Olfaction in the canine cognitive and emotional processes: From behavioral and neural viewpoints to measurement possibilities.

Domestic dogs (Canis familiaris) have excellent olfactory processing capabilities that are utilized widely in human society e.g., working with customs, police, and army; their scent detection is also used in guarding, hunting, mold-sniffing, searching for missing people or animals, and facilitating the life of the disabled. Sniffing and searching for odors is a natural, species-typical behavior and essential for the dog's welfare. While taking advantage of this canine ability widely, we understand its foundations and implications quite poorly. We can improve animal welfare by better understanding their olfactory world. In this review, we outline the olfactory processing of dogs in the nervous system, summarize the current knowledge of scent detection and differentiation; the effect of odors on the dogs' cognitive and emotional processes and the dog-human bond; and consider the methodological advancements that could be developed further to aid in our understanding of the canine world of odors.

Modulation of dog-owner relationship and dog social and cognitive behavior by owner temperament and dog breed group.

As companion dogs spend most of their lives with humans, the human-dog relationship and owner temperament may affect the dog behavior. In this study (n = 440), we investigated the relationship between the dog owner temperament (ATQ-R), owner-perceived dog-owner relationship (MDORS) and the dog behavior in three behavioral tests: the object-choice test, the unsolvable task, and the cylinder test. Dog owner temperament influenced the dog-owner relationship. Owners with high negative affectivity showed higher emotional closeness and perceived costs of their dog, whereas owners with high effortful control showed lower emotional closeness and perceived costs. Higher dog activity during the behavioral tests was also connected with owner-perceived lower emotional closeness. Furthermore, dog breed group modulated the connection between the owner temperament and dog behavior. Owner's high negative affectivity correlated with herding dogs' lower scores in the object choice test, while the behavior of primitive type dogs was unaffected by the owner temperament. Our results confirm that human characteristics are associated with the owner-reported dog-owner relationship, and owner temperament may have a modulatory effect on the dog social and cognitive behavior depending on the dog breed group, which should be investigated further.

Matters of development and experience: Evaluation of dog and human emotional expressions by children and adults.

Emotional facial expressions are an important part of across species social communication, yet the factors affecting human recognition of dog emotions have received limited attention. Here, we characterize the recognition and evaluation of dog and human emotional facial expressions by 4-and 6-year-old children and adult participants, as well as the effect of dog experience in emotion recognition. Participants rated the happiness, anger, valence, and arousal from happy, aggressive, and neutral facial images of dogs and humans. Both respondent age and experience influenced the dog emotion recognition and ratings. Aggressive dog faces were rated more often correctly by adults than 4-year-olds regardless of dog experience, whereas the 6-year-olds' and adults' performances did not differ. Happy human and dog expressions were recognized equally by all groups. Children rated aggressive dogs as more positive and lower in arousal than adults, and participants without dog experience rated aggressive dogs as more positive than those with dog experience. Children also rated aggressive dogs as more positive and lower in arousal than aggressive humans. The results confirm that recognition of dog emotions, especially aggression, increases with age, which can be related to general dog experience and brain structure maturation involved in facial emotion recognition.

Dog-Owner Relationship, Owner Interpretations and Dog Personality Are Connected with the Emotional Reactivity of Dogs.

We evaluated the effect of the dog-owner relationship on dogs' emotional reactivity, quantified with heart rate variability (HRV), behavioral changes, physical activity and dog owner interpretations. Twenty nine adult dogs encountered five different emotional situations (i.e., stroking, a feeding toy, separation from the owner, reunion with the owner, a sudden appearance of a novel object). The results showed that both negative and positive situations provoked signs of heightened arousal in dogs. During negative situations, owners' ratings about the heightened emotional arousal correlated with lower HRV, higher physical activity and more behaviors that typically index arousal and fear. The three factors of The Monash Dog-Owner Relationship Scale (MDORS) were reflected in the dogs' heart rate variability and behaviors: the Emotional Closeness factor was related to increased HRV (p = 0.009), suggesting this aspect is associated with the secure base effect, and the Shared Activities factor showed a trend toward lower HRV (p = 0.067) along with more owner-directed behaviors reflecting attachment related arousal. In contrast, the Perceived Costs factor was related to higher HRV (p = 0.009) along with less fear and less owner-directed behaviors, which may reflect the dog's more independent personality. In conclusion, dogs' emotional reactivity and the dog-owner relationship modulate each other, depending on the aspect of the relationship and dogs' individual responsivity.

Description of movement sensor dataset for dog behavior classification.

