Emotional contagion in the human/dog dyad - physiological and cognitive consequences, and implications for pain management: A scoping review

doi:10.21203/rs.3.rs-3036868/v1

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Systematic Review

Emotional contagion in the human/dog dyad - physiological and cognitive consequences, and implications for pain management: A scoping review

https://doi.org/10.21203/rs.3.rs-3036868/v1

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Objective

The objective of this scoping review is to explore the implications of human-dog dyadic interactions on canine chronic pain, by investigating the mediating role of human emotion on the affective and behavioural states of dogs typically associated with canine pain.

Introduction:

Canine chronic osteoarthritis pain causes significant burden of disease in pet dog populations. It is understood that chronic pain is complex and multidimensional, with poor correlation between disease severity and functional disability. Interactions with their human caregivers have measurable effects of affective and physiological states in dogs. A better understanding of how these interactions may affect functional disability in dogs with osteoarthritis pain will inform patient management approaches.

Inclusion criteria:

This review included studies evaluating behavioural, physiological, affective or cognitive changes in dogs, within a human-dog dyad, in response to human caregiver behaviour, personality or emotion.

Methods

The databases searched included PUBMED, SCOPUS, CINAHL, SOCINDEX, PSYCHARTICLES AND PSYCHINFO, and articles were screened by two independent reviewers for assessment against the inclusion criteria for the review.

Results

55 Full text articles were included in the results.

Conclusions

The data support the hypothesis that human affective states influence canine affect, physiology, cognition and behavioural adaptation.

Chronic pain attributed to osteoarthritis causes significant burden of disease in domestic animal patient populations, with 20% of pet dogs experiencing painful osteoarthritis, affecting on average 11% of their lives (Anderson, Zulch et al. 2020). The assessment of canine osteoarthritis pain is based primarily on the pet owner’s observation of functional changes in the pet’s physical or affective behaviour (Gingerich and Strobel 2003, Brown, Boston et al. 2008, Piel, Kroin et al. 2014). Current approaches to understanding and treating canine osteoarthritis pain focus on the structural characteristics of osteoarthritis, disease modifying treatment approaches and pharmacological analgesia (Bland 2015, Anderson, Zulch et al. 2020). However, the nature of chronic pain is now understood to be more complex than a linear consequence of structural changes and nociceptive input from affected joints.

Pain can be classified based on both the duration (acute and chronic) as well as the physiological mechanism contributing to pain (Abd-Elsayed and Deer 2019). Mechanism-based pain classification includes nociceptive, neuropathic and nociplastic pain. Pain associated with osteoarthritis may be a combination of these pain types. Designing the most effective management plan for osteoarthritis pain requires an understanding which pain mechanisms are involved.

Mechanism-based classification of pain

Nociceptive pain occurs when nociceptors, widely distributed in the joints and surrounding tissues, are triggered by a potentially or actually noxious stimulus (Middleton, Barry et al. 2021). Such stimuli could be related to mechanical pressure or irritation of the articular and periarticular tissue, or a chemical stimulus caused by enzymes associated with joint inflammation. These nociceptive stimuli are then processed by several areas of the brain, including the somatosensory cortex and the limbic system to generate the perception of pain and to either amplify or attenuate pain, and generate an appropriate physiological and behavioural response. In a healthy system, descending nociceptive inhibitory pathways modulate pain through the action of beta-endorphins, enkephalins, and dynorphins on opioid receptors (Kendroud, Fitzgerald et al. 2021), among others. Nociceptive pain tends to respond in a predictable way to analgesics and anti-inflammatory medication.

Neuropathic pain occurs subsequent to lesion or disease of a somatosensory nerve resulting in silent, or mechanically insensitive nociceptor subtypes becoming active in the presence of inflammation. The nerve activation threshold drops, and changes in the dorsal root ganglia cause alterations in the type and number of peripheral receptors ready to sense nociceptive input. If this is not resolved, it may induce an increase in the excitability and receptive fields of central sensory neurons at spinal cord level, in a process likely mediated by the activation of glial cells. This process results in generalised hyperalgesia, which can lead to cortical reorganisation and a reduction in thalamic and prefrontal grey matter in patients with chronic pain, impairing the activity of the descending nociceptive inhibitory pathways to modulate pain (Curatolo, Arendt-Nielsen et al. 2006).

Nociplastic pain is defined as pain that arises from altered nociception despite no clear evidence of actual or potential tissue damage. It occurs where altered functioning of pain-related sensory pathways in the periphery and CNS causes increased sensitivity to somatosensory stimuli, which is experienced by the individual as pain. Nociplastic pain can co-occur with nociceptive and/or neuropathic pain, and is often associated with co-morbidities such as fatigue, interrupted sleep, sensitivity to light and/sound and cognitive problems. Nociplastic pain is the underlying mechanism behind chronic primary pain, where pain is experienced in the absence of any actual or potential tissue damage, and without evidence of somatosensory sensitisation (Abd-Elsayed and Deer 2019). Examples of nociplastic pain syndromes include chronic widespread pain, complex regional pain syndrome, chronic visceral pain syndromes and chronic primary musculoskeletal pain (Fitzcharles, Cohen et al. 2021, Nijs, Lahousse et al. 2021). It is increasingly understood that musculoskeletal pain, such as osteoarthritis pain, can be attributable to multiple, co-occuring pain mechanisms (Kosek, Clauw et al. 2021). The theoretical model of nociplastic pain in animals is recognised in the veterinary literature (Herzberg and Bustamante 2021). Most medications used to treat nociplastic conditions provide only a modest benefit, and adverse effects are more likely to occur in (Fitzcharles, Cohen et al. 2021). Therefore treatment for nociplastic pain syndromes emphasise non-pharmacological interventions.

