New approaches to quantify social development in rhesus macaques (Macaca mulatta): Integrating eye tracking with traditional assessments of social behavior.

The nonhuman primate provides a sophisticated animal model system both to explore neurobiological mechanisms underlying complex behaviors and to facilitate preclinical research for neurodevelopmental and neuropsychiatric disease. A better understanding of evolutionarily conserved behaviors and brain processes between humans and nonhuman primates will be needed to successfully apply recently released NIMH guidelines (NOT-MH-19-053) for conducting rigorous nonhuman primate neurobehavioral research. Here, we explore the relationship between two measures of social behavior that can be used in both humans and nonhuman primates-traditional observations of social interactions with conspecifics and eye gaze detection in response to social stimuli. Infant male rhesus macaques (Macaca mulatta) serving as controls (N = 14) for an ongoing study were observed in their social rearing groups and participated in a noninvasive, longitudinal eye-tracking study. We found significant positive relationships between time spent viewing eyes of faces in an eye tracker and number of initiations made for social interactions with peers that is consistent with similar observations in human populations. Although future studies are needed to determine if this relationship represents species-typical social developmental processes, these preliminary results provide a novel framework to explore the relationship between social interactions and social attention in nonhuman primate models for neurobehavioral development.

Saccadic oscillations in 4 dogs and 1 cat.

Disorders affecting the control of saccadic eye movements result in involuntary saccadic oscillations and are widely reported in human medicine. Information regarding the occurrence and potential importance of saccadic oscillations in veterinary medicine is currently limited. The clinical histories of three dogs and one cat displaying involuntary eye movements consistent with opsoclonus are presented, with final diagnoses including idiopathic generalized tremor syndrome and neuronal ceroid lipofuscinosis (NCL). A dog with eye movements closely resembling macrosaccadic oscillations is also presented, for which a final diagnosis of NCL was made. All animals had clinical signs of cerebellar disease. As in human medicine, recognition of these forms of involuntary eye movement might suggest a cerebellar neuroanatomic localization. Opsoclonus and macrosaccadic oscillations are forms of involuntary saccadic eye movement that are both unrecognized and under-reported in veterinary medicine.

How dogs scan familiar and inverted faces: an eye movement study.

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.

Dogs do look at images: eye tracking in canine cognition research.

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.

Eye-tracking with nonhuman primates is now more accessible than ever before.

Human and nonhuman primates rely almost exclusively on vision for social communication. Therefore, tracking eye movements and examining visual scan paths can provide a wealth of information about many aspects of primate social information processing. Although eye-tracking techniques have been utilized with humans for some time, similar studies in nonhuman primates have been less frequent over recent decades. This has largely been owing to the need for invasive manipulations, such as the surgical implantation of devices to limit head movement, which may not be possible in some laboratories or at some universities, or may not be congruent with some experimental aims (i.e., longitudinal studies). It is important for all nonhuman primate researchers interested in visual information processing or operant behavior to realize that such invasive procedures are no longer necessary. Here, we briefly describe new methods for fully noninvasive video eye-tracking with adult rhesus monkeys (Macaca mulatta). We also describe training protocols that require only ∼30 days to accomplish and quality control measures that promote reliable data collection. It is our hope that this brief overview will reacquaint nonhuman primate researchers with the benefits of eye-tracking and promote expanded use of this powerful methodology.