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Comparative studies of human–dog cognition have grown exponentially since the 2000’s, but the focus on how dogs look at us (as well as other dogs) as social partners is a more recent phenomenon despite its importance to human–dog interactions. Here, we briefly summarise the current state of research in visual perception of emotion cues in dogs and why this area is important; we then critically review its most commonly used methods, by discussing conceptual and methodological chal- lenges and associated limitations in depth; finally, we suggest some possible solutions and recommend best practice for future research. Typically, most studies in this field have concentrated on facial emotional cues, with full body information rarely considered. There are many challenges in the way studies are conceptually designed (e.g., use of non-naturalistic stimuli) and the way researchers incorporate biases (e.g., anthropomorphism) into experimental designs, which may lead to problematic conclusions. However, technological and scientific advances offer the opportunity to gather much more valid, objective, and systematic data in this rapidly expanding field of study. Solving conceptual and methodological challenges in the field of emotion perception research in dogs will not only be beneficial in improving research in dog–human interactions, but also within the comparative psychology area, in which dogs are an important model species to study evolutionary processes. Keywords Emotion cues · Visual perception · Facial expressions · Bodily expressions · Human–dog relationship · Methodology Introduction followed by a thread of invited commentaries, explored the questions of if and how dogs may experience emotion, but Several reviews have been published recently on dog cogni- no review has so far focused on the issue of perception of tion (Arden et al. 2016; Bensky et al. 2013; Kubinyi et al. emotion cues, and more importantly on the methodologies 2007; Lea and Osthaus 2018; Miklósi and Kubinyi 2016; used to study this topic. An increase in studies (Fig. 1) has Wynne 2016), visual abilities (Barber et al. 2020; Byosiere been changing the status of the domestic dog in biological et al. 2018; Miller and Murphy 1995), and dog–human com- research, from inadequate/irrelevant for “real biology” due munication (Siniscalchi et al. 2018a, b), including atten- to its domestication, to an ideal model species (Cooper et al. tion to pointing gestures (Kaminski and Nitzschner 2013) 2003; Miklosi 2014; Topal et al. 2009) for understanding a and faces (Huber 2016). Another review (Kujala 2017), range of phenomena, from explanations of their uniqueness (Miklosi 2014; Prato-Previde and Marshall-Pescini 2014) to the evolution of communication and emotion in humans and * Catia Correia-Caeiro non-human animals (Andics et al. 2014; Gruber and Bekoff email@example.com 2017; Hare 2007). Given this increased scientific interest in School of Psychology, University of Lincoln, Brayford Pool, this field, an early critical appraisal of concepts and meth- Lincoln LN6 7TS, UK odologies is timely for future research. Department of Life Sciences, University of Lincoln, Here, we have used a critical review methodology (Grant Lincoln LN6 7DL, UK and Booth 2009) to briefly summarise the most salient pub - Primate Research Institute, Kyoto University, lications in this area, and to critically evaluate concepts and Inuyama 484-8506, Japan methodologies commonly applied, as well as what can be Center for the Evolutionary Origins of Human Behavior, learned from them. We structured this critique to cover the Kyoto University, Inuyama 484-8506, Japan Vol.:(0123456789) 1 3 Animal Cognition emotion and cognition in dogs. We do not however address other topics such as the philosophical debate concerning what an emotion is nor other perceptual modalities, but we briefly summarise in the next section and in the Supple- mentary Text S1 the wider debate of emotion nature and function, and justify our focus on visual cues, respectively. We also do not intend to extensively review the evolutionary processes of dogs as a domestic species nor what is known about dogs' perception of emotion, but we give a brief sum- mary of both topics in Sects. “Why is the dog a good model for research on the perception of emotion cues?” and “What is known about how dogs visually perceive emotion cues?” for a better understanding of the methodological critique. We conclude this review by briefly describing the method- ologies used in this area and discussing its limitations and future considerations in Sects. “What methodologies have been used to assess the perception of emotion cues in dogs?” – “What are the limitations and challenges to investigate the perception of emotion cues in dogs?”, respectively. Fig. 1 Comparison of articles published until 2000 and from 2001 till A brief summary of the nature of emotion 2020 available on GoogleScholar, searched using the keywords “dog and its perceptual processes cognition”, “dog perception”, or “dog emotion”. The same search using the terms “cat cognition”, “cat perception”, or “cat emotion” was used for comparison purposes in the same periods. The explo- Emotion processes are thought to have evolved to allow sion of studies in these areas is particularly evident since the turn of individuals to avoid harm/punishment and seek valuable the millennium for dogs: up to the year 2000, GoogleScholar dis- resources/rewards (Dawkins 2000; Duncan 2006; Paul et al. plays only 10 results when searching, for example, for “dog cogni- 2005; Rolls 2005). Emotions have been defined as short- tion”, but in the next 20 years period (2001–2020) 720 results appear; “dog perception” returns 47 results pre-2000 and 170 studies since, lived internal states occurring in response to external or while “dog emotion” returns 7 results pre-2000 and 86 results since. internal stimuli that are perceived to have a specific value This represents a 72, 3.6, and 12.2 times increase for these research to the individual (emotionally-competent stimuli), and pro- topics in dogs, respectively compared with only 3.4, 1.2, and tenfold duce both internal and external changes, including cognitive increase for cats appraisal, physiological activation, motor expression and behavioural tendency (Scherer 2005). For example, if an following key questions in studying the perception of emo- aversive stimulus is identified, an array of internal responses tion cues in dogs: (e.g., amygdala activation and release of CRF, Adolphs 2013; Panksepp 2011; increase in heart rate, LeDoux 2003; 1) What is the nature of emotion and its perceptual pro- Thayer and Lane 2009) is usually accompanied by certain cesses? behavioural tendencies (e.g., flight) and expressive/commu- 2) Why is the dog a good model species? nicative components (e.g., fearful face, Chevalier-Skolnikoff 3) What is known about the perception of emotion cues in 1973; Darwin 1896; Leopold and Rhodes 2010). The exter- dogs? nal responses (i.e., emotion cues) are particularly important 4) What methodologies have been used to study the percep- in social interactions, as they can be perceived and processed tion of emotion cues in dogs? by other individuals present in the same environment (i.e., 5) What are the limitations and challenges of studying the receivers). Even if signals evolve for the benefit of the send- perception of emotion cues in dogs? ers and not the receivers, receivers still have the potential to 6) What are the scientific and practical considerations use these as cues (i.e., any stimulus that an individual can regarding the methodologies currently used when study- detect and learn to use: Saleh et al. 2007) as valuable infor- ing the perception of emotion cues in dogs? mation to improve navigation of their social and physical environment (e.g., a fearful face in the sender might indi- Given that the perception of emotion cues is central to cate an environmental danger). Hence, perception of emo- understanding social interactions in individuals, this review tion cues is critical for survival and increases fitness, but it fills an important knowledge gap in the wider fields of is not a simple or straightforward task to accomplish due to 1 3 Animal Cognition differences in how emotions are activated and cues produced cues such as facial expressions can probably function both by the senders. These differences create a population of emo- as emotional expressive or communicative cues. One of the tionally distinct individuals, who may not produce similar classical examples in humans of this multi-function of facial emotion cues in terms of type or intensity to certain stimuli expressions is probably the “smile” with its wide range of (Anderson and Adolphs 2014). For example, more fearful meanings and functions (Ekman and Friesen 1982), includ- individuals might produce cues related to flight (e.g., fearful ing for example the “felt” or Duchenne smile, which is a facial expressions), freeze (e.g., absence of response or neu- correlate of a positive internal state, or the “Pan-Am” smile tral face) or fight (e.g., angry facial expression) situations, (named due to its normative display by air crew greeting which subsequently can have different outcomes impacting passengers) that is displayed as a greeting signal (uncorre- fitness and survival of both the sender and the receiver. lated to internal states). We support this more nuanced and Whilst emotions are internal states and arise from multi- complex view of emotions and emotion cues (encompassing component complex biological and perceptual processes BET and BECV), in which emotions are biologically well (and thus are subjective and hard to measure as a single defined, but its measurable outputs can be both biological concept), emotion cues are variably present on a sender, may (e.g., facial expressions acting as emotion cues) or socially be observable by a receiver, and belong to distinct modali- and evolutionary shaped (e.g., facial expressions acting as ties (and thus can be objectively quantified). Emotion cues communication signals). are one of the ways of communicating between individuals In any case, indubitably, investigating the perception (and which have not evolved to function as a signal (for distinc- by extension, production) of emotion cues in dogs may not tion between cue and signal, see Freeberg et al. 2021). How- only add to this debate by providing an evolutionary (e.g., ever, although we use the term “emotion cues” as described which emotional processes are shared with humans and how/ above, these cues do not contain emotion per se, i.e., facial why they might have evolved?) and comparative perspec- expressions, body postures, vocalisations, etc., are not inher- tive (e.g., what each species makes of emotion cues, are ently an emotion and can be used independently from a par- these emotion cues homologous or analogous in dogs?), but ticular emotion state. For example, in humans, a smile may it might actually bypass a lot of the requirement issues (e.g., be displayed when the individual is in a positive state or language, consciousness) that at the moment entangle the when the individual is simply greeting someone (see below debates in emotion perception, production and experience. for more on the multiple functions of facial expressions). Importantly, in this review we focus exclusively on The biologically-based definition of emotion displays we what is known so far on how dogs are able to extract visual use here is thus in line with the Basic Emotion Theory (BET, information from their environment (social and non-social) reviewed for example in Tracy and Randles 2011), in which through their specialised visual system (e.g., Barber et al. it is agreed by different researchers that an internal state fits 2020; Byosiere et al. 2018), and perceive emotion cues intra- the criteria for basic emotion if (1) it is discrete, (2) presents and inter-specifically. Therefore, this review does not aim fixed neural (subcortical) and behavioural correlates (i.e., at (1) discussing theories of emotions, as this necessarily the emotion cues), (3) has a fixed feeling or motivational would include a much more extensive and broad work on response, and importantly, (4) it can be generalised across experience of emotion as internal states, production of emo- species (but not necessarily). Nonetheless, we recognise that tion and/or social cues, intentionality, flexibility, control over there are opposing theories of emotion cues production, in displays, etc.; (2) discussing the exclusivity of proximate particular regarding facial displays (e.g., Behavioral Ecology (emotional) or ultimate (communicative) mechanisms of View: BECV proposes facial expressions to be disassoci- visual cues (for this, see for e.g., Waller et al. 2017); (3) ated from internal states, lacking fixed appearance changes reviewing human nor dog emotion-related experiences (e.g., or meanings, and instead act as “social tools”: Crivelli and feelings, moods, sensations) per se; (4) speculating on the Fridlund 2018), with growing debates on definitions and/or meaning of cues as signals, as no study has yet empirically functions of both emotions and emotion cues (Barrett 2006; tested for this in dogs (e.g., by examining both sender and Crivelli and Fridlund 2019; Damasio 2003; Izard 2007; receiver simultaneously). Jack et al. 2012a, b; Jack et al. 2014; Jack and Schyns 2015; Keltner et al. 2019; LeDoux 2015; Seyfarth and Cheney 2003), as well as questions on the universality of emotion Why is the dog a good model for research cues (Chen and Jack 2017; Cowen et al. 2021; Cowen and on the perception of emotion cues? Keltner 2017; Russell 1994; Volynets et al. 2020), or even its existence beyond a social construct (Barrett 2016). Nonethe- Despite being a species with a tremendous sense of smell, less, these opposing views are not mutually exclusive, and dogs seem to have a well-developed visual system (Barber they can be combined into a more nuanced view (Camerlink et al. 2020; Byosiere et al. 2018) and a remarkable abil- et al. 2018; Waller and Micheletta 2013), in which visual ity to visually read humans’ communication, emotions, 1 3 Animal Cognition and intentions (Arden et al. 2016; Huber 2016; Lea and some extent to create convergence in cognitive skills ((Hare Osthaus 2018; Reid 2009). The recent wealth of studies 2007; Hare and Ferrans 2021; Hare and Tomasello 2005), on the dog (Fig. 1) reveal this species is highly sensi- but for further debate on this topic, see (Range and Marshall- tive to visual social cues, particularly when it comes to Pescini 2022; Udell et al. 2010; Udell and Wynne 2008)). human–dog communication. For example, dogs can take The group size and complex dynamics of ancestral wolf- into account what other individuals can see (Kaminski type populations may also have provided an important et al. 2013; Savalli et al. 2013) or know (Catala et al. 2017; substrate for the evolution of the human–dog relationship. Maginnity and Grace 2014), follow human action to solve Typically, social species display complex social signals a task (Pongrácz et al. 2001), respond and adapt to human (Dobson 2009b, 2009a), which, according to the "Social behaviour (Gácsi et al. 2013; Kaminski et al. 2017), under- brain hypothesis", also requires advanced cognition to navi- stand human intentions and beliefs (Lonardo et al. 2021; gate these more demanding social environments (Dunbar Schünemann et al. 2021), and act to manipulate others' 1998; Whiten and Byrne 1988). This, coupled with the need attention (Horowitz 2009). These abilities in perspective to operate within a framework of rapid exchanges to prevent taking and attention sensitivity have been used to argue harm to either or both parties (Mills and Westgarth 2017), initially for a “rudimentary Theory of Mind” (ToM) in would favour the development of these abilities within both dogs (Horowitz 2011), and since then evidence on differ - visual and acoustic sensory channels. The extraordinary ent aspects of ToM in dogs has been growing (Lea and proficiency of dogs in being able to read emotion cues in Osthaus 2018; however, see (Wynne 2021) for an oppos- humans, might then be a key feature in their successful ing view). Researchers have also found evidence of rapid domestication and subsequent ubiquity in society in roles facial mimicry (Palagi et al. 2015), contagious yawning such as a companion, assistance and therapy animal as evi- (Joly-Mascheroni et al. 2008), pupillary (Axelsson and denced by their economic significance (Hall et al. 2016). Fawcett 2020) and emotional contagion (Palagi et al. Taken together, the known wide set of perceptual skills, 2015), and empathy-like behaviour (Custance and Mayer the co-evolutionary processes with humans, and the high 2012; Silva and Sousa 2011) in dogs. Dogs are also able sociability tendency make dogs a unique model species for to integrate cues from different modalities to extract emo- studying the perception of emotion cues at both the intra and tion information (Albuquerque et al. 2016; Faragó et al. interspecific level. 2010) and show social referencing (Merola et al. 2013, 2014; Yong and Ruffman 2013). Although not all these abilities are exclusive of dogs (e.g., wolves also show per- What is known about how dogs visually spective taking: Udell et al. 2011), and some aspects are perceive emotion cues? still being debated (e.g., contagious yawning: Harr et al. 2009; O’Hara and Reeve 2011; Yoon and Tennie 2010) When dogs are exposed to an ambiguous/threatening situa- or empathy-like behaviour (Adriaense et al. 2020), taken tion, they gaze at humans to look for information about the together, these studies indicate that social and emotion situation and react according to the emotion cues expressed cues are crucial for dogs' social interactions. by their owners (Merola et al. 2012), with body movement There is evidence that domestication has shaped dogs’ and vocal intonation being enough to elicit social referenc- communicative and perceptual processes, where some differ - ing (Salamon et al. 2020). Beyond negative situations, in the ences have been noted between wolves and dogs (Gácsi et al. last decade or so, a wealth of research has focused on this 2005, 2009; Johnston et al. 2017; Kubinyi et al. 2007; Lampe question of what dogs perceive from human emotions cues. et al. 2017). On the other hand, similarities in the neurobio- However, nearly all studies focused on how dogs perceive logical basis for social abilities have been suggested between human facial expressions. This face bias might be due to humans and dogs (Buttner 2016) as well as similarities in an anthropocentric effect, since human faces are extremely other social features, such as behavioural synchronisation, important in conspecific social interactions (more so than which potentially increases social cohesion and affiliation the body or voice, Ekman et al. 1980). When humans inter- (Duranton and Gaunet 2018). More importantly, there is now act with dogs they are very likely to display frequent facial wide evidence of interspecific emotion cues perception and cues, since dogs are seen as quasi-social partners by humans recognition in different modalities (e.g., dog vocalisations, (Serpell 2009). Pongrácz et al. 2006; human facial expressions, Albuquerque Furthermore, a mechanism known as Face Based Emo- et al. 2016; Buttelmann and Tomasello 2013; Correia-Caeiro tion Recognition (FaBER) is suggested to be widespread et al. 2020; Müller et al. 2015; Nagasawa et al. 2011; Pitteri in mammals with good visual acuity, including humans et al. 2014a; Racca et al. 2012), lending further support to (Tate et al. 2006) and dogs (Lind et al. 2017), which may the proposed idea that co-evolution between humans and explain this face bias. However, despite humans being very dogs within a shared environment may have occurred to facially expressive, and both humans and dogs being perhaps 1 3 Animal Cognition Fig. 2 Facial landmarks in dogs and humans (adapted from Dog- as skull shape, fat deposits, and hair coverage. For example, dogs FACS and HumanFACS, respectively: Ekman et al. 2002a; Waller do not have a forehead or eyebrows (anatomical features unique to et al. 2013). The FACS systems are anatomically-based, standardised humans) and instead have a frontal region and browridges. Pictures and objective methods of facial coding that avoid subjective label- by Mouse23 from Pixabay.com (2021) and by Natalie Heathcoat from ling (e.g., "smile"). The position of facial landmarks in both species Unsplash.com (2021), free for commercial use is arranged differently due to the variation in anatomical features such well-equipped to perceive each other's facial cues (due to FaBER), there is large variance in facial morphology (Fig. 2) and the display of emotion cues between species (Caeiro et al., 2017, Fig. 3). Thus, the next question is