Movement sensor data from seven static and dynamic dog behaviors (sitting, standing, lying down, trotting, walking, playing, and (treat) searching i.e. sniffing) was collected from 45 middle to large sized dogs with six degree-of-freedom movement sensors attached to the collar and the harness. With 17 dogs the collection procedure was repeated. The duration of each of the seven behaviors was approximately three minutes. The order of the tasks was varied between the dogs and the two repetitions (for the 17 dogs). The behaviors were annotated post-hoc based on the video recordings made with two camcorders during the tests with one second resolution. The annotations were accurately synchronized with the raw movement sensors data. The annotated data was originally used for training behavior classification machine learning algorithms for classifying the seven behaviors. The developed signal processing and classification algorithms are provided together with the raw measurement data and reference annotations. The description and results of the original investigation that the dataset relates to are found in: P. Kumpulainen, A. Valldeoriola Cardó, S. Somppi, H. Törnqvist, H. Väätäjä, P. Majaranta, Y. Gizatdinova, C. Hoog Antink, V. Surakka, M. V. Kujala, O. Vainio, A. Vehkaoja, Dog behavior classification with movement sensors placed on the harness and the collar, Applied Animal behavior Science, 241 (2021), 105,393.

Observing animals and humans: dogs target their gaze to the biological information in natural scenes.

BACKGROUND: This study examines how dogs observe images of natural scenes containing living creatures (wild animals, dogs and humans) recorded with eye gaze tracking. Because dogs have had limited exposure to wild animals in their lives, we also consider the natural novelty of the wild animal images for the dogs. METHODS: The eye gaze of dogs was recorded while they viewed natural images containing dogs, humans, and wild animals. Three categories of images were used: naturalistic landscape images containing single humans or animals, full body images containing a single human or an animal, and full body images containing a pair of humans or animals. The gazing behavior of two dog populations, family and kennel dogs, were compared. RESULTS: As a main effect, dogs gazed at living creatures (object areas) longer than the background areas of the images; heads longer than bodies; heads longer than background areas; and bodies longer than background areas. Dogs gazed less at the object areas vs. the background in landscape images than in the other image categories. Both dog groups also gazed wild animal heads longer than human or dog heads in the images. When viewing single animal and human images, family dogs focused their gaze very prominently on the head areas, but in images containing a pair of animals or humans, they gazed more at the body than the head areas. In kennel dogs, the difference in gazing times of the head and body areas within single or paired images failed to reach significance. DISCUSSION: Dogs focused their gaze on living creatures in all image categories, also detecting them in the natural landscape images. Generally, they also gazed at the biologically informative areas of the images, such as the head, which supports the importance of the head/face area for dogs in obtaining social information. The natural novelty of the species represented in the images as well as the image category affected the gazing behavior of dogs. Furthermore, differences in the gazing strategy between family and kennel dogs was obtained, suggesting an influence of different social living environments and life experiences.

Time-resolved classification of dog brain signals reveals early processing of faces, species and emotion.

Dogs process faces and emotional expressions much like humans, but the time windows important for face processing in dogs are largely unknown. By combining our non-invasive electroencephalography (EEG) protocol on dogs with machine-learning algorithms, we show category-specific dog brain responses to pictures of human and dog facial expressions, objects, and phase-scrambled faces. We trained a support vector machine classifier with spatiotemporal EEG data to discriminate between responses to pairs of images. The classification accuracy was highest for humans or dogs vs. scrambled images, with most informative time intervals of 100-140 ms and 240-280 ms. We also detected a response sensitive to threatening dog faces at 30-40 ms; generally, responses differentiating emotional expressions were found at 130-170 ms, and differentiation of faces from objects occurred at 120-130 ms. The cortical sources underlying the highest-amplitude EEG signals were localized to the dog visual cortex.

Human Empathy, Personality and Experience Affect the Emotion Ratings of Dog and Human Facial Expressions.

Facial expressions are important for humans in communicating emotions to the conspecifics and enhancing interpersonal understanding. Many muscles producing facial expressions in humans are also found in domestic dogs, but little is known about how humans perceive dog facial expressions, and which psychological factors influence people's perceptions. Here, we asked 34 observers to rate the valence, arousal, and the six basic emotions (happiness, sadness, surprise, disgust, fear, and anger/aggressiveness) from images of human and dog faces with Pleasant, Neutral and Threatening expressions. We investigated how the subjects' personality (the Big Five Inventory), empathy (Interpersonal Reactivity Index) and experience of dog behavior affect the ratings of dog and human faces. Ratings of both species followed similar general patterns: human subjects classified dog facial expressions from pleasant to threatening very similarly to human facial expressions. Subjects with higher emotional empathy evaluated Threatening faces of both species as more negative in valence and higher in anger/aggressiveness. More empathetic subjects also rated the happiness of Pleasant humans but not dogs higher, and they were quicker in their valence judgments of Pleasant human, Threatening human and Threatening dog faces. Experience with dogs correlated positively with ratings of Pleasant and Neutral dog faces. Personality also had a minor effect on the ratings of Pleasant and Neutral faces in both species. The results imply that humans perceive human and dog facial expression in a similar manner, and the perception of both species is influenced by psychological factors of the evaluators. Especially empathy affects both the speed and intensity of rating dogs' emotional facial expressions.