Time-based classification of pain

Acute pain is pain that occurs immediately after an injury, and is usually nociceptive in nature unless a nerve lesion has occurred, in which case it would be nociceptive and neuropathic. Chronic pain is pain that continues beyond the normal healing process i.e. three months. Despite a general convention to classify pain as chronic when it lasts for three months or longer, pain can be considered chronic as soon as it becomes a maladaptive – it no longer serves a protective purpose and is no longer associated with the actual state of tissue repair [13].

Pain and disability

Chronic pain is associated with, and frequently measured in terms of functional disability in humans (Breivik, Borchgrevink et al. 2008, Dansie and Turk 2013) as well as animals (Gingerich and Strobel 2003, Brown, Boston et al. 2008, Piel, Kroin et al. 2014). However, there is not a consistent correlation between disability and pain (Vina, Ran et al. 2018, Vaughn, Terry et al. 2019, Helminen, Arokoski et al. 2020). In human arthritis patients, including children, it has been demonstrated that functional disability is moderated by physiological, emotional and cognitive factors(Kruger-Jakins, Saw et al. 2016, Louw, Zimney et al. 2016, Coakley, Wihak et al. 2018, Ernstzen, Keet et al. 2022), and caregiver self-efficacy (Woby, Urmston et al. 2007, Ashcraft, Asato et al. 2019, Rondon-Ramos, Martinez-Calderon et al. 2020, Bacardit Pintó, Ickmans et al. 2021). The Fear-Avoidance Model of pain links pain avoidance, cognitive processes and physiological reactivity to pain and disability in human chronic pain patients, including paediatric populations [13]. It describes the contribution of pain-related fear to the development of chronic pain, with growing evidence supporting the role of pain-related fear in pain catastrophising, hypervigilance, increased avoidance behaviours, and intensified pain intensity and functional disability (Leeuw, Goossens et al. 2007).

In animals, the experience of chronic pain also involves negative affective experiences and altered cognitive functioning (Pais-Vieira, Mendes-Pinto et al. 2009, Low 2013, Rochais, Fureix et al. 2016, Cockburn, Smith et al. 2018, Cowen, Phelps et al. 2018, Smith 2019), and similarly affects physiological processes (VMD 1998, Yu, Lundeberg et al. 2003, Kang, Park et al. 2022). Dogs have a cognitive ability structure, or phenotype, that is similar to that found in people, and are able to learn abstract concepts, often through interspecies (human-dog) social learning (Bensky, Gosling et al. 2013, Arden and Adams 2016, Lazarowski, Davila et al. 2021). Behaviour is the primary measure of chronic pain in dogs (Gingerich and Strobel 2003, Brown, Boston et al. 2008, Hielm-Björkman, Rita et al. 2009), but canine behaviour is, in part, a socially learnt phenomenon (Elgier, Jakovcevic et al. 2009, Horowitz 2009), and is mediated by affective states (Mendl, Brooks et al. 2010, Fureix and Meagher 2015, Ahloy-Dallaire, Espinosa et al. 2018). A dog’s cognitive processing and judgement biases of a situation or experience are influenced by the dog’s affective state, which affects behaviour (Starling, Branson et al. 2013, Cimarelli, Schoesswender et al. 2021). Canine affective states are also correlated with physiological changes such as fluctuations in cortisol and oxytocin, as well as dysregulation of heart rate variability, which are all factors associated with poor pain regulation in humans (Evans, Seidman et al. 2013, Vachon-Presseau, Roy et al. 2013, Carlesso, Sturgeon et al. 2016, Telles, Sharma et al. 2016, Tracy, Ioannou et al. 2016, Boll, Ueltzhoeffer et al. 2020, Ferrero, Amri et al. 2021, Paschali, Lazaridou et al. 2021).It is reasonable then to expect that cognitive, social and emotional factors will influence the pain experience of a dog in a way similar to that demonstrated in humans.

The behavioural expressions of the multi-dimensional, subjective pain experience of an individual dog is used as an objective measure of the dog’s pain levels (Mota-Rojas, Marcet-Rius et al. 2021), usually by the pet-parent, often with little awareness by the observer that their own behaviour can have a mediating effect on the behaviour they are observing in their dog. This interplay between the states and traits of the observer (pet parent) and the subject (dog) introduces an intersubjective dimension to chronic pain as being a phenomenon experienced by a dyad.