whether dogs can read and infer meaning from human facial expressions by overcoming the challenges in successfully decoding emo- tion signals across a species barrier. In one study, dogs could discriminate human smil- ing faces from neutral faces (Nagasawa et al. 2011), but in another study (Buttelmann and Tomasello 2013) that included five breeds and two conditions (lab and open field), results were less clear: only one of the five breeds in the open field condition could discriminate happy from neutral faces. However, all breeds in both conditions could discriminate happy from disgusted faces (Buttelmann and Tomasello 2013), which might indicate some variation in breed ability and environment-dependent performance. Nonetheless, in these studies dogs showed expected dif- ferential reactions (approach/avoidance behaviours) when presented with joyful, angry, fearful and disgusted human faces compared with neutral face presentation. This suggests Fig. 3 Example of differences between characteristic facial cues of that the inconsistencies in both studies may be due to meth- emotion in a human and dog (Ekman et al. 2002a; Waller et al. 2013) odological differences in how dogs were tested, although it in equivalent emotional contexts (Correia-Caeiro et al. 2017; Ekman et al. 1994). Fearful facial expressions in humans tend to include is also possible that opposite valences are easier for dogs to eyes wide open (AU5) and lip corners stretched horizontally (AU20) discriminate. Another study (Müller et al. 2015) in which while dog fearful facial expressions tend to include panting (AD126). dogs successfully discriminated opposite valences (happy Happy facial expressions in humans tend to include the wrinkling vs angry) further examined how dogs were processing these around the eyes (AU6), while in dog happy facial expressions tend to include wide open mouths (AU27). AD: Action Descriptor, AU: facial cues. Here, dogs’ discrimination of facial expressions Action Unit, AD126: Panting, AU5: Upper Lid Raise, AU6: Cheek was shown to be based on configural cues, in which dogs Raise, AU20: Lip Stretch, AU27: Mouth Stretch. Dog images modi- might form associations based on previous experience of fied from Caeiro et al. (2017); Images by users Pexels and 2,843,603 faces, between different regions of the face and its expres- from Pixabay.com (2021), free for commercial use, and by Sifis Kav - roudakis from Youtube.com (2021) sion of emotion cues (Müller et al. 2015). Racca et al (2012) 1 3 Animal Cognition has also presented dog and human facial expressions with humans (e.g., configural process in reading faces and facial different valences (angry, neutral, and happy) to dogs, and expressions). However, there is a lack of comparative studies observed a consistent Left Gaze Bias (LGB) for negative leaving several important gaps in our knowledge concerning and neutral human facial expressions, but no bias for posi- the differences and similarities between how dogs perceive tive expressions. They argued that perhaps dogs interpret other dogs vs. humans (see Table S1 in the Supplementary human neutral facial expressions as potentially negative, Text for examples of studies). Comparative studies of how given their lack of clear signals to encourage approach. By wolves perceive emotion cues in conspecifics and humans contrast, there was a differential gaze asymmetry for dog are also needed if we wish to disentangle domestication and faces based on their valence, with no gaze bias for neutral ontogenetic effects. expressions but a LGB for negative expressions and a Right Gaze Bias (RGB) for positive expressions (Siniscalchi et al. 2010, 2013). This gaze asymmetry is possibly a reflection What methodologies have been used of brain lateralisation processes, also reflected in tail and to assess the perception of emotion cues head turning when facing or displaying emotion cues. This in dogs? might indicate a more general mechanism for perception of emotion cues, in which left and right hemispheres are In order to study the perception of emotion cues in dogs, mainly involved in the processing of positive and negative researchers need to conceptually define and then design emotions, respectively (Siniscalchi et al. 2008). Although it stimuli that contain these emotion cues (e.g., facial expres- could be argued that the gaze bias in dogs might be related sions). However, we need to recognise the difficulty, even in to approach/avoidance behaviour and is not necessarily cor- humans, of actually measuring emotion responses, due to the related with emotion cue perception or emotion experience. highly subjective nature of emotions (see “A brief summary Several eye-tracking studies with dogs have provided of the nature of emotion and its perceptual processes”). Most further fine-grained information on how this species per - studies of human emotion (regardless of whether they assess ceives visual cues (e.g., Barber et al. 2016; Park et al. 2019; perception, expression or experience) rely on self-report Somppi et al. 2014; Téglás et al. 2012; Völter et al. 2020; (i.e., explicit processes) in some form or another, which Völter and Huber 2022; Williams et al. 2011). These stud- presents a range of issues (Hofmann et al. 2005; Stone et al. ies have shown that, as with humans, dogs prefer to fix- 1999) (see S2 in the Supplementary Text for why implicit ate more on the internal facial features (especially on the measures are better than explicit ones, particularly for dog eyes) when viewing human and dog faces (Somppi et al. studies). Nonetheless, technological and scientific advances 2014) and process the composition formed by eyes, midface are opening up possibilities of measuring emotion percep- and mouth as a whole in facial expressions (Somppi et al. tion in more detail and using more controlled and system- 2016). Furthermore, dogs seem to have a specific gazing atic stimuli, while achieving better ecological validity. Next, pattern dependent on the facial expression they are look- we describe and critique the most common methodologies ing at, which may be associated with their interpretation of in dog studies, organised according to common biological the viewed expressions (Barber et al. 2016; Correia-Caeiro indicators of emotion, and whenever necessary for under- et al. 2020; Somppi et al. 2016). In one of these studies standing the method used or the critique to the method, we (Somppi et al. 2016), dogs quickly reacted to human threat broadly report how these have advanced our understanding faces by looking away, suggesting that dogs can recognise of how dogs perceive emotion cues. the expression content and respond as expected as per the dog species-specific repertoire (i.e., averted gaze in dog–dog Neurophysiological correlates interactions is widely used in averting visual threat, Brad- shaw and Nott 1995). Additionally, this ability to process By using fMRI in awake unrestrained dogs, researchers have human facial expressions seems to be influenced by the qual- been identifying which brain regions are activated when ity and amount of exposure to human faces in general, and, perceiving a variety of stimuli, including faces, voices, and particularly, if these faces are familiar or unfamiliar (e.g., gestures (Berns et al. 2012; Boch et al. 2021a, 2021b; Cook owner vs stranger, Barber et al. 2016). et al. 2014; Cuaya et al. 2016; Dilks et al. 2015; Karl et al. Overall, these studies show not only that dogs are atten- 2020). Whilst this methodology clarifies perceptual mecha- tive to humans (and conspecifics), but also that they are nisms at the brain level, it depends on both a substantial perceiving and reacting to cues of emotion in their social volume and prolonged period of activation for the signal environment. Dogs can also visually discriminate (at least to be detected. Small transient responses and regions will some common) facial expressions of emotion and infer or not be detected, which might be problematic when looking respond to these emotion cues accordingly, and some of into low activation perceptual mechanisms of emotion cues. their perception mechanisms seem to be similar to those of Nonetheless, fMRI studies have successfully shown how the 1 3 Animal Cognition dog brain responds to the emotion content of the human were detected slightly later (127–170 ms) and are closer to voice (reviewed in Andics and Miklósi 2018) and face (Karl “conscious” human responses. et al. 2020; Thompkins et al. 2018, 2021). This technology Despite their technical demands in terms of equipment, has also shown that different regions of the dog cortex pro- dog training and data analysis, these are certainly valuable cess dog vs. human facial expressions and that these regions methods for non-invasive studies of dog emotion perception. (Thompkins et al. 2018, 2021), in dogs seem to be analogous Particularly in comparative studies with humans, neurophys- to those found in humans, suggesting the existence of shared iological measures and their correlates (e.g., with behaviour) ancient neural networks for emotion cue perception (Haxby provide important measures of how dogs perceive emotion et al. 2000; Thompkins et al. 2021). Whether dogs have a cues. specific brain region for face processing is less clear, with some fMRI studies finding a dog face region (Cuaya et al. Systemic physiological correlates 2016; Dilks et al. 2015; Thompkins et al. 2018), while oth- ers do not (Bunford et al. 2020; Szabó et al. 2020). Bunford The autonomic responses that regulate, for example, endo- and colleagues (2020) suggested that the inconsistency of crine and stress responses (HPA axis, e.g., Mormède et al. results may be due to sensitivity of analysis, contrasts used 2007) can be measured through a variety of techniques in and/or data analysis. As such, even though dog studies with order to understand how individuals respond internally to fMRI have shown replicability (Berns et al. 2013), they are particular emotion cues or environmental triggers. Changes also a technically highly demanding method that still needs in cortisol, oxytocin, heart rate, and temperature are exam- fine-tuning at both methodological and conceptual levels ples of widely used indicators of internal states in dogs, that (Huber and Lamm 2017; Thompkins et al. 2016). For exam- can potentially be measured and/or manipulated non-inva- ple, event-related experimental designs in fMRI with few sively (e.g., by using salivary sampling, nasal