The role of cat eye narrowing movements in cat–human communication

IntroductionFor companion animals, humans act as key social partners, with these species often spending more time with humans than conspecifics1. The ability to engage in interspecific communication, not only by reading human-given cues but also by producing signals directed at humans, would have obvious adaptive advantages for domestic species, allowing the exchange of important social information. A number of domestic animals have been shown to use human-given cues to derive contextual information and perform tasks. Dogs are highly skilled in reading human gestural cues to locate hidden food2,3, and can differentiate between the attentive states of handlers when making choices4,5,6. More recent studies have revealed that dogs can also gain information through the use of human cues to emotion7,8,9,10. Horses, pigs and goats also all perform successfully in following certain human-given cues in object choice tasks11,12,13, and horses and goats can discriminate between different human emotions14,15,16, adjusting their behaviour in functionally relevant ways (in horses17). Interspecific communication is not one sided either—some domestic animals can also direct communicative behaviour towards humans. Human-directed gazing behaviour has been suggested to be a form of referential and intentional communication18,19 and is seen in dogs as young as 2 months old20, as well as in other domestic species, such as horses21 and goats22.It is notable that the socio-communicative abilities of another key species in the human household, the domestic cat (Felis Catus), have been relatively understudied—perhaps because of the cat’s solitary ancestry23. However, research assessing human-directed gazing by cats in a social referencing paradigm found that most cats do look to their owners when faced with an ambiguous situation24. In addition, domestic cats have been shown to perform equally as well as dogs in object choice tasks using human pointing25, and only slightly worse than dogs in tasks that require human-directed attention-getting to obtain food23. Cats have also been shown to attract and manipulate human attention effectively in the auditory modality, through solicitation purring26, as well as discriminate their name from other words, even when unfamiliar humans are calling27. There is evidence that they also display specific facial actions during negative emotional contexts with humans compared to the same emotional contexts without human interaction28,29. Furthermore, there is circumstantial evidence that cats may be sensitive to human emotional cues, displaying more allo-rubbing (a communicative signal of affiliation in cats30) toward owners in a depressed mood31. Cats also alter their behaviour in different ways, depending on the valence of the emotional cues presented by a familiar human32. These findings collectively suggest that the cat may be an interesting model for further investigation of inter-specific communication, particularly in the context of emotional communication with humans. This line of study has particular relevance for enhancing the cat–human bond and feline welfare.One common anecdotally acknowledged yet subtle behavioural display that cats appear to direct at humans is the slow blink sequence (see also33). Slow blink sequences involve a series of half-blinks (where the eyelids move towards each other without ever fully closing the eye34) followed by either prolonged narrowing of the eye aperture or a full eye closure (see Fig. 1). Anecdotal evidence and personal observations suggest that the slow blink sequence can be used as a method of cat–owner communication, and is said to occur in calm, positive contexts35,36. Interestingly, narrowing of the eyes, the main characteristic of the slow blink sequence, also features in the positive emotional displays of some other species, including the play and consummatory faces of canids37, in horses and cows during stroking38,39,40 and the human Duchenne smile41, and might therefore be a positive emotional indicator in cats.Figure 1The cat slow blink sequence, starting from a neutral face moving to a half blink, then towards eye closure and then eye narrowing expression.We performed two experiments with the aim of exploring the communicatory significance of slow blink behaviour in human-cat interactions. We first examined whether cats respond to human-initiated slow blink stimuli with slow blink sequences of their own (Experiment 1). We then investigated whether cats were more likely to approach an unknown experimenter after a slow blink interaction (Experiment 2). Across the experiments, the slow blink sequence was compared with two controls: no human interaction, and a neutral face.Materials and methodsExperiment 1SubjectsA total of 21 cats from 14 different households were included. Fourteen different owners participated in this experiment. Ten of the cats were male and 11 of the cats were female, cat age ranging