Facial Indicators of Positive Emotions in Rats

Abstract

Until recently, research in animal welfare science has mainly focused on negative experiences like pain and suffering, often neglecting the importance of assessing and promoting positive experiences. In rodents, specific facial expressions have been found to occur in situations thought to induce negatively valenced emotional states (e.g., pain, aggression and fear), but none have yet been identified for positive states. Thus, this study aimed to investigate if facial expressions indicative of positive emotional state are exhibited in rats. Adolescent male Lister Hooded rats (Rattus norvegicus, N = 15) were individually subjected to a Positive and a mildly aversive Contrast Treatment over two consecutive days in order to induce contrasting emotional states and to detect differences in facial expression. The Positive Treatment consisted of playful manual tickling administered by the experimenter, while the Contrast Treatment consisted of exposure to a novel test room with intermittent bursts of white noise. The number of positive ultrasonic vocalisations was greater in the Positive Treatment compared to the Contrast Treatment, indicating the experience of differentially valenced states in the two treatments. The main findings were that Ear Colour became significantly pinker and Ear Angle was wider (ears more relaxed) in the Positive Treatment compared to the Contrast Treatment. All other quantitative and qualitative measures of facial expression, which included Eyeball height to width Ratio, Eyebrow height to width Ratio, Eyebrow Angle, visibility of the Nictitating Membrane, and the established Rat Grimace Scale, did not show differences between treatments. This study contributes to the exploration of positive emotional states, and thus good welfare, in rats as it identified the first facial indicators of positive emotions following a positive heterospecific play treatment. Furthermore, it provides improvements to the photography technique and image analysis for the detection of fine differences in facial expression, and also adds to the refinement of the tickling procedure.

Understanding others: Emotion recognition in humans and other animals

“…However, the visual signals conveying emotional information are scarcely explored. A small number of studies have described facial expression in mice and rats, mostly as indicators of animal welfare or reward processing . Whether these expressions are perceived as relevant cues by conspecifics has not been determined yet.…”

“…A small number of studies have described facial expression in mice and rats, mostly as indicators of animal welfare or reward processing. [203][204][205][206][207] Whether these expressions are perceived as relevant cues by conspecifics has not been determined yet. Similarly, information is poor about the perception of conspecific body postures, which in rodents are largely used to communicate states or intention during a social encounter (such as pain, pleasure, playful attitudes or dominant/submissive intentions).…”

Goats prefer positive human emotional facial expressions

“…In addition, facial expressions are also prevalent in non-human animals [4,5], and the question of whether and how animals perceive emotional facial expressions is of major interest to understand their underlying ultimate functions and phylogenetic origins [6,7]. …”

Assessing Affective State in Laboratory Rodents to Promote Animal Welfare—What Is the Progress in Applied Refinement Research?

“…While grimace scales are used frequently, other facial indicators are, in contrast to their use in farm animals, rarely used for affective state assessment in laboratory rodents. An exception is the study of Finlayson and co-authors that observed a change in ear color and ear angle in rats during positive affective states, i.e., after heterospecific play [43].…”

“…While mice do vocalize in social contexts, examples are mating songs of male mice, social vocalization of female mice, and distress calls of mice pups [41], analyses of mouse vocalization have not revealed frequencies or patterns allowing for unambiguous discrimination between positive or negative affective states. In rats, ultrasonic vocalization has been used successfully in refinement research, for example, to prove the negative effects of gradual-fill CO 2 killing in rats [42] or to set out the welfare enhancing effects of rat tickling (heterospecific play) (e.g., [43,44]). Contrary to rats, in mice, no vocalization indicative for negative affective states was detectable when different inhalants for euthanasia were tested [45].…”