administration, trials per condition (such as in Thompkins et al. 2021) lead and external monitors; Barber et al. 2017; Buttner 2016; to issues of low signal-to-noise ratio and statistical under- Katayama et al. 2016; Kis et al. 2015; Kuhne et al. 2014; power, and hence typically need very large trial numbers McGowan et al. 2018; Siniscalchi et al. 2018a, b). Very (~ 50–100 per condition) to compensate. Whilst these stud- recently, tear volume has also been examined in dogs as a ies give us unique direct insight into the activity of the dog new physiological indicator (Murata et al. 2022). Since these brain when looking at emotion cues, fMRI is perhaps better physiological indicators are correlated with internal states, used in combination with other methods (Karl et al. 2020) they allow us to investigate perceptual processes when an or taken cautiously until greater consensus on its value and individual is exposed to emotion cues. For example, in dogs limitations is achieved. cortisol increase is correlated with negative arousal (e.g., Another method, fNIRS (functional Near-InfraRed Spec- after an acute stress: Chmelíková et al. 2020) and oxytocin troscopy), that similarly to fMRI was first used in the early increase is correlated with positive arousal (e.g., after affilia- 90’s to measure human brain cortex activity (Ferrari and tive interactions with humans: MacLean et al. 2017); Hence, Quaresima 2012), has been used successfully only once in with adequate controls in place, these responses can poten- dogs to understand how their brains respond to visual and tially be used to determine if dogs perceive certain emotion tactile stimuli (Gygax et al. 2015). In humans, fNIRS has cues in a positive or negative way. Conversely, we can also been proposed as a good method for investigating emotion examine how perceptual processes might be modulated by processing (Balconi et al. 2015) and thus, might be a good inducing changes in these physiological indicators, such as complementary method to fMRI to investigate emotion cues by administering intranasal oxytocin (Kis et al. 2015). perception in dogs. Oxytocin, with its social bonding role (Romero et al. Surprisingly, the first established method to measure 2014), has also received particular recent interest due to human cortical brain activity, the EEG (electroencephalo- its function in modulating fundamental emotion processes gram, Shipton 1975), has only recently been used to meas- (e.g., attention to facial expressions), and thus how it ure dogs’ cortical activity related to emotion cues process- might facilitate dogs’ interspecific socio-cognitive abilities ing (Kujala et al. 2020). EEG can complement fMRI data (Buttner 2016; Kikusui et al. 2019). The application of oxy- since it may be more sensitive to shorter periods of activity. tocin seems to result in a marked change in gazing pattern Indeed, Kujala et al. study (2020) showed temporal resolu- to human facial expressions, with elimination of gaze bias tion analogies with humans when dogs processed facial cues towards the eyes in “happy faces” and decreased fixation on of emotion: threatening conspecific faces triggered strong “angry faces” (Kis et al. 2017; Somppi et al. 2017). Kis et al. “preconscious” responses with 30–40 ms response latency (2017) suggested this oxytocin effect is due to fear reduction, (typically < 75 ms response latency for visual stimuli in and thus less attention paid to the eyes as a relevant threat dogs, Törnqvist et al. 2013), while other facial expressions cue. Other authors (e.g., Macchitella et al. 2017) suggested a more general mechanism involving the creation of a positive 1 3 Animal Cognition expectation bias towards human behaviour to facilitate the found between conditions. In this latter study, IRT was only interpretation of the observed cues. used 2 min after the approach action, so perhaps thermal Studies measuring heart rate in dogs also show signifi- changes are detectable only whilst a particular positive or cant effects when dogs are exposed to human emotion cues. negative stimulus is present. For example, heart rate increased and heart rate variability Despite its value as a direct link to the internal changes decreased when dogs were exposed to a threatening stranger during emotions in individuals, physiological correlates on (i.e., fixed gaze on the dog while approaching, Gácsi et al. their own are extremely difficult to interpret due to both 2013). Similarly, in another study (Barber et al. 2017), dogs individual variation and numerous co-variates (e.g., time of gazing at human “angry faces” showed the highest increase day, age of the dog, etc.), which demand intense protocol in heart rate when compared to neutral, followed by “happy standardisation (Chmelíková et al. 2020). Furthermore, they faces”. On the other hand, “sad faces” decreased heart rate tend to vary in response to multiple stimuli that may be unre- in comparison to “neutral faces”. Since both “happy” and lated to emotions (e.g., physical or cognitive activity level: “angry faces” triggered an increase in heart rate and “sad Colussi et al. 2018), and often produce conflicting results faces” led to a decrease, it suggests heart rate is a better cor- (e.g., MacLean et al. 2017 vs. Powell et al. 2019). Physi- relate of arousal or emotion intensity, which when used with ological correlates, while potentially useful to assess how behavioural indicators of emotion quality might be useful to individuals perceive emotion cues in others, require much disentangle these potentially confounding factors. more research and should only be used in conjunction with Infrared thermography (IRT) has also successful been other measures, in particular behavioural indicators. used to record surface temperature changes in different parts of the body (e.g., eye, ears) when dogs were subjected to Cognitive and behavioural measures positive and negative situations (e.g., veterinarian examina- tion, Travain et al. 2015, Csoltova et al. 2017; owner sepa- These are probably the most common indicators used for ration, Riemer et al. 2016; receiving preferred food, Tra- measuring canine perception of emotion cues, due to rela- vain et al. 2016). In the negative situations, eye temperature tive ease of implementation in terms of methodology and tended to increase, whilst ear temperature decreased (Rie- generally lower ethical concerns. By using a wide variety mer et al. 2016). However, in another study (Fukuzawa et al. of experimental setups and equipment (Fig. 4, Table 1), 2016) in which strangers or owners approached dogs with researchers can systematically record how individuals neutral or smiling facial expressions, no differences were Fig. 4 Examples of various experimental setups and equipment that behind or next to the dog, 2: Dog participant, 3: Frame for free-range can be used to investigate perception of emotion cues in dogs (pic- of motion for the eye-tracker, 4: Eye-tracker camera, 5: Infrared cam- tures selected may not be from studies on perception of emotion cues era, 6: Back-projected stimuli, 7: Experimenter facing away from the as they are for illustrative purposes only). Experimental setups from: dog, 8: Eye-tracker target for eye triangulation, 9: LCD display, 10: A Correia-Caeiro et al. (2020, 2021), B Barber et al. (2016), C Kis Chin-rest, 11: Canvas with front-projected stimuli, 12: Speaker, 13: et al. (2017), D Ogura et al. (2020), E Faragó et al. (2010), F Lind Grey board to pin stimuli, 14: Separator between stimuli pair, 15: et al. (2017), G Muller et al. (2015), H Albuquerque et al. (2021). Paper printed stimuli, 16: Touchscreen, 17: Owner involved in the Image 4-B and 4-G courtesy of Ludwig Huber. 1: Owner sitting task, 18: Experimenter performing emotional displays for the task 1 3 Animal Cognition 1 3 Table 1 Comparison of experimental setups and equipment that can be used to investigate perception of emotion cues in dogs (see Fig. 4 for pictures of each experimental setup) Figure 4 Study reference Experimental paradigm/ Stimuli presentation Pre-experiment training? Owner present and Experimenter present? cross-refer- data recording method blinded? ence A Correia-Caeiro et al. (2020, Eyelink 1000 Plus (SR Back-projection screen No Yes Yes, facing away from the 2021) Research) eye-tracker on dog and stimulus free moving head mode B Barber et al. (2016) Eyelink 1000 eye-tracker on Back-projection screen Trained dogs to place head Owner sitting behind the No chin rest mode still on the chin rest dog C Kis et al. (2017) Tobii X50 eye-tracker on 17-inch LCD screen No Owner sitting behind the No free moving head mode dog, holding the dog’s body D Ogura et al. (2020) ISCAN ETL-300-HD eye- 21.3-inch LCD screen No Owner outside the room Two experimenters present tracker on chin rest mode instructing and/or holding the dog's head to rest on the chin-rest E Faragó et al. (2010) Intermodal Visual Paired Front projection canvas No Owner behind the dog No Comparison (IVPC), wearing headphones looking time recorded on camera and manually scored F Lind et al. (2017) Two-choice discrimination Printed on paper and pinned Pre-training of dogs to Owner behind the dog No paradigm to a board associate one stimulus looking down with reward G Muller et al. (2015) Two-choice discrimination Touchscreen Pre-training of dogs to use Owner present out of view Yes paradigm on a touch- the touchscreen and to from the dog screen associate one stimulus with reward H Partial experimental setup Effect of human social Human experimenter No Owner present and Two experimenters present from Albuquerque et al. cues on a “V” detour to perform emotional instructed to play a role in (2021) task, behaviour recorded displays and demonstrate the task on camera and manually how to solve a task scored Animal Cognition respond to a controlled stimulus, and thus inferences can be the audio-visual cues and look more at the non-matching made about their perceptual abilities. stimuli due to being presented with cues that cannot exist For example, in the lateralisation studies such as those together (found when individuals look more at incongruent mentioned in “What is known about how dogs visually per- stimuli). Whilst these methods can be easily implemented ceive emotion cues?” (Siniscalchi et al. 2010, 2013), dogs to investigate dog perception of emotion cues, these may produced particular behaviours with a side bias towards also be a limited method which traditionally has relied on valenced stimuli (e.g., head turn left when seeing human manually coding eye movements in dogs, (a task notori- facial expressions). This relationship between brain hemi- ously difficult due to the iris usually being dark colour sphere bias in valence processing and lateralised behaviour and without a visible white sclera). A better approach might give us insight into how the dog might be perceiv- from a methodological point of view (but perhaps more ing a certain stimulus, including stimuli featuring emotion expensive and harder to implement), is the combination of cues. However, exceptions and/or inconsistencies in the side eye-tracking as a recording method and IVPC and EV as bias studies (e.g., head turn left for negative but also “happy experimental paradigms, but no study has yet used them faces”) between behavioural and neural correlates remain in combination. It is also difficult to objectively interpret to be elucidated before its further use for the assessment of what the preferential looking actually means, which can perception of emotion cues. be both interpreted as visual preference for congruency, Another widely used behavioural measure in dog cogni- because it integrates matching information (e.g., voice and tion studies is gaze or body orientation towards a stimulus; face of owner), or preference for incongruency, because Despite these measures not always recording exclusively it is unexpected and hence draws more attention (Winters active observation or attention (but may also record blank et al. 2015). stares (Aslin 2007) or gaze avoidance), how individuals Within the studies looking at perception of facial expres- observe their environment often provides important infor- sions, two pieces of equipment have perhaps proved more mation on perception and processing of emotion cues. Gaze informative regarding dogs’ perceptual worlds: touchscreens behaviour can be recorded and interpreted through cognitive (Fig. 4-G) and eye-trackers (Fig. 4-A-D). Touchscreens have paradigms and/or eye-trackers (Fig. 4, Table 1). been widely used for examining many cognitive and per- Following on from infant studies, classical or variations ceptual abilities in dogs (e.g., categorisation, Range et al. of cognitive paradigms such as Intermodal Visual Paired 2008; face processing, Pitteri et al. 2014b; learning, Wallis Comparison (IVPC, Albuquerque et al. 2016, Fig. 4- et al. 2016; illusion perception, Keep et al. 2018), but rarely E) and Expectancy Violation (EV, Adachi et al. 2007) for emotion cue perception (Müller et al. 2015). This latter have been used in studies with dogs to assess different study showed that dogs are able to discriminate human facial aspects of facial processing. IVPC has been used to test expressions. However, perhaps due to restrictions in sample if dogs can extract and integrate emotion cues from dif- size (i.e., not all dogs can easily learn the task) or in the time ferent modalities (e.g., voice and facial expression), and needed for training, despite their huge potential for cogni- thus recognise the associated emotion (Albuquerque et al. tion and emotion perception studies, touchscreens are not 2016). These studies typically compare the duration of the yet used extensively in this area. By contrast, eye-trackers natural gaze of dogs towards each of two visual stimuli have been used for dogs in an increasing number of studies (e.g., facial expressions pictures) presented side-by-side (Gergely et al. 2019; Karl et al. 2019; Ogura et al. 2020; following an auditory stimulus (e.g., voice), to infer how Park et al. 2019; Rossi et al. 2014; Somppi et al. 2012, 2014; individuals process these stimuli (Fig. 4-E). Similarly, EV Téglás et al. 2012; Törnqvist et al. 2015, 2020; Völter et al. has been used in dogs to test cross-modal recognition of 2020) and specifically to investigate emotion cue percep- owner identification (Adachi et al. 2007) and other dogs tion (Barber et al. 2016; Correia-Caeiro et al. 2020, 2021; as a species (Mongillo et al. 2021), but not yet for emo- Karl et al. 2020; Kis et al. 2017; Somppi et al. 2016, 2017). tion cues (but see (Nakamura et al. 2018) for EV used These studies have investigated not only how dogs read with horses for successful emotion cues recognition). facial expressions (and in one study also body expressions, EV studies repeatedly present one stimulus followed by Correia-Caeiro et al. 2021), but also what factors modulate a second stimulus (e.g., congruent or incongruent image) this behaviour (e.g., experience with humans: Barber et al. and then compare looking times between conditions. 2016) and how this influences the human–dog relationship Both experimental paradigms test internal representa- (e.g., Karl et al. 2020). The advent of mobile eye-tracking tions of concepts, but are based on slightly different pro- technology (Pelgrim et al. 2022; Williams et al. 2011) can cesses: IVPC is based on the integration of cues from two extend this work to more ecologically valid settings with real modalities (found when individuals face two simultaneous rather than recorded stimuli. While most modern eye-track- visual stimuli and prefer to look at matching audio-visual ers (i.e., based on detecting near-infrared pupil and cornea stimuli), while in EV individuals are assumed to integrate reflections) have been specifically developed for the human 1 3 Animal Cognition eye, its use with dogs has been remarkably successful, prob- Breed and individual differences ably due to the similarity between the human and dog pupil and cornea-generated reflections (Barber et al. 2020; Somppi Dogs are often viewed as a homogenous species, despite et al. 2012). However, dogs do present some differences in their wide morphological, genetic, and behavioural varia- their visual system, such as a horizontally wider fovea (Bel- tion, which makes the generalisation of results to “dogs” tran et al. 2014) and different eye movements (Park et al. questionable in many circumstances, since the sample is 2019), but it is still unclear if or how these differences may not representative of all types of dog. Added to this are impact visual perception of emotion cues. potential lifespan changes that might not be apparent if the sample is not truly representative of all types of dog of all ages. Differences in how dogs perceive their (social and What are the limitations and challenges non-social) environment have been found with regards to to investigate the perception of emotion a dog’s skull length, breed, sex and/or age (Bognár et al. cues in dogs? 2018; Correia-Caeiro et al. 2021; Heberlein et al. 2017; Jakovcevic et al. 2010; Scandurra et al. 2018). For exam- When compared to neurophysiological and systemic physi- ple, hunting dogs were more attentive to their owners than ological correlates, behavioural and cognitive correlates are shepherd dogs (Heberlein et al. 2017), while aging led to perhaps the most prone to issues of subjectivity and observer decreased attention to human facial expressions (Correia- biases, and thus the choice of observational tool and use of Caeiro et al. 2021). controls become crucial to the evaluation of experimental Functional anatomical differences in sensory abilities validity. Fortunately, there has been a rapid technological between types of dog (e.g., see Barber et al. 2020 for a and scientific progress of methodologies such as eye-track - comprehensive review of the visual system of dogs relative ing to investigate dog perception of emotion cues, accom- to humans and its implications) mean that the social envi- panied by many practical advantages (e.g., ethical, ease of ronment might be perceived very differently, regardless of use). Nonetheless, other issues still need some further dis- any central capacities; i.e., the brain may be receiving very cussion to allow successful replication of studies, such as the different stimuli which may affect the subsequent process- use of consistent and precise definitions or what variables ing and behavioural responses. In addition, dogs live in a are being measured (such as quantification of facial move- variety of human environments (companion/urban vs free- ment or anatomically-driven Areas of Interest—AOIs in ranging/village dogs), which seems to impact, for exam- eye-tracking data analysis). Instruments such as DogFACS ple, sociability (Bhattacharjee et al. 2021) but not some (Waller et al. 2013) allow both standardisation of facial cues perceptual abilities (Bhattacharjee et al. 2020), although of emotion when designing/selecting experimental stimuli companion dogs have been much more studied than free- and objective measurement of facial responses to emotive ranging dogs. stimuli. Likewise, eye-trackers (e.g., Somppi et al. 2016) In addition, factors related to an individual’s life his- precisely collect an extensive array of metrics related to eye tory, experience, personality, etc. may also shape the way movements and pupil size (Völter and Huber 2021, 2022) individuals perceive their social environment, particularly that can be objectively represented relative to the stimulus emotion cues. These raise the importance of the concept being viewed (e.g., as fixation points and heat maps, Hol- of umwelt (Uexküll 1957) in animal communication (Man- mqvist et al. 2011; Kowler 2011). However, it is important to ning et al. 2004; Partan and Marler 2002; Uexküll 1957; appreciate methodological constraints that may be present, Uexküll and Mackinnon 1926), and likewise in dog emo- not only when using certain equipment, experimental para- tion perception, in which the subjective phenomenal world digms or when measuring certain indicators, but also when varies between individuals. The umwelt of an individual using dogs as a model species. Therefore, in this section, might influence, for example, sensitivity to certain cues we critically consider some of the most pervasive issues in or the motivation and attention needed to perform a task. the dog perception/cognition literature and suggest some This inevitably generates a sample bias by selecting dogs best practices and recommendations following from each who complete the task. Differences in temperament (and issue. We also suggest examples of research questions that also impulsivity, Fadel et al. 2016; Wright et al. 2011) may are needed to address issues arising from the methodologies lead to some dogs being more easily trained or intrinsi- used and its challenges (summarised in Table 2). In this sec- cally motivated within the