Many robust studies have been published that explore human-dog interactions from both anthrozoological (the interdisciplinary study of the interaction between humans and other animals), as well as comparative cognition approaches (Pfaller-Sadovsky and Hurtado-Parrado 2021). Studies of animal cognition are methodologically challenging (Miklósi and Abdai 2021, Pérez-Manrique and Gomila 2022), but evidence suggests that the similarities between human and dog social behaviours facilitate interaction and bonding with familiar humans (McGreevy, Starling et al. 2012, Duranton and Gaunet 2018, Grigg, Liu et al. 2022). Some dog-human interactions resemble intra-specific (dog-dog) prosocial behaviours, particularly in terms of affiliative behaviours and the use of body language. However, differences between intra-specific and inter-specific (human-dog) behaviours are observed in other situations, such as behaviour around food, the use of social referencing and rescue behaviour (Nowbahari and Hollis 2010, Quervel-Chaumette 2016, Quervel-Chaumette, Mainix et al. 2016).It has been suggested that novel forms of cognition arise out of human-dog interactions that cannot be explained by the individual species’ ethograms. In other words, behaviours observed during dog-human interactions may differ from behaviours normally observed between members of the same species – dog-dog and human-human (Merritt 2021).

Emotional contagion has been defined as: “The tendency to automatically mimic and synchronize expressions, vocalizations, postures, and movements with those of another person’s and, consequently, to converge emotionally” (Hatfield, Cacioppo et al. 1993). Behavioural synchronisation is an accepted proxy for emotional contagion, as it is an adaptive social phenomenon seen in many animal species (Duranton and Gaunet 2016). Synchronisation increases the chances of survival of each member of a social group by improving predator avoidance, increasing foraging efficiency and promoting social cohesion among individuals. It also helps to maintain pair bonds Suggestions that basic aspects of mimicry, or behavioural synchronisation, are precursors of emotional contagion are supported by neuroimaging studies in humans. (Duranton and Gaunet 2015). Rapid mimicry (RM) and yawn contagion (YC) are two such behavioural synchronisation processes, and have been shown to be socially modulated, occurring more frequently between individuals sharing close relationships.

Yawn contagion is considered to be a primitive form of behavioural synchronisation, although it is not associated with a specific emotional valence. The social modulation of yawn contagion is supported by psychological, ethological and neurological evidence, and demonstrates an association with the level of attachment bond (Palagi, Celeghin et al. 2020). Yawn contagion has been shown to occur in intraspecific relationships in Canid species. Romero et al (2014) found that wolves in their natural habitat yawned more frequently when exposed to conspecific yawning – yawning of other wolves - an observation that was positively linked to the strength of social attachment of the pair (Romero, Ito et al. 2014). There is less agreement that interspecies yawn contagion occurs between dogs and humans, with contradictory results emerging from experimental studies. Yawning is a well-described stress-response in dogs, which poses challenges in an experimental environment where dogs are exposed to novel stimuli, making it difficult to draw conclusions about yawn observations.

Another primitive form of emotional contagion is rapid mimicry. As a foundation for social competence, rapid mimicry facilitates play and reduces escalating aggression by functioning as a communicative signal to indicate shared intent. Mimicry occurs outside of conscious awareness and of voluntary control. Mimicry differs from imitation in that it involves no recognition of a goal associated with the action, and is thought to be generated by the mirror neuron system (Davila Ross, Menzler et al. 2008, Hess and Fischer 2013). The empathic nature of rapid mimicry, particularly during play, is supported by observations of a gradient of rapid mimicry behaviour related to the familiarity of the partner. This suggests that it is possible for two or more individuals who are synchronising their behaviour (i.e. mimicking) to share the same affective state (emotional contagion) (Palagi, Celeghin et al. 2020). The neurological processes underlying mimicry can be explained by the perception-action model (See Fig. 2). This states that the perception of the emotional state of others involuntarily produces a corresponding state in the receiver. This allows for social alignment of non-congruent emotional states, which stimulates reward centres in the brain (Preston and De Waal 2002). Mimicry is the foundation of play-related behavioural synchronisation – through the positive feedback loops generated by play-related behavioural synchronisation, play serves as an unconscious mechanism for reinforcing social affiliation (Preston and De Waal 2002, Palagi and Scopa 2017). Mimicry facilitates a self-sustaining loop that fosters emotional engagement (longer play duration), which in turn increases social closeness and synchronization (familiarity), increasing the probability for mimicry to occur (Palagi and Scopa 2017). Play is defined as all activity which has no immediate benefits, and which involves motor patterns typical of serious contexts (Burghardt 2005). Play may be a tool for reducing stress and improving social cohesion, and as such is often considered an indicator of welfare in dogs (Sommerville, O’Connor et al. 2017, Ahloy-Dallaire, Espinosa et al. 2018). Dogs combine body postures and facial expressions (eye and mouth movements) to convey emotional states (Quaranta, Siniscalchi et al. 2007) as well as motivation to play (Horowitz 2009). The adaptive value of mimicry depends on the ability of an individual dog to discriminate play signals when performed by other dogs.