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

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.

Comparison of dogs and humans in visual scanning of social interaction.

Previous studies have demonstrated similarities in gazing behaviour of dogs and humans, but comparisons under similar conditions are rare, and little is known about dogs' visual attention to social scenes. Here, we recorded the eye gaze of dogs while they viewed images containing two humans or dogs either interacting socially or facing away: the results were compared with equivalent data measured from humans. Furthermore, we compared the gazing behaviour of two dog and two human populations with different social experiences: family and kennel dogs; dog experts and non-experts. Dogs' gazing behaviour was similar to humans: both species gazed longer at the actors in social interaction than in non-social images. However, humans gazed longer at the actors in dog than human social interaction images, whereas dogs gazed longer at the actors in human than dog social interaction images. Both species also made more saccades between actors in images representing non-conspecifics, which could indicate that processing social interaction of non-conspecifics may be more demanding. Dog experts and non-experts viewed the images very similarly. Kennel dogs viewed images less than family dogs, but otherwise their gazing behaviour did not differ, indicating that the basic processing of social stimuli remains similar regardless of social experiences.

Empathic veterinarians score cattle pain higher.

The treatment of cattle pain often relies upon veterinarians. The aim of this study was to qualify the influence of veterinarians skills, attitudes, and empathy on cattle pain assesment and consequently disbudding pain management. A web-based questionnaire was sent to Finnish veterinary students in either the preclinical or clinical stage, and also to production-animal practice oriented veterinarians. The questionnaire recorded demographics, statements of opinions, pain scoring of cattle conditions and procedures. Empathy towards humans (Interpersonal Reactivity Index, IRI) and reworded IRI to measure empathy towards animals were also covered. The overall response rate was approximately 40%. The association between pain and empathy scores were analyzed by Pearsons correlation, and the factors affecting pain scores and empathy towards animals analyzed using linear models. The need for pain medication of calves during disbudding was well recognized and the intention to treat such pain was very common. Higher mean scores for cattle pain were associated with greater empathy towards humans. On average, respondents' empathy towards animals was greater than towards humans, and was associated with respondents' empathy towards humans, family size and attachment to family pet.

Reactivity of dogs' brain oscillations to visual stimuli measured with non-invasive electroencephalography.

Studying cognition of domestic dogs has gone through a renaissance within the last decades. However, although the behavioral studies of dogs are beginning to be common in the field of animal cognition, the neural events underlying cognition remain unknown. Here, we employed a non-invasive electroencephalography, with adhesive electrodes attached to the top of the skin, to measure brain activity of from 8 domestic dogs (Canis familiaris) while they stayed still to observe photos of dog and human faces. Spontaneous oscillatory activity of the dogs, peaking in the sensors over the parieto-occipital cortex, was suppressed statistically significantly during visual task compared with resting activity at the frequency of 15-30 Hz. Moreover, a stimulus-induced low-frequency (~2-6 Hz) suppression locked to the stimulus onset was evident at the frontal sensors, possibly reflecting a motor rhythm guiding the exploratory eye movements. The results suggest task-related reactivity of the macroscopic oscillatory activity in the dog brain. To our knowledge, the study is the first to reveal non-invasively measured reactivity of brain electrophysiological oscillations in healthy dogs, and it has been based purely on positive operant conditional training, without the need for movement restriction or medication.

Visual event-related potentials of dogs: a non-invasive electroencephalography study.

Previously, social and cognitive abilities of dogs have been studied within behavioral experiments, but the neural processing underlying the cognitive events remains to be clarified. Here, we employed completely non-invasive scalp-electroencephalography in studying the neural correlates of the visual cognition of dogs. We measured visual event-related potentials (ERPs) of eight dogs while they observed images of dog and human faces presented on a computer screen. The dogs were trained to lie still with positive operant conditioning, and they were neither mechanically restrained nor sedated during the measurements. The ERPs corresponding to early visual processing of dogs were detectable at 75-100 ms from the stimulus onset in individual dogs, and the group-level data of the 8 dogs differed significantly from zero bilaterally at around 75 ms at the most posterior sensors. Additionally, we detected differences between the responses to human and dog faces in the posterior sensors at 75-100 ms and in the anterior sensors at 350-400 ms. To our knowledge, this is the first illustration of completely non-invasively measured visual brain responses both in individual dogs and within a group-level study, using ecologically valid visual stimuli. The results of the present study validate the feasibility of non-invasive ERP measurements in studies with dogs, and the study is expected to pave the way for further neurocognitive studies in dogs.