experimental setup (Brady et al. tion, we also discuss some of the limitations and challenges 2018; Cavalli et al. 2018). further, to assist researchers reviewing previous work or While the standardisation of the laboratory environment planning future studies with dogs, especially in relation to is often projected as a way of controlling for extraneous vari- dog emotion cue perception. ables, in the context of emotion cues perception, it needs to be recognised that two dogs may perceive the sterile 1 3 Animal Cognition 1 3 Table 2 Points to consider and recommendations to design experimental stimuli and protocols, and tailor it to each particular dog as necessary (middle columns). Suggestions of research ques- tions for future studies that may answer particular methodological 592 challenges are also listed (column on the right). Points to consider and suggestions for future studies (both novel questions or 593 deepening of published questions) are organised by the features more prone to challenges (column on the left) Features prone to challenges Points to consider Recommendations Examples of future research questions 6.1. Breed, individual differences, and the Diversity of dogs as a species Sample larger diversity of dog types regarding breed, How does perception of emotion cues develop and umwelt of each dog age, sex, cephalic type, facial morphology, human vary over the lifetime of the individual? environment, life history, etc. Individual differences within Consider the umwelt of the dog that may vary within How does perception of emotion cues vary between dog types dog types regarding temperament, personality, moti- different temperaments? vation, mood, etc. Assess preferred rewards (e.g., food vs praise vs play) to ensure optimal motivation and attention during task Use validated psychometric scales and/or behavioural tests to assess individual differences Assess sensitivity to rewards and aversives with e.g., PANAS, Positive and Negative Activation Scale (Sheppard and Mills 2002) to assess each dog’s emotional predispositions and avoid sampling bias or excluding dogs Assess temperament and impulsivity to understand to which dogs the task provides an inherent reward (e.g., play with a human), and which dogs require external rewards (e.g., treat) to increase extrinsic motivation (Deci et al. 1999) Keep motivation and focus high, whilst keeping over habituation and boredom at a minimum (e.g., allowing the dog to leave/stop the experiment at any time for a short break, keep trials/sessions short and stimuli as varied as possible) Differences between dogs and Consider differences between dogs and humans when To what extent do dogs and humans use similar humans adapting experiments developed for humans and mechanisms for processing emotion cues of both regarding sensorial abilities (visual and other) conspecifics and heterospecifics? Control for other sensorial contaminants and influxes Investigate sensory abilities present in dogs but not in the testing environment, which may go undetected in humans: Does magnetism or temperature affect by humans but bias dog behaviour (e.g., odour, dog's visual perceptual mechanisms? magnetism, temperature) Animal Cognition 1 3 Table 2 (continued) Features prone to challenges Points to consider Recommendations Examples of future research questions 6.2. Experimental design: controlling variables Presence of the owner Allow presence of the owner, since 1) this makes the How does the presence of the owner affect the whilst maintaining ecological validity controlled environment of a laboratory more natu- performance of dogs in tasks of visual perception ralistic and also emotionally equable for different of emotion cues? subjects; 2) owners can act as secure bases for dogs in novel environments and when encountering stran- gers such as the experimenter (Gácsi et al. 2013) But also blind owners (both metaphorically—with- hold experiment goal until its end, and literally—use blindfold, earplugs), as owner’s inadvertent cuing must be controlled to avoid Clever Hans effects (Miklösi et al. 1998; Schmidjell et al. 2012) Collection of dog spontane- Allow for free full body movement responses to the Does immobilisation of the dog affect the percep- ous responses and ecological stimulus (e.g., tail wagging, head turns), since the tion of emotion cues? validity absence of natural responses may impact perceptual How does the wide range of experimental and processes stimuli properties (Fig. 4, Table 1) influence Give preference to naturalistic experimental protocol perception of emotion cues in dogs? For example, steps (luring/holding lightly vs. extensive training real-life demonstrators vs. video, spontaneous for immobilisation), and avoid conditioned or emo- vs. posed emotion cues, passive viewing vs. task tionally primed responses engaged, trained for remaining immobile vs. If less naturalistic steps are absolutely needed (e.g., allowing movement (e.g., tail or head turns) immobilisation in fMRI or to assess eye saccades), Does the equipment used in experimental setups discuss how these may have impacted the results with thermal and magnetic emissions impact the (e.g., not moving the head when perceiving emo- stimuli perception or the dog performance? tional cues, which are known to cause head turns in dogs (Siniscalchi et al. 2010, 2013)) But also control for increased random error and risk of correlated systematic error, which can make the correct and precise identification of the influential variable(s) more difficult. Random error effects may mask important effects that would be significant in a more controlled environment, and systematic error associated with other factors may lead to inaccurate associations Discuss how effects found in a highly controlled setting would stand in a real-life scenario. More controlled experiments (e.g., in the lab) facilitate equipment handling and ensure important but small effects are not masked by other variables, but may lose ecological validity Consider the thermal and magnetic properties of the equipment used (e.g., visual display units, fMRI, Fig. 5) with dogs as a potential confound in experi- ments (since dogs can sense these) Animal Cognition 1 3 Table 2 (continued) Features prone to challenges Points to consider Recommendations Examples of future research questions What are the differences in potential emotional 6.3. Experimental stimuli: spontaneity and valid- Selection and design of stimuli Thoroughly define and justify the conceptual basis for states and its associated cues between dogs and ity of stimuli, but with well-defined categories the stimuli selection and design (e.g., psychobiologi- humans? and objectively measured cues cal approach, context and triggers used to induce What contexts and triggers are ideal to collect facial expression, quantification of cues that match stimuli for perception of emotion cues in dogs? the dog behavioural repertoire) What potential emotional states may be triggered Avoid face-centric stimuli and include body postures by sensing magnetism or a distant source of heat and gestures, which are particularly important for and are there any cues displayed during these dogs, according to their natural behaviour and recent states? eye-tracking evidence (Correia-Caeiro et al. 2021)— this will counter the evident face publication bias and consider the umwelt of dogs Avoid the use of the exact same triggers to create stimuli featuring humans and dogs; Give preference to functional equivalent triggers (e.g., adult humans are generally not afraid of thunderstorms (Silverman et al. 2001), while dogs often are, at a clinical level (Lopes Fagundes et al. 2018; McPeake et al. 2017; Overall et al. 2001), hence thunderstorms may be a good trigger for dog fearful behaviour, but not for humans) Avoid (or be particularly cautious with) the use of emotion categories and corresponding behaviours/ visual cues common in humans but that may not be found in dogs (or at least not in the same form), including emotion categories and respective cues that are currently still being debated in canine sci- ence (e.g., guilt (Ostojić et al. 2015), jealousy (Cook et al. 2018; Karl et al. 2021)) And vice-versa, use emotion categories that are more common/relevant in dogs and have associated emotion cues in dogs but not humans. For example, positive anticipation cues are present in dogs but not humans Animal Cognition 1 3 Table 2 (continued) Features prone to challenges Points to consider Recommendations Examples of future research questions Classification and description Avoid emotion labels for stimuli, since these are sub- Exactly what AUs/gestures/postures (e.g., facial of stimuli jective and too broad and bodily expressions) dogs display in response Avoid using anthropomorphic/anthropocentric emo- to different emotional triggers? (also very little tion categories, i.e., based solely on human research studied in dogs) (e.g., from facial expressions), particularly if there haven’t been fundamental studies demonstrating these to be associated with a particular type of display in dogs Explicitly describe the context in which the stimuli were collected (i.e., dog growling during food com- petition/territory defence, etc.) Quantify the emotion cues observed in the stimuli (e.g., how many/which/duration of AUs/gestures/ postures), by for example using tools such as DogFACS (Waller et al. 2013) or DogBAPS (Huber et al. 2018) Validation of stimuli Give preference to ecological (i.e., pertaining to appropriate environment for the species) and evolu- tionary (i.e., pertaining to survival value for the spe- cies) validity, whilst considering the species natural behaviour, ecology and motivation (Tomasello and Call 2008), in order to ensure laboratory findings can be generalised to the outside world Avoid asking vague “expert opinion” (or a sample of random human observers) to validate the stimuli regarding the emotion as the only validation step— this will likely just incur in circular reasoning and confirm human observers biases Instead validate the stimuli by asking experts to independently quantify cues present in the stimuli and/or describe the context in which the cues were produced (see previous point about classification and description of stimuli)—this will assess agreement on objective and measurable cues instead of subjec- tive impressions Describe in detail in the methods section how the experts validated the stimuli as appropriate for the tested effect (e.g., a “happy dog face” needs