Abstract: Summary For humans, facial expressions are important social signals, and how we perceive specific individuals may be influenced by subtle emotional cues that they have given us in past encounters. A wide range of animal species are also capable of discriminating the emotions of others through facial expressions [1, 2, 3, 4, 5], and it is clear that remembering emotional experiences with specific individuals could have clear benefits for social bonding and aggression avoidance when these individuals are encountered again. Although there is evidence that non-human animals are capable of remembering the identity of individuals who have directly harmed them [6, 7], it is not known whether animals can form lasting memories of specific individuals simply by observing subtle emotional expressions that they exhibit on their faces. Here we conducted controlled experiments in which domestic horses were presented with a photograph of an angry or happy human face and several hours later saw the person who had given the expression in a neutral state. Short-term exposure to the facial expression was enough to generate clear differences in subsequent responses to that individual (but not to a different mismatched person), consistent with the past angry expression having been perceived negatively and the happy expression positively. Both humans were blind to the photograph that the horses had seen. Our results provide clear evidence that some non-human animals can effectively eavesdrop on the emotional state cues that humans reveal on a moment-to-moment basis, using their memory of these to guide future interactions with particular individuals.

Abstract: Recent research has shown that domestic dogs are particularly good at reading human attentional cues, often outperforming chimpanzees and hand reared wolves [1, 2]. It has been suggested that the close evolutionary relationship between humans and dogs has led to the development of this ability, however very few other species have been studied [3]. We tested the ability of 24 domestic horses to discriminate between an attentive and inattentive person when choosing whom to approach for food. While the attentive person faced forwards, the inattentive person either stood with their body turned 180° away from the subject (body orientation condition), stood with their body facing forwards but their head facing away (head orientation condition) or stood facing forwards but with their eyes closed (eyes closed condition). A fourth, mixed condition was included where the attentive person stood with their body facing away from the subjects but their head turned towards the subject while the inattentive person stood with their body facing the subject but their head turned away. Horses chose the attentive person significantly more often using the body cue (n = 24, k = 19, p = 0.003), the head cue (n = 24, k = 18, p = 0.011), and the eye cue (n = 24, k = 19, p = 0.003) but not the mixed cue (n = 24, k = 13, p = 0.42). In an additional pilot study, horses were tested in an object choice task. A human experimenter cued one of two buckets by either tapping the bucket (tap condition), orienting their body towards the bucket and pointing (body and point condition), pointing while facing forwards (point condition) or orienting their body towards the bucket (body condition). If the subjects chose the correct bucket they were rewarded. Subjects were able to use the tap cue (n = 31, k = 21, p = 0.035), body + point cue (n= 31, k = 21, p = 0.035) and the point cue (n = 30, k = 21, p = 0.021) but not the body cue (n = 31, k = 11, p = 0.076). These results taken together suggest that domestic horses are also very sensitive to human attentional cues, including gaze.
Keywords:
social cognition, animal-human interaction, horses, attention attribution, domestication
1. Hare, B., Brown, M., Williamson, C., and Tomasello, M. (2002). The domestication of social cognition in dogs. Science 298, 1634-1636.
2. Gacsi, M., Miklosi, A., Varga, O., Topal, J., and Csanyi, V. (2004). Are readers of our face readers of our minds` Dogs (Canis familiaris) show situation-dependent recognition of human’s attention. Animal Cognition 7, 144-153.
3. Hare, B., and Tomasello, M. (2005). Human-like social skills in dogs? Trends Cogn. Sci. 9, 439-444.