Nasal Oxytocin Treatment Biases Dogs' Visual Attention and Emotional Response toward Positive Human Facial Expressions

Abstract

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.

Keywords: domestic dog; emotional arousal; eye movements; facial expressions; nasal oxytocin; pupil diameter.

FIGURE 1

Examples of the stimuli images (from Radboud faces database; Langner et al., 2010) and scan paths of one dog during 7000 ms viewing after the placebo (PLB) and the oxytocin treatments (OXT). The dotted white rectangular area in the top left image represents the analyzed area of interest. Circles represent the gaze fixations of one dog and the lines trace the path that the gaze traveled across the image. Circle size is proportional to the fixation time. The numbers in the circles represent the order of the fixations.

FIGURE 2

(A) The mean number of fixations targeted to the eye regions of happy and angry faces (Lg10 transformed values). (B) The mean number of revisits targeted to the eye regions of happy and angry faces (Lg10 transformed values). (C) The mean pupil diameter (mm) during the presentation of two facial expressions (Happy and Angry) and two treatments (PLB and OXT). Error bars represent SE. Asterisks indicate significant differences (^∗∗p < 0.01, ^∗p < 0.05) and a statistical trend (^#p < 0.09).