to dis- play “relaxed open mouths”, “lip corners retracted”, and absence of “ears backwards”) Animal Cognition laboratory or same experimenter in very different ways (due to their umwelt). One may adapt and the other may perceive it as stressful; accordingly they may be emotion- ally primed in very different ways and this may affect their attention focus and perception (Burman et al. 2011; Sümegi et al. 2014). Experimental design The balance between controlling variables and maintaining ecological validity is a delicate and challenging one, which must be carefully considered. The problem of highly con- trolled and “aseptic” laboratory studies is that they might find effects that are of little relevance in the “real world” where many more variables are interacting with the experi- mental variables of interest. This can lead to problems of replicability, which are a concern not only in this area, but in the wider area of psychology (Farrar et al. 2021; Open Science Collaboration 2015; Tecwyn 2021). Furthermore, it also means research is focused on what we can measure in the laboratory rather than what might be ecologically important. Typically, emotion cue perception experiments with dogs tend to feature a passive visualisation of many trials and repetitions of relatively similar stimulus (e.g., facial expressions), which might lead to habituation and/or boredom, and subsequently affect attentional mechanisms which are crucial for such perceptual experiments. There are also protocol differences in how dogs are expected to participate in the experiment (Fig. 4, Table 1). For instance, in some eye-tracking studies the dogs are lightly physically held in place (e.g., Fig. 4-C, Kis et al. 2017) or lured to lie still (e.g., Fig. 4-A, Correia-Caeiro et al. 2020) on the day of the experiment, but in others, dogs are trained for several weeks/months throughout several stages before the experimental stage in order to remain immobile and place their heads on a chin rest to face the screen (Karl et al. 2019; Somppi et al. 2012). While an eye-tracker protocol with training is preferred due to limi- tations in certain eye-tracker models that do not allow head movements or whenever high-accuracy of eye movements is needed, protocol without training has a range of advan- tages, including less time/work invested before the test- ing stage, fewer exclusions of individuals that might not reach criteria during training (and thus better representa- tion of the species), as well as allowing for unconditioned responses and more naturalistic behaviour (allowing head turns for aversive stimulus, tail wagging, etc.). In particu- lar, free head movements might be important when meas- uring eye movements as head fixation may impact percep- tual and cognitive processes. For example, eye movements differ in humans (Collewijn et al. 1992) and mice (Meyer et al. 2020) between head fixed and head free setups. A 1 3 Table 2 (continued) Features prone to challenges Points to consider Recommendations Examples of future research questions Presentation of stimuli Present stimuli in an ecological valid way (e.g., facial Is there an impact when stimuli are placed at the expressions not at the dog’s eye level) dog’s eye level when in real-life it is not (e.g., Give preference to video as stimuli (Correia-Caeiro over-inflation of face which may modify eye et al. 2021; Karl et al. 2020) and avoid static movements)? pictures, since the former includes onset, apex and Does dynamic information change perception of offset of a visual cue (e.g., facial expression), natural emotion cues in dogs as it does for humans? timing, symmetry, intensity, etc. that the dog is more How do canine displays performed on command familiar with in their daily life differ from spontaneous displays? Give preference to spontaneous stimuli and avoid posed stimuli (e.g., real-life demonstrators will vary in their behaviour and will have posed behaviours, spontaneous facial expressions differ from posed facial expressions) But also match the specs of the equipment used for stimuli presentation to the visual abilities/needs of dogs (e.g., screen high refresh rate) Animal Cognition non-training protocol that allow individuals to choose used in experimental setups with dogs vary the tempera- whether to watch the stimuli or not may also incur in lower ture distribution across the colour spectrum on the screen data/calibration quality or data loss and the need to repeat (Fig. 5). Heavily magnetic equipment (e.g., fMRI) may calibration and trials more often, so due consideration to also interfere with dog’s perceptual processes. However, these aspects must be given. Another difference between very little research has of yet been done on these sensorial training and non-training protocols is the time dogs spend modalities in dogs (also see Table 2). watching a stimulus. Whilst with training protocols, indi- viduals are more likely to watch the stimulus (because they Experimental stimuli were trained to do so and due to the immobilised posture facing the screen) and thus more data points are collected, Whereas humans can produce posed facial expressions (even these may not represent how dogs observe stimuli in real though these vary in timing, intensity, and complexity in life (e.g., dogs avoid staring at faces of other dogs as this comparison to spontaneous ones, Cohn and Schmidt 2003; is a threatening signal). On the other hand, non-training Raheja and Gupta 2010), there is no evidence that dogs can protocols allow the individuals to watch or to avoid the “act out” emotion reactions. Even when trained to perform stimuli according to natural behaviour, but data collected a certain display (Déaux et al. 2015), it is unknown if this may be less or with lower quality. A final consideration is represents a faithful reproduction of the spontaneous reac- that in both cases the preconditioning with rewards might tion that would be displayed in a naturalistic context. This itself create an emotional bias. poses a problem since, typically, studies of dog (and human) The same consideration needs to be given to differences perception use pictures/videos of dogs often displaying ste- in the degree of active involvement by dogs in the pro- reotypically aggressive/happy facial expressions taken out of tocol of choice: some simply require passive viewing of context and without any control for the emitted cues. Thus, stimuli (e.g., eye-tracking, IVPC/EV paradigms), while the experimental stimuli may lack empirical evidence to cat- others request dogs to perform in more complex scenarios egorically state that they represent a happy/sad/angry dog. in which they need to make choices (e.g., through target In general, humans are quite poor at classifying dog facial approach: Fig. 4-F, touchscreen activation: Fig. 4-G) or expressions and body postures (Kujala et al. 2012; Meints take part effectively in social interactions with live dem- et al. 2010; Meints 2017; Meints and de Keuster 2009) and onstrators (e.g., Albuquerque et al. 2021; Buttelmann and this might extend to their selection of appropriate stimuli Tomasello 2013; Vas et al. 2005). While it can be argued for emotion cue perception studies. “Expert” agreement on that all scenarios are to some extent naturalistic, since its own, potentially creates a circular reasoning centred on dogs not only passively view emotion cues in social part- the human perception of what a “happy dog” looks like. The ners but also process these cues when interacting with tautology goes like this: there is a general idea that a happy their social partners, there might be a difference in the dog looks in a specific way based on broad and non-stand- cognitive processes recruited when additional cognitive ardised descriptions of dog behaviour (e.g., Darwin 1896; and physical processes are accompanying emotion cue McGreevy et al. 2012), “experts” agree with each other what perception. is the best example of this particular look, generally without Another common protocol approach when presenting specifying why, and then this is shown to other humans (e.g., visual stimuli to dogs is to place all stimuli vertically participants in a survey) that unsurprisingly, agree with the centred at dog's eye/head level, in order to enhance the experts. However, this is basically assuming that the human chances of detection of stimuli (particularly important in perception of emotion cues in dogs is interchangeable with immobile setups, where the head should be at a comfort- the actual emotion experience and thus expression of cues able angle for the dog for a period of time). However, spe- in the dog, which may not be the case. In Bloom and Fried- cifically when presenting human facial expressions, this man (2013), the authors created stimuli featuring facial cues might be problematic, as dogs do not usually see human of emotion in a single dog to parallel a database of human faces at eye level in real-life interactions, but instead need facial expressions for basic emotions (Ekman 1992; Ekman to look up on the vertical axis to detect facial cues of emo- and Friesen 1976). The dog facial expressions included emo- tion (Correia-Caeiro et al. 2021). tion cues for responses such as disgust, whose neurologi- Dogs may also make use of senses that humans or other cal, physiological and behavioural correlates have not been primates are not known to be able to use. For example, studied in dogs. Since the human facial expressions for the recently it was discovered that dogs can sense heat with basic human emotions have not all been found in dogs, this their noses from a distant source (Bálint et al. 2020) and approach does not have a scientific basis. The opposite may can sense magnetism both from the Earth’s field and from also be true, where some emotions may not have a defined magnetic objects (Adámková et al. 2017, 2021; Hart et al. human facial expression. For example, positive anticipation 2013; Martini et al. 2018). Visual display units commonly (i.e., reward anticipation) in dogs has strong neurocognitive 1 3 Animal Cognition Fig. 5 Top left: Laptop screen displaying a coloured image in the visible spectrum; Bottom left: thermal image of same laptop screen after 5 min—the thermal differential is associated with the keyboard and screen base; Top right: LED monitor displaying a coloured image in the visible spectrum; Bottom right: thermal image of same LED monitor after 5 min, high- lighting thermal gradient associ- ated with different