels and behavioral data for both dogs and owners.
The included oxytocin variables for both dogs and owners were: basal oxytocin levels, maximum oxytocin levels recorded at 1, 3, or 5 min and the delta value between basal and maximum oxytocin levels, as a measure of the increase in oxytocin levels. Cortisol variables included for both dogs and owners were: basal cortisol levels and cortisol levels at 15 min.
The following behavioral variables were included in the statistical analysis: the frequency of the owners’ stroking, scratching, patting, the total number of times the owner touched her dog, the frequency of rewarding or reprimanding verbal interaction, the total number of verbal instructions given by the owner, the time the dog spent sitting, standing, or lying down and the frequency of the dogs’ position changes. In addition, the frequency of scratching and patting were combined into one new variable, “activating touch,” which was also included in the statistical analysis (
The dogs’ and the owners’ oxytocin and cortisol levels which were used in the present study have been published previously (
The owners’ and the dogs’ oxytocin and cortisol levels during the experiment (data from the 10 female owners for both oxytocin and cortisol, and from nine dogs for oxytocin and ten dogs for cortsiol).
| 0 min | 1 min | 3 min | 5 min | 15 min | 30 min | 60 min | OT max | ||
|---|---|---|---|---|---|---|---|---|---|
| Oxytocin levels (pmol/l) | Dogs | 155.8 (26.9) | 211.2 (30.7) | 236.9 (38.7) | 178.6 (29.6) | 163.5 (34.5) | 157.5 (36.0) | 157.5 (41.1) | 251.8 (34.5) |
| Owners | 168.5 (34.6) | 169.8 (34.1) | 180.6 (34.4) | 170.2 (27.8) | 146.4 (34.7) | 171.3 (34.2) | 165.1 (26.3) | 187.0 (33.6) | |
| Cortisol levels (nmol/l) | Dogs | 168.4 (14.8) | 169.4 (16.1) | 168.1 (15.3) | 180.1 (17.8) | 224.1 (32.5) | 202.8 (18.3) | 190.2 (18.8) | |
| Owners | 389.8 (119.7) | 382.7 (107.4) | 382.7 (109.9) | 387.6 (119.6) | 362.1 (107.9) | 331.6 (80.1) | 305.2 (62.6) |
None of the different types of touch affected the owners’ oxytocin levels in specific ways but there were significant negative correlations between the owners’ basal and maximum oxytocin levels and the total number of times they touched their dogs during the 3 min of interaction; that is, owners with low oxytocin levels before and during the interaction, touched their dogs more frequently (0 min:
Correlation table of hormone levels and behaviors.
| Hormone | Behavior | ||
|---|---|---|---|
| Dog oxytocin max | Frequency of stroking 0–3 min | ||
| Dog cortisol 0 min | Frequency of activating touch 0–3 min | ||
| Dog cortisol 15 min | Frequency of activating touch 0–3 min | ||
| Owner oxytocin 0 min | Frequency of total touch 0–3 min | ||
| Owner oxytocin max | Frequency of total touch 0–3 min | ||
| Owner oxytocin increase | Frequency of total touch 4–60 min | ||
| Owner cortisol 0 min | Time dog standing up 4–60 min | ||
| Owner oxytocin max | Time dog sitting down 4–60 min | ||
| Owner oxytocin max | Frequency of the dogs’ position changes | ||
| Owner oxytocin increase | Frequency of verbal reprimands |
There was a significant negative correlation between the dogs’ maximum oxytocin levels and how many times the owners stroked their dogs; that is, the lower the dogs’ oxytocin levels during the interaction, the more stroking they received (
There were no significant relationships between the frequency and type of touch initiated by the owners and their cortisol levels.
There were several significant positive correlations between the frequency of activating touch (scratching and patting) during the first 3 min of the experiment and the dogs’ cortisol levels at start of the experiment but also during the remaining part of the experiment; that is, the higher the dogs’ cortisol levels were at start of interaction the more activating touch they received and the higher their cortisol levels became (0 min:
The owners’ maximum oxytocin levels correlated negatively to the number of position changes the dog performed during the entire experiment (Rs = -0.817,
In addition, the higher the owners’ increase in oxytocin was during the interaction, the less verbal reprimands they gave the dogs during the experiment (
There was a positive correlation between the owners’ basal cortisol levels and the time the dogs spent standing up during the 4th and 60th minutes (following the interaction) of the experiment; that is, the higher the owners’ cortisol in the beginning of the experiment, the longer time the dogs were in a standing position (0 min:
Based on previous data from the experiment presented in this manuscript, we have shown that interaction between owners and their dogs results in increasing levels of oxytocin in both owners and dogs, whereas cortisol levels decrease in the owners, but increase in the dogs (
Based on these previous results, findings from other studies, and the fact that behavioral data was also recorded in our study, we were interested in investigating whether the previously obtained oxytocin and cortisol levels in the owners and the dogs were associated with their behaviors during the interaction.