from an estimated 0.45–16 years (M = 7.05, S.D. = 4.59). All cats were housed indoors with outdoor access and had been living with their owners for a minimum of 3 months. Due to the nature of the study, partially blind/visually impaired cats or cats with medical issues involving the eyes were not included. All subjects were filmed during the slow blink stimulus, and this was counter-balanced with the no human interaction condition. Three dyads were outliers and excluded from subsequent analyses (> 2 standard deviations from the mean), thus the final analyses included 18 cat–human dyads.ProcedureCats were individually tested in a familiar room within their home. The home environment is more comfortable for the cats than laboratory based contexts, increasing the ecologically validity of the testing conditions. The experimenters (RS and TH) demonstrated the slow blink action, an eye closure (lasting more than 0.5 s), and gave advice verbally on how to perform the facial actions associated with slow blinking. Additional exerts from the FACS manual were provided if owners required more detailed descriptions of related movements (see Supplementary Note). The experimenter also gave verbal instructions on the intensity of these actions and then asked the owner to produce the slow blink movements to check that the cue was appropriate, giving corrections if necessary. The cat was present at all times throughout the experiment. Once the cat had settled down in one place, the experimenter asked the owner to either sit approximately 1 m in front of their cat or not to interact with their cat for the duration of the trial, depending on the condition. A Sony DSC-HX9V video camera was positioned 1.0–1.5 m in front of the owner to record their facial expressions, and a second Canon G9 video camera was placed the same distance in front of the cat. The experimenter was situated behind the video camera that recorded the cat’s facial expressions.Paired slow blink stimulus and no human interaction conditions were counterbalanced across cats, with each cat being presented with each condition once. Before delivering each slow blink stimulus, owners were asked to ensure the cats were attentive and if they were not, to gain their cat’s attention. Once the cat gave direct eye contact, owners performed the slow blink action. Owners were asked to repeat this procedure until the experimenter indicated the end of the trial. Trials varied slightly in length due to the cat’s motivation to participate in the interaction but were 2 min maximum or ended when the cat walked away. On average trials lasted 62.75 s (s.e.m = 8.71; range: 19.14–120) long and the average owner’s stimulus delivery was at a rate of 14.58 (s.e.m = 0.03; range: 3–30.6) slow blink stimulus eye movements per minute. During the no human interaction condition, the owner remained in the room with the cat, but did not sit in front of or interact with the cat—owners were free to speak to the experimenter at this time. Mean trial length for the no human interaction control condition was 59.86 s (s.e.m = 8.50; range: 21.03–120).Behavioural codingCat’s eye movements were coded using actions defined in CatFACS, an anatomically based system designed to objectively measure facial actions based on their underlying muscle movements34. One additional code (not specifically accounted for in CatFACS), ‘eye narrowing’, was included in the current study to take into account situations where the eye aperture was held partially closed for at least 2 frames (0.08 s) rather than returning to the neutral eyelid position in a continuous movement, as in the half blink (see Table 1). The eye narrowing and eye closure movements of the owner were also coded. Eye movements of both cats and humans were coded by one researcher (TH), who had been present in only a proportion of the original trials and was blind to the conditions for the cats’ eye movements; human facial expressions could not be coded blind, as the condition was obvious from the owner’s facial expression. A second independent coder analysed a random 25% of the videos. The independent coder was familiar with the research aims and was completely blind to condition (and had not been present during any of the trials). Both researchers were certified CatFACS coders and the inter-observer reliability on coding the presence of all cats’ and owners’ eye movements yielded a Cronbach’s alpha of 0.9, which is deemed a good level of inter-observer reliability. Figure 1 shows the cat slow blink sequence taken from video frames of one of the subjects; video available as Supplementary Video.Table 1 Cat and human eye movements and corresponding FACS action units.Full size tableStatistical analysisDue to trials varying in length, the rate of each cat’s individual eye movements (half-blink, blink, eye closure and eye narrowing) was calculated by dividing the total number of a particular eye movement by the total length of the trial in seconds. The resulting rates of the individual cat eye