Despite intense research on the visual communication of domestic dogs, their cognitive capacities have not yet been explored by eye tracking. The aim of the current study was to expand knowledge on the visual cognition of dogs using contact-free eye movement tracking under conditions where social cueing and associative learning were ruled out. We examined whether dogs spontaneously look at actual objects within pictures and can differentiate between pictures according to their novelty or categorical information content. Eye movements of six domestic dogs were tracked during presentation of digital color images of human faces, dog faces, toys, and alphabetic characters. We found that dogs focused their attention on the informative regions of the images without any task-specific pre-training and their gazing behavior depended on the image category. Dogs preferred the facial images of conspecifics over other categories and fixated on a familiar image longer than on novel stimuli regardless of the category. Dogs' attraction to conspecifics over human faces and inanimate objects might reflect their natural interest, but further studies are needed to establish whether dogs possess picture object recognition. Contact-free eye movement tracking is a promising method for the broader exploration of processes underlying special socio-cognitive skills in dogs previously found in behavioral studies.
Faces play an important role in communication and identity recognition in social animals. Domestic dogs often respond to human facial cues, but their face processing is weakly understood. In this study, facial inversion effect (deficits in face processing when the image is turned upside down) and responses to personal familiarity were tested using eye movement tracking. A total of 23 pet dogs and eight kennel dogs were compared to establish the effects of life experiences on their scanning behavior. All dogs preferred conspecific faces and showed great interest in the eye area, suggesting that they perceived images representing faces. Dogs fixated at the upright faces as long as the inverted faces, but the eye area of upright faces gathered longer total duration and greater relative fixation duration than the eye area of inverted stimuli, regardless of the species (dog or human) shown in the image. Personally, familiar faces and eyes attracted more fixations than the strange ones, suggesting that dogs are likely to recognize conspecific and human faces in photographs. The results imply that face scanning in dogs is guided not only by the physical properties of images, but also by semantic factors. In conclusion, in a free-viewing task, dogs seem to target their fixations at naturally salient and familiar items. Facial images were generally more attractive for pet dogs than kennel dogs, but living environment did not affect conspecific preference or inversion and familiarity responses, suggesting that the basic mechanisms of face processing in dogs could be hardwired or might develop under limited exposure.
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.
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.
The neuropeptide oxytocin plays a critical role in social behavior and emotion regulation in mammals. The aim of this study was to explore how nasal oxytocin administration affects gazing behavior during emotional perception in domestic dogs. Looking patterns of dogs, as a measure of voluntary attention, were recorded during the viewing of human facial expression photographs. The pupil diameters of dogs were also measured as a physiological index of emotional arousal. In a placebo-controlled within-subjects experimental design, 43 dogs, after having received either oxytocin or placebo (saline) nasal spray treatment, were presented with pictures of unfamiliar male human faces displaying either a happy or an angry expression. We found that, depending on the facial expression, the dogs’ gaze patterns were affected selectively by oxytocin treatment. After receiving oxytocin, dogs fixated less often on the eye regions of angry faces and revisited (glanced back at) more often the eye regions of smiling (happy) faces than after the placebo treatment. Furthermore, following the oxytocin treatment dogs fixated and revisited the eyes of happy faces significantly more often than the eyes of angry faces. The analysis of dogs’ pupil diameters during viewing of human facial expressions indicated that oxytocin may also have a modulatory effect on dogs’ emotional arousal. While subjects’ pupil sizes were significantly larger when viewing angry faces than happy faces in the control (placebo treatment) condition, oxytocin treatment not only eliminated this effect but caused an opposite pupil response. Overall, these findings suggest that nasal oxytocin administration selectively changes the allocation of attention and emotional arousal in domestic dogs. Oxytocin has the potential to decrease vigilance toward threatening social stimuli and increase the salience of positive social stimuli thus making eye gaze of friendly human faces more salient for dogs. Our study provides further support for the role of the oxytocinergic system in the social perception abilities of domestic dogs. We propose that oxytocin modulates fundamental emotional processing in dogs through a mechanism that may facilitate communication between humans and dogs.
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.
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.
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