The first question addressed was whether the frequency and type of touch initiated by the owner were associated with oxytocin levels in owners and dogs. The results indicate that this is true for the owners and probably also for the dogs. Owners with lower oxytocin levels touched their dogs more frequently and dogs with lower oxytocin levels received more stroking. Since we know from previous results that the oxytocin levels in the dogs and their owners are closely related (
The second question addressed was whether the frequency and types of touch initiated by the owner were associated with cortisol levels in owners and dogs. As presented previously in
In contrast, the dogs’ cortisol levels correlated positively and significantly with the amount of activating touch they received from their owners. In everyday-life interactions between dogs and owners, the activating type of touch is probably used more frequently during play. On the other hand, the stroking type of touch is probably used more frequently during calm interaction between owners and their dogs and hence it might have a more calming effect on the dogs. The activating touch applied to the dogs in this study might therefore have triggered an expectation of play in the dogs.
It is important to point out that the observed increase in the dogs’ cortisol levels does not appear to have anything to do with stress, since they did not display behaviors related to stress (looking at frequency of position changes). The increasing cortisol levels are therefore probably a reflection of positive arousal (
The third question addressed was whether the owners’ oxytocin and cortisol levels were associated with the dogs’ behavior. According to the results from the present analysis it appears as if there are associations between the owners’ oxytocin levels and the dogs displaying calm behaviors. This was demonstrated by the findings showing that the higher the owners’ maximum oxytocin level, the fewer position changes the dogs made during the experiment and the shorter time they spent in a sitting position. Together these data suggest that high oxytocin levels in the owners are associated with a friendly and calm behavior toward the dog and hence with calming effects in the dogs.
It is also possible that the owners with high cortisol displayed a more active, or even stressed, behavior which influenced the dogs, as demonstrated by the finding showing that the higher the owners’ cortisol were in the beginning of the experiment, the longer time the dogs spent in a standing position.
It appeared as if the dogs and their owners responded to the interaction in similar ways with regard to oxytocin. The interaction induced oxytocin release in the owners who displayed behaviors that are associated with anti-stress effects. The dogs seemed to sense this and responded in a similar way. The calmer behaviors displayed by the dog then enhanced the calming effect in the owners. It appears as if the owners and the dogs could mutually sense the other’s emotional state based on an increased ability to read the other’s behavioral cues. As previously described oxytocin can facilitate and stimulate friendly social interactions, induce anti-stress and anxiolytic effects and increase trust. It has been shown that oxytocin relates to the level of maternal interaction and sensitivity to the infant cues (
The results from the present and previous studies suggests that the activity and effect of the oxytocinergic system are probably part of a “mammalian heritage” that can be activated by individuals from different species, as in the interspecies relationship seen between dogs and their owners, and not only by individuals from the same species. Due to their evolutionary history (
Even though both dogs and owners responded in similar ways with regard to oxytocin some differences were noticed in the responses related to cortisol. An explanation to the mismatch in cortisol responses between the owners and the dogs might be that the interaction was driven by the owners, rather than a reciprocal, two-way decision process. The owners knew that it was going to be a calm interaction and were prepared for this and initiated the contact. The dogs on the other hand were unaware of what type of interaction that was going to take place and since the interaction was driven by the owners it might have caused some confusion for the dogs. This could explain the difference in responses between dogs and their owners.
To keep variations due to breed and gender to a minimum we chose to study male Labrador dogs and their middle-aged female owners. Labradors are friendly and easy to work with and is one of the most common types of companion dogs. However, in future studies it would be interesting to study both female and male dogs and dog owners but also other breeds.
We are aware that the number of participants in this study is low (10 dog–owner pairs) and that the results need to be interpreted with caution but still the results may serve as proof of a concept. One of the strengths of the study is the study design which included repeated sampling. This made it possible to detect the interplay between oxytocin concentrations and physical contacts. Studies with a larger number of participants and performed under even more standardized conditions need to be done to help gaining a better understanding of the responses in dogs and their owners as a consequence of interaction.
The present study showed that oxytocin and cortisol levels, in both dogs and their owners, are associated with the way the owners interact with their dogs and also with behaviors caused by the interaction.
MP: involved in study design and writing manuscript. KU-M: main applicant for funding, responsible for study design, involved in writing manuscript. AN: involved in data collection and writing manuscript. L-LG: involved in data analysis and writing manuscript. EH-S: involved in funding, study design and writing manuscript. LH: involved in study design, main responsible for data collection, statistical analysis and writing manuscript.
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 the dogs and owners who participated in the study and also Ulla Nilsson, Thomas Gustavsson, and Sara Magnusson for assisting during the experiment.