colours. Image courtesy of Tim Simon evidence (Berns et al. 2012; Cook et al. 2016) and is asso- cues in dogs have used static facial expressions “frozen” at ciated with specific facial and ear movements (Bremhorst a high intensity as stimuli, that suddenly appear on a screen et al. 2019; Correia-Caeiro et al. 2017). However, in humans, (e.g., Fig. 6 from Barber et al. 2016; Somppi et al. 2016). it does not present a stereotypical facial expression, being While high intensity static stimuli might produce a larger identified instead by the absence of corrugation movement response and thus less noisy data due to their visual sali- (Korb et al. 2020). ency, such stimuli pose some issues regarding ecological This attribution of human features to animals (at least validity. For example, for human facial expressions, high without scientific evidence) or if selecting human features intensity static stimulus is dissimilar from facial expres- as the only ones important to consider when looking at sions displayed in real-life, which have an onset, apex and human–dog interactions results in anthropomorphic and/or offset (i.e., appearing/disappearing gradually with very spe- anthropocentric stimuli. In addition, stimuli that are “stereo- cific timings, or displayed at different, usually much lower typically” human, might also be socially and experientially intensities, Cohn and Schmidt 2003; Ekman et al. 2002a, constructed to some extent (i.e., they are learned and vary b), and omit the dynamic information that is an integral part across cultures, Barrett 2006; Elfenbein et al. 2007; Jack of facial expression processing (Kilts et al. 2003; Rymarc- et al. 2012a, b; Keltner and Haidt 1999). A more naturalistic zyk et al. 2016). Hence, when these stimuli are presented to approach based on investigating what kind of displays are dogs, they may be seen as novel/unusual stimuli or harder produced when the dog is faced with a potential emotion to be processed due to lack of experience with such stimuli. triggering context along with other evidence to triangulate While both video and static image stimuli may have limita- the emotion may offer a more logical, systematic, and sci- tions regarding visual properties (2D, colour use, refresh entific solution (Mills 2017). To gain a deeper understand- rate, etc.), these type of stimuli are easier to control and ing of what a “happy” dog truly looks like, recent studies some of their visual properties can be adapted (e.g., using (Bremhorst et al. 2019, 2021; Correia-Caeiro et al. 2017, higher refresh rate), However, in some studies on how 2020, 2021; Park and Kim 2020) have applied DogFACS dogs perceive emotion cues, real-life human demonstrators (Waller et al. 2013). This anatomically-based, standardised have been used to display the stimuli (e.g., facial and vocal and objective method of facial coding allows not only valida- expressions in the social referencing paradigm (Merola et al. tion and precise control of stimuli displayed in perceptual 2012, 2013, 2014) or its effect on learning tasks (Albuquer - experiments, but also empirical measurements of emotion- que et al. 2021)). Whilst real-life demonstrators might bet- ally-linked facial movements. ter engage and motivate dogs in the experimental tasks, it Not only is it important to define and capture spontane- also introduces varying degrees of lack of control and thus ous experimental stimuli, but we need to also consider its validity, such as in the difficulty involved in fully blinding dynamic nature. Typically, studies of perception of emotion demonstrators, in the display of posed cues, in the ability to 1 3 Animal Cognition repeat identical cues between trials, or in what cues exactly domestic dog is an excellent model to investigate the vis- dogs are taking from the demonstrators. ual perception of emotion cues, given its phylogenetic and Moreover, research has concentrated on how dogs per- ontogenetic adaptation to the human environment (“Why ceive facial emotion cues, due to the face being crucial in is the dog a good model for research on the perception of human–human interactions, but little is known about what emotion cues?”). We answer our second question concern- cues are important from the dog’s perspective. Dogs com- ing what is known about the mechanisms of perceiving municate much more with their bodies (e.g., play bow, emotion cues in dogs (“What is known about how dogs Bekoff 1977; Byosiere et al. 2016; Horowitz 2009), and visually perceive emotion cues?”), by focusing on studies there is evidence that full body motion is significant for dogs that demonstrated a set of refined skills for visual percep- (Delanoeije et al. 2020; Eatherington et al. 2019; Ishikawa tion of emotion cues in dogs. It is clear that dogs have the et al. 2018; Kovács et al. 2016). Even though humans still ability to discriminate and respond to facial expressions communicate a lot of emotion information with their bodies both in humans and dogs, but some inconsistent results (e.g., Martinez et al. 2016), faces with emotional cues are demand further research into this. Comparative research more important or informative for humans than for dogs between humans and dogs has been revealing both simi- (e.g., Correia-Caeiro et al. 2021). Thus, perhaps not surpris- larities (e.g., importance of emotion cues: Correia-Caeiro ingly when presented with whole human or dog figures, dogs et al. 2021; Thompkins et al. 2021) and differences (e.g., attend more to emotion cues from bodies than from faces how facial expressions are perceived, Correia-Caeiro et al. whereas humans attend more to faces than bodies (Correia- 2020). However, both for face and body perception, it was Caeiro et al. 2021), suggesting a marked difference in how also clear that more comparative studies are needed (i.e., both species perceive emotion cues. four-way studies with human and dog participants exposed to human and dog stimuli, e.g.,Correia-Caeiro et al. 2020, 2021). Furthermore, the notable gap in empirical studies Summary and general conclusions in how dogs process body cues both in conspecifics and in humans reveals deep anthropomorphic and anthropo- In this critical review of the concepts and methodologies centric biases. In “What methodologies have been used commonly used when investigating the visual perception to assess the perception of emotion cues in dogs?”, we of emotion cues in dogs, we aimed to briefly synthesise answer our third question concerning how emotion cue relevant results while critically evaluating methodologies, perception has been measured in dogs, by critiquing meth- in terms of their ability to make conceptual contributions odologies commonly used to collect and analyse each of to the field. In addition, we present frequent challenges them (grouped by neurobiological, physiological, and cog- in the literature and suggest crucial points for considera- nitive and behavioural indicators). Finally, in “What are tion and recommendations and outstanding questions for the limitations and challenges to investigate the perception future research (Table 2). We began by justifying why the of emotion cues in dogs?”, we detail important limitations Fig. 6 Examples of stimuli used in experiments aimed at investigating dog perception of facial expressions, with emotion labels and AOIs selected by the respective authors. A—Areas of Interest—AOIs labelled as “eyes”, “midface”, “mouth”, and “whole face”, adapted from Somppi et al. (2016), B—AOIs labelled as “forehead”, “eyes”, “mouth”, and “face rest”, adapted from Barber et al. (2016) 1 3 Animal Cognition Supplementary Information The online version contains supplemen- and challenges associated with measuring the perception tary material available at https://doi. or g/10. 1007/ s10071- 023- 01762-5 . of emotion cues in dogs, and list points to consider and recommendations for future studies. Small/easy to imple- Funding An early draft of this manuscript was included in the first ment adjustments (Table 2) based on our critique in this author PhD thesis, which work was supported by a PhD scholarship from the Research Investment Fund of the University of Lincoln. section, in most instances have the potential to increase robustness, reliability, and validity in future studies. The Declarations research area of emotion cue processing in dogs could strengthen its methodological approach if it more often Conflict of interest All authors declare that they have no competing acknowledged and then justified the balance between the interests. ecological and functional relevance of the experimental Open Access This article is licensed under a Creative Commons Attri- design with the validity, reliability, and objectivity of the bution 4.0 International License, which permits use, sharing, adapta- methods used. There is a need for a clearer conceptual tion, distribution and reproduction in any medium or format, as long foundation, where consideration should be given to the as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes underlying operational definitions for each hypothesis were made. The images or other third party material in this article are investigated (Correia-Caeiro 2017). Widely varied and cut- included in the article's Creative Commons licence, unless indicated ting-edge equipment, methods, and techniques are already otherwise in a credit line to the material. If material is not included in applied in this area (or at least in the more broader cog- the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will nition/perception areas), such as DogFACS, fMRI, EEG, need to obtain permission directly from the copyright holder. To view a fNIRS, fixed and mobile eye-tracking, thermal imaging, copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . and physiological monitors, which allow the objective measure of the dogs’ behavioural, physiological, and neu- rological responses when viewing emotion cues. None- References theless, these cutting-edge techniques should be applied alongside careful consideration of individual differences Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s (i.e., by using larger sample sizes), and experimental and face upon hearing the owner’s voice. 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Animal Cognition – Springer Journals
Published: Jun 1, 2023
Keywords: Emotion cues; Visual perception; Facial expressions; Bodily expressions; Human–dog relationship; Methodology
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