Dog experts' brains distinguish socially relevant body postures similarly in dogs and humans.

We read conspecifics' social cues effortlessly, but little is known about our abilities to understand social gestures of other species. To investigate the neural underpinnings of such skills, we used functional magnetic resonance imaging to study the brain activity of experts and non-experts of dog behavior while they observed humans or dogs either interacting with, or facing away from a conspecific. The posterior superior temporal sulcus (pSTS) of both subject groups dissociated humans facing toward each other from humans facing away, and in dog experts, a distinction also occurred for dogs facing toward vs. away in a bilateral area extending from the pSTS to the inferior temporo-occipital cortex: the dissociation of dog behavior was significantly stronger in expert than control group. Furthermore, the control group had stronger pSTS responses to humans than dogs facing toward a conspecific, whereas in dog experts, the responses were of similar magnitude. These findings suggest that dog experts' brains distinguish socially relevant body postures similarly in dogs and humans.

Engagement of amygdala in third-person view of face-to-face interaction.

Humans often watch interactions between other people without taking part in the interaction themselves. Strikingly little is, however, known about how gestures and expressions of two interacting humans are processed in the observer's brain, since the study of social cues has mostly focused on the perception of solitary humans. To investigate the neural underpinnings of the third-person view of social interaction, we studied brain activations of subjects who observed two humans either facing toward or away from each other. Activations within the amygdala, posterior superior temporal sulcus (pSTS), and dorsomedial prefrontal cortex (dmPFC) were sensitive to the interactional position of the observed people and distinguished humans facing toward from humans facing away. The amygdala was most sensitive to face-to-face interaction and did not differentiate the humans facing away from the pixelated control figures, whereas the pSTS dissociated both human stimuli from the pixel figures. The results of the amygdala reactivity suggest that, in addition to regulating interpersonal distance towards oneself, the amygdala is involved in the assessment of the proximity between two other persons.

Facial expressions of pain modulate observer's long-latency responses in superior temporal sulcus.

The strength of brain responses to others' pain has been shown to depend on the intensity of the observed pain. To investigate the temporal profile of such modulation, we recorded neuromagnetic brain responses of healthy subjects to facial expressions of pain. The subjects observed grayscale photos of the faces of genuine chronic pain patients when the patients were suffering from their ordinary pain (Chronic) and when the patients' pain was transiently intensified (Provoked). The cortical activation sequence during observation of the facial expressions of pain advanced from occipital to temporo-occipital areas, and it differed between Provoked and Chronic pain expressions in the right middle superior temporal sulcus (STS) at 300-500 ms: the responses were about a third stronger for Provoked than Chronic pain faces. Furthermore, the responses to Provoked pain faces were about 40% stronger in the right than the left STS, and they decreased from the first to the second measurement session by one-fourth, whereas no similar decrease in responses was found for Chronic pain faces. Thus, the STS responses to the pain expressions were modulated by the intensity of the observed pain and by stimulus repetition; the location and latency of the responses suggest close similarities between processing of pain and other affective facial expressions.

Brain basis of human social interaction: from concepts to brain imaging.

Modern neuroimaging provides a common platform for neuroscience and related disciplines to explore the human brain, mind, and behavior. We base our review on the social shaping of the human mind and discuss various aspects of brain function related to social interaction. Despite private mental contents, people can share their understanding of the world using, beyond verbal communication, nonverbal cues such as gestures, facial expressions, and postures. The understanding of nonverbal messages is supported by the brain's mirroring systems that are shaped by individual experience. Within the organism-environment system, tight links exist between action and perception, both within an individual and between several individuals. Therefore, any comprehensive brain imaging study of the neuronal basis of social cognition requires appreciation of the situated and embodied nature of human cognition, motivating simultaneous monitoring of brain and bodily functions within a socially relevant environment. Because single-person studies alone cannot unravel the dynamic aspects of interpersonal interactions, it seems both necessary and beneficial to move towards "two-person neuroscience"; technological shortcomings and a limited conceptual framework have so far hampered such a leap. We conclude by discussing some major disorders of social interaction.