Emotional contagion appears to be mediated by neurobiological reward mechanisms such as oxytocin release (Zoratto, Sbriccoli et al. 2018, Laviola, Busdraghi et al. 2021). It likely arose as an adaptive consequence of environmental sharing rather than genetic factors, and functions as a flexible social learning strategy (Nakahashi and Ohtsuki 2018). Emotional contagion can result in personal distress: “a self-focused, aversive emotional reaction to the vicarious experiencing of another’s emotion” (Eisenberg and Eggum 2009) or empathy “the naturally occurring subjective experience of similarity between the feelings expressed by self and others without losing sight of whose feelings belong to whom” (Decety and Jackson 2004). Behavioural indicators of empathy are considered to be comfort-offering or helping behaviours in response to another’s distress (Custance and Mayer 2012). While evidence for emotional contagion is widespread in the animal kingdom, it is mostly observed in the context of negative emotional states such as fear or pain. Negative emotional states tend to be easier to detect, and methods for identifying negative emotional states in animals are well-established. Consequently, most reports of emotional contagion are in the aversive domain (Düpjan*, Krause et al. 2020).

The human/dog dyad has been shown to be analogous to parent-child attachments (Prato-Previde, Spiezio et al. 2003, Taggart 2011, Asher, England et al. 2020), therefore it is hypothesised that pet-parent affective/cognitive states and behaviours have similar impacts on physical disability in dogs with painful osteoarthritis as have been observed in parent-child dyads (Mumme, Fernald et al. 1996, De Rosnay, Cooper et al. 2006, Robins, Perron et al. 2016, Bacardit Pintó, Ickmans et al. 2021). To support this hypothesis, evidence is needed to demonstrate that negative emotional states associated with amplified pain experiences can be transmitted from the pet-parent to their dog (emotional contagion). A preliminary search of MEDLINE and the Cochrane Database of Systematic Reviews was conducted and no current or underway systematic reviews or scoping reviews on the topic of the mediating effect of human caregiver emotional states on dogs’ emotional and cognitive pain processing were identified. Several studies, including one scoping review, demonstrate the beneficial effect of the human-dog relationship on human chronic pain (Horowitz 2008, Markovich 2011, Bradley and Bennett 2015, 2019, Carr, Norris et al. 2020, Nitkin and Buchanan 2020), but no studies evaluate the potential positive effect of this relationship on canine chronic pain.

The aim of this scoping review, therefore, was to evaluate the literature on emotional contagion in the human-animal dyad, with specific focus on the mediating role of human emotion on the affective and behavioural states of dogs that are typically associated with canine pain. These domains include the following: cognitive/emotional processing, behaviour and physiological parameters (Fig. 1). The rationale for selecting these criteria are the interconnected nature of these domains as they relate to pain. We were interested to explore the potential impact of modifying the beliefs, attitudes and behaviour of pet owners on pain-related functional disability in dogs with chronic pain. We conclude by discussing the potential implications of these dyadic phenomena for the management of chronic pain in dogs.

Review question

Aim:

In this review, we will explore the potential implications of human-dog dyadic interactions on chronic pain in the dog, by better understanding inter-species emotional contagion, specifically the human-dog dyad, and its physiological and cognitive consequences.

Our objectives are to determine the following:

Affect and effect: How do human affective states mediate canine affective states and cognition as measured by behaviour?

Affect and physiology: the measurable effects of negatively valenced inter-specific interactions on canine physiological variables

Affect and environmental adaptation: how does the valence of human-dog interactions influence a dog's ability to deal with novel (and potentially frightening) situations?

What are the potential implications of these dyadic interactions on chronic pain in the dog.

The scoping review was conducted in accordance with the Joanna Briggs Institute methodology for scoping reviews (Aromataris E, Peters, Marnie et al. 2020).

Search strategy

In this review, we wanted to specifically evaluate the effect of the human on the dog, within the context of the human-dog dyad. Studies evaluating the human-dog dyad were included in this review if they included the following concepts:

A behavioural response by dogs to human behaviour, personality or emotion.

A physiological response by dogs to human behaviour, personality or emotion.

An affective response by dogs to human behaviour, personality or emotion.

A cognitive response by dogs to human behaviour, personality or emotion.

Studies were excluded if they did not include dogs, referred to intra-specific relationships, or if the topic under investigation did not fall within one of the four domains described above.

The search strategy aimed to locate both published and unpublished studies. An initial limited search of GOOGLE SCHOLAR was undertaken to identify articles on the topic. The text words contained in the titles and abstracts of relevant articles, and the index terms used to describe the articles were used to develop a full search strategy. The search strategy, including all identified keywords and index terms, was adapted for each included database and/or information source. The reference list of all included sources of evidence was screened for additional studies.

Only studies published in English were included. The databases searched included PUBMED, SCOPUS, CINAHL, SOCINDEX, PSYCHARTICLES AND PSYCHINFO.

Search terms used:

emotional contagion and dogs”; “human-dog dyad”; “social referencing and dog”; “neurobiology and human/dog dyad”; “interspecies hormonal interactions AND dog”; “Interspecific social; cognition AND dog”; “Interspecific Referential communication AND dog”; “human-dog Referential communication”; “human-dog social learning”; “dog-human behavioral synchronization

Study/Source of Evidence selection

Following the search, all identified citations were collated and uploaded into EndNote 20.3 (Clarivate Analytics, PA, USA)) and duplicates removed. Following a pilot test, titles and abstracts were then screened by two independent reviewers for assessment against the inclusion criteria for the review. The full text of selected citations were assessed in detail against the inclusion criteria by an independent reviewer. Reasons for exclusion of sources of evidence at full text that did not meet the inclusion criteria were recorded. Any disagreements that arose between the reviewers at each stage of the selection process were resolved through discussion. The results of the search and the study inclusion process are presented in a Preferred Reporting Items for Systematic Reviews and Meta-analyses extension for scoping review (PRISMA-ScR) flow diagram (Fig. 1) (2018).

Types of Sources

This scoping review considered both experimental and quasi-experimental study designs including randomised controlled trials, non-randomised controlled trials, before and after studies and interrupted time-series studies. In addition, analytical observational studies including prospective and retrospective cohort studies, case-control studies and analytical cross-sectional studies were considered for inclusion. This review also considered descriptive observational study designs including case series, individual case reports and descriptive cross-sectional studies for inclusion.

In addition, systematic reviews that met the inclusion criteria were also considered, depending on the research question.

Text and opinion papers were also considered for inclusion in this scoping review.

Sources included in the study met the following criteria:

Population: The article had to make specific reference to pet or domestic dogs, defined as living in homes with permanent owners.

Concept: The article had to include an exploration of how human behaviour and emotion influence dogs' assessment of a situation both cognitively and emotionally.

Context: the article had include a dog-centred evaluation of how interaction with a human mediates the dog's experience of a situation

Data Extraction

Data were extracted from papers included in the scoping review by two independent reviewers using a data extraction tool developed by the reviewers. The data extracted included specific details about the participants, concept, context, study methods and key findings relevant to the review question/s.

The extraction form is provided (see Appendix II). The data extraction tool could be modified and revised as necessary during the process of extracting data from each included evidence source, but no modifications were made. Any disagreements that arose between the reviewers were resolved through discussion.

55 articles met the inclusion criteria and are included in this scoping review. The included articles included 43 experimental studies and four reviews.

In order to align the analysis of the articles with the objectives of this review, the results are grouped as follows:

Articles investigating the effect of human affective states on canine affective states and cognition

Articles investigating the effect of negatively valenced inter-specific interactions on canine neurobiology and physiology.

Articles exploring how these affective, cognitive and neurobiological effects influence a dog's ability to deal with novel (and potentially frightening) situations.

Affect and Effect – how do human affective states mediate canine affective states and cognition as measured by behaviour?

To evaluate whether emotional contagion occurs between humans and dogs we need a way of observing and measuring such an effect. Observing changes in dogs’ behaviour is one method of evaluating dogs’ emotional states, and how their affective states influence their cognition. Huber et al (2017) demonstrated that behaviour is a valid measure for observing emotional contagion, and proposed that the criteria for demonstrating emotional contagion in dogs through observation of behaviour should be as follows:

The dogs should behave differently in response to emotional and non-emotional information;

The dogs should respond differently to positive compared to negative emotional information

The behaviours expressed in response to negative emotional sounds should become more pronounced with prolonged exposure to the negative information.

Yawn Contagion

As a primitive form of emotional contagion, Yawn contagion has no emotional valence. However, its presence may serve as a marker for the potential for converging emotional states between individuals. Since yawning is also a well-described stress response in dogs, studies exploring yawn contagion between humans and dogs need to be designed carefully to control for stress-induced yawning. While O’Hara et al (2011) were unable to confirm human-dog yawn contagion in a group of 22 dogs, Silva et al (2012) and Romero et al (2017) found that yawn contagion was significantly higher when dogs observed a familiar human yawning. Silva et al tested how dogs would respond to auditory yawning sounds compared to control sounds in 28 dogs. They found that more dogs yawned uniquely at yawn sounds compared to control sounds (p = 0.04), with more yawns elicited in response to familiar yawns (p = 0.02) demonstrating that social modulation mediates yawn contagion. Romero et al measured dogs’ yawning responses to observed yawning when compared to control mouth movements. In this study, comprising 25 dogs, the researchers found that dogs yawned 5x more frequently when exposed to yawns than to control mouth movements (p = 0.025). They also found that familiarity with the human yawning increased yawn contagion frequency (p = 0.032), supporting the data published by Silva et al (2012). To control for stress-induced yawning, they monitored heart rate variability in all the dogs, and found no association between changes in heart rate variability and yawn contagion. This suggests that it unlikely that the yawning was stress induced (Silva, Bessa et al. 2012, Romero, Konno et al. 2013).

Mimicry

Mimicry is a fundamental social competency, functioning as a communicative signal to indicate shared intent. In their review on the subject, Palagi and Cordoni suggest that mimicry phenomena may depend more on social closeness, such as that between a dog and its owner, than on phylogenetic relatedness (dog-dog), which is possibly due to activation of the limbic regions involved in emotional processing. The ability of dogs to identify human affective states allows dogs to engage in mimicry of human behaviour, creating an affective bridge (or emotional connection) that makes interspecies play possible (Palagi and Scopa 2017, Palagi, Celeghin et al. 2020). Rooney et al demonstrated the effectiveness of human play signals in increasing frequency and duration of human-dog play. However, they also found that effective human-dog play signals do not necessarily reflect dog-dog play signals, supporting the work by Merritt et al that suggests novel forms of communication arising in the human-dog dyad. In other words, dogs can derive communicative intent from humans despite the signalling behaviours that do not reflect the canine ethogram, demonstrating that affective alignment – or emotional contagion – is occurring between human and dog (Rooney, Bradshaw et al. 2001, Merritt 2021).

Table 1

Included articles evaluating behavioural aspects of emotional contagion
DATE	AUTHOR	POPULATION	BEHAVIOURAL MEASURE	CONCEPT	CONTEXT	TYPE OF EVIDENCE
DATE	AUTHOR	Dogs in a human-animal dyad	BEHAVIOURAL MEASURE	Human behaviour and emotion influence dogs' assessment of a situation both cognitively and emotionally	Must relate to how interaction with a human mediates the dog's experience of a situation (dog-centred)	TYPE OF EVIDENCE
2019	Duranton et al	Pet dogs	Mimicry	Dogs prefer humans who synchronize with them	Dogs will have better affiliative bonds with humans who display behaviours that can match their state	Experimental
2020	Palagi et al	Pet dogs, wolves and humans	Mimicry	Behavioural synchronisation has a social adaptive function	Relationship between RM/YC and emotional contagion allowing for inter-specific emotional sharing	Review
2017	Palagi et al	Humans & non-human animals	Mimicry; Play	Proximate causation, ontogeny, function, and evolution of mimicry associated with social play is discussed		Review
2001	Rooney et al	Pet dogs	Play	Dogs recognise human play signals	Specific actions used by humans can be interpreted by dogs as interspecific play signals.	Experimental
2007	Quaranta et al	Pet dogs	Response to human expressions	A fundamental asymmetry exists in the control of functions related to emotion.	Seeing their owner elicits higher left brain hemisphere activation.	Experimental
2011	Deputte et al	Pet dogs	Response to human expressions	Dogs recognise human facial expressions of emotion	The dog responds by either approach, avoidance or increased attention behaviours	Experimental
2011	Nagasawa et al	Pet dogs	Response to human expressions	Dogs can learn to recognise smiling human faces	Dogs can learn to adapt their behaviour in response to the valence of human facial expressions	Experimental
2014	Merola et al	Pet dogs	Response to human expressions	Dogs have learned to associate their owners’ positive emotional messages to positive outcomes	Dogs find information provided by familiar humans easier to interpret	Experimental
2014	Yong et al	Pet dogs	Response to human expressions	The sound of human infants crying evoke a behavioural response in dogs	Dogs demonstrate increased submissive and attentive behaviours in response to human infant crying sounds	Experimental
2015	Duranton et al	Pet dogs	Response to human expressions	Dogs are sensitive to humans' emotional cues, and adjust their behaviour accordingly	Dogs exhibit social referencing	Review
2015	Muller et al	Pet dogs	Response to human expressions	Dogs can learn to recognise smiling human faces	Dogs can learn to adapt their behaviour in response to the valence of human facial expressions	Experimental
2016	Somppi et al	Pet dogs	Response to human expressions	Dogs use the composition formed by eyes, midface and mouth as a whole to interpret salience of human facial expressions	Dogs evaluate social threat based on facial expression rapidly, increasing attentional bias and evoking an avoidance response.	Experimental
2018	Colbert-White et al	Pet dogs	Response to human expressions	Dogs prefer positive human intonation	Dogs are more likely to select an object paired with a positive vocal intonation	Experimental
2021	Thompkins et al	Pet dogs	Response to human expressions	Human-dog attachment bonds have cognitive effects	Familiar and emotionally salient faces activate dog brain areas associated with reward and emotion processing	Experimental
2012	Custance et al	Pet dogs	Response to human stress/distress	Dogs exhibit approach behaviours to humans showing emotional distress	Emotional contagion motivates approach/affiliative behaviour in dogs	Experimental
2016	Buttner	Dogs (all)	Response to human stress/distress	Oxytocin mediates social behaviour	Overview of several factors associated with human-dog interaction	Review
2017	Huber et al	Pet dogs	Response to human stress/distress	Dogs express more behavioural indicators for arousal and negatively valenced states after hearing negative emotional sounds	Dogs can discern valences of human emotional sounds, and exhibit emotional contagion	Experimental
2018	Dzik et al	Pet dogs	Response to human stress/distress	OT increased positive cognitive bias and induced positive expectations	Proximity and contact seeking are associated with OT release in stressful situations.	Review
2019	Silas et al	Pet dogs	Response to human stress/distress	Dog participants in a canine therapy stress-reduction program experience increased stress	Handler stress negatively contributes to the affective experience of working therapy dogs	Experimental
2020	Meyers-Manor et al	Pet dogs	Response to human stress/distress	Dogs show more approach behaviour to humans in distress while themselves exhibiting signs of distress	Emotional contagion occurrs in the human-animal dyad	Experimental
2020	Carballo et al	Human-dog dyads	Response to human stress/distress	Dogs exhibit rescue behaviour in response to stressed, trapped owners more than calm owners	Emotional contagion motivates rescue behaviour in dogs	Experimental
2020	Van Bourg et al	Pet dogs	Response to human stress/distress	Rescue behaviour is empathically motivated pro-social behaviour	Human distress causes emotional contagion driving rescue behaviour	Experimental
2021	Pereira et al	Pet dogs	Response to human stress/distress	Owners trait anxiety mediate dogs' reactivity to their owners' emotions.	Dog owners' trait anxiety is significantly associated with anxiety-related behaviors in their dogs.	Experimental
2022	Helsly et al	Pet dogs	Response to human stress/distress	Owner stress = dog stress, owner behaviour mediates dog behaviour and affect	Emotional contagion and social referencing influence canine affect and behaviour	Experimental
2016	Duranton et al	Pet dogs	Social referencing behaviour	Dogs take cues from owners when about the safety of a situation	Dogs exhibit social referencing	Experimental
2016	Flom et al	Pet dogs	Social referencing behaviour	Negative human affect reduces canine exploratory behaviour	Emotional contagion mediates canine social referencing	Experimental
2012	Silva et al	Pet dogs	Yawning	Dogs show yawn contagion to the sound of human yawning	Yawn contagion is more pronounced when exposed to familiar humans' yawns	Experimental
2013	Romero et al	Pet dogs	Yawning	Contagious yawning is modulated by inter-species affective components	Dogs exhibit rudimentary empathy with humans	Experimental
2011	O'Hara	Pet dogs	Yawning	Unable to confirm empathy as basis for interspecies contagious yawning	Interspecies yawn contagion may not be empathy based	Experimental

The role of mimicry in fostering social affiliation was further demonstrated by Duranton et al, who found that pet dogs show a greater affiliation with humans who mimic their walking behaviour (Duranton, Bedossa et al. 2019). In this study, which included 28 dogs, two experimenters, to whom the dog had been familiarised, took turns to enter a room with the dog and its owner, who was instructed to remain motionless and quiet. One experimenter synchronised her movements with the dog’s (random) behaviour, remaining 5m away, but did not engage with the dog in any other way. The second experimenter moved randomly around the room, not engaging with the dog. The order of experimental conditions was randomised, with a 10 minute break in between. Following another break, both experimenters entered the room, not engaging with the dog, and the dog was released. Dogs demonstrated a preference for the person who had shown behavioural synchronisation with them, although some differences between breed types were observed. The researchers acknowledge that simple exposure effect could be at play, but consider that this was adequately controlled for by both the familiarisation phase as well as the fact that the non-synchronised experimenter was still near the dog for the duration of the experiment, just not acting in a synchronised way. These data suggest that the way in which humans respond to the behaviour of dogs may influence the perceived affiliative responses by the dog towards the human.

Behavioural response to human facial and auditory emotional cues

Dogs can recognise behavioural displays by humans, including facial expressions (Deputte and Doll 2011, Nagasawa, Murai et al. 2011, Merola, Prato-Previde et al. 2014, Somppi, Törnqvist et al. 2016, Proops, Grounds et al. 2018, Thompkins, Lazarowski et al. 2021), body postures and vocalisations (Rooney, Bradshaw et al. 2001), and adjust their behaviour accordingly. Dogs appear to experience happy human faces as appetitive or rewarding, while their response to angry faces suggest that they experience this as aversive (punishing). It is not clear whether this preference reflects a recognition of the affective information of the facial expressions, or whether it is a function of associative learning through previous positive or negative experiences associated with the expressions (Müller, Schmitt et al. 2015). The suggestion that dogs seem to react to a voice or odor of a human in accordance with the valence of interactions they had previously experienced with that person, and the findings that happy human facial expressions are associated with a right hemisphere (negative) bias in some dogs, may support the role of associative learning in dogs’ behavioural responses to human facial expressions, rather than emotional contagion (Jardat and Lansade 2022).

The extent to which a dog’s recognition of the valence of human facial expressions depends on familiarity with the specific human is unclear. Nagasawa et al (2011) found that dogs are able to distinguish between happy (smiling) and neutral facial expressions in the absence of other stimuli (i.e. through photographs), and are able to do so for strangers as well as familiar humans. However, they found that the dogs’ ability to generalise facial expressions to strangers appears to be dependent on their exposure to individuals of the same gender as the stranger (Nagasawa, Murai et al. 2011). Merola et al (2014) demonstrated that dogs find it easier to distinguish between emotional expressions (facial and vocal) delivered by a familiar human compared to a stranger (Merola, Prato-Previde et al. 2014), while Muller et al (2014) did not find this discrepancy in face recognition between familiar and novel faces, (Müller, Schmitt et al. 2015). In their 2022 review on canine cognition, Jardat and Lansade argue that dogs differentiate our emotions, across different forms of facial expression, and react to them accordingly, through a variety of behavioural responses. For example, dogs are more likely to stop an ongoing meal after hearing angry compared to happy human voices. (Jardat and Lansade 2022).

Somppi et al studied dogs’ gaze fixation to demonstrate that dogs use a combination of human facial features to derive socially relevant cues, and that threatening human faces triggered an avoidance response in the dogs. Dogs appear to be able to discern a threatening human facial expression without needing to fixate on the human face, and rapidly adopt avoidance or appeasement behaviours (Somppi, Törnqvist et al. 2016).

Huber et al (2017) explored the behavioural responses of 53 dogs to non-emotional sounds, as well as positively and negatively valenced emotional sounds of both other dogs and humans. By pooling ten behavioural variables, categorised as either person/object orienting behaviours or behaviours indicating arousal and negative emotional states, they were able to demonstrate that emotional contagion does occur in intraspecific (dog-human) contexts. (Huber, Barber et al. 2017).

Colbert-White et al investigated the effects of vocal intonation only on dogs’ object choices, and compared that to combined vocal and pointing cues (Colbert-White, Tullis et al. 2018) in a study of 24 dogs. Although the sample size was small, the study was well designed to control for confounding variables. Dogs preferred positive vocal intonation above neutral breath and negative intonation. Positive-valence vocalizations are associated with activation of reward centres in dogs’ brains (Andics, Gácsi et al. 2014, Andics, Gábor et al. 2016). Therefore, the positive-valenced vocal cue may have had the effect of increasing arousal compared to the neutral and negative cues, and the dog’s positive response to these positive intonations may be influenced by previous associative learning, rather than it being a true reflection of the dog’s understanding of a social cue. Regardless of the mechanism behind the dogs’ choice, the Colbert-White study did show a positive behavioural response to positive vocal cues. This effect appears to be more salient when it involves a familiar human compared to an unfamiliar human. Response to vocal affective information may also be context dependant. Helsly et al did not find that positive vocal cues alone reduced stress behaviours in 29 female-owned dogs during veterinary examinations, but that neutral or negative vocal cues (like scolding the dog) increased the dogs’ stress behaviours (Helsly, Priymenko et al. 2022).

Behavioural responses to human displays of stress/distress

Emotional contagion between humans and dogs is supported by the finding that observed levels of stress in dogs (measured through behavioural observations), correlate with human affective state, independent of environment or activity. Yong and Ruffman (Yong and Ruffman 2014) tested the behavioural responses of dogs to only the sound of a baby crying, and observed an increase in submissive behaviours and attentiveness in the test condition. This study suggests that emotional contagion – in this case contagious distress - is a potential driver of behaviour change in dogs. The authors suggest that this demonstrates the presence of a primitive form of empathy. However, empathy requires perspective-taking of the distressed individual, and it is unlikely that the dogs were able to identify the source of the distress in this test paradigm. It has been postulated that parents are biologically primed to experience suffering in response to the sound of infant crying, in order to motivate feeding behaviour. We do not consider that the data from this study satisfy the criteria for demonstrating empathy.

Silas et al (2019) used observations of dog behaviour to evaluate the stress levels of 40 dogs participating in an on-campus stress-reduction programme. These programmes provide students on university campuses an opportunity to spend time with therapy dogs – each dog is accompanied by a handler. On-campus Canine Assisted Intervention programmes have been found to reduce homesickness, increase life satisfaction, and reduce stress in university students. Each dog was rated for signs of stress at three time points: (1) ten minutes after arrival; (2) half-way through the session; and (3) at the end of the session by both their handler as well as a researcher trained in the recognition of canine behavioural stress indicators. These stress signs included trembling, yawning, nose licking, paw lifting, and looking away, and was rated on a scale from 1 (not very stressed) to 5 (very stressed). Both dog handlers and students self-reported their own stress at the start and again at the end of the session. 25% of the dogs exhibited behavioural signs of increased stress, which correlated with the stress of their own handlers at the start of the session, rather than the stress of the students participating in the programme (Silas 2019). These findings are supported by data from a study by Pereira et al (2021). This study evaluated self-reported data by 1172 dog owners to explore the link between owners’ trait anxiety and their dogs’ fear and anxiety-related behaviour. They found a positive correlation between owners’ trait anxiety and dogs’ anxiety-related behaviour problems (Pereira 2021). These data were further analysed to determine whether dog-directed owner behaviour, such as coercive training methods were mediating factors that could underlie the observation, but no relationship was found for this variable. Over-protective behaviours by owners towards their dogs were significantly associated with fear and anxiety-related behaviour in dogs, a finding independent of owners’ trait anxiety.

A specific behavioural measure that is often used to assess emotional contagion is rescue behaviour. Rescue behaviour is a form of pro-social behaviour in which a rescuer exhibits behaviours directed towards averting a threat to an endangered individual, thereby potentially putting itself at risk (Hammers and Brouwer 2017). The following criteria have been proposed to identify rescue behaviour: 1) the ‘victim’ should be in distress, and at risk of physical harm should it not escape from the situation; 2) the ‘rescuer’ places themselves at risk; 3) the behaviour of the ‘rescuer’ should be relevant to the circumstances of the victim’s distress; and 4) the rescuer should gain no reward or benefit from performing the behaviour (Nowbahari and Hollis 2010). One of the mechanisms that have been suggested to underlie rescue behaviour is the presence of empathy, the capacity to recognize and share feelings experienced by another individual, while recognising that these feeling arise outside of the “self” and are attributable to the unique experience of an “other”. In other words, empathy requires the capacity for perspective-taking, and is distinguished from other forms of emotional contagion by its emphasis on the feelings of the observed individual. (Preston and De Waal 2002, Quervel-Chaumette 2016). Therefore, rescue behaviour paradigms are models commonly used in behavioural science to explore the presence of empathy in non-human animals. However, pro-social behaviours such as rescue behaviours can occur without empathy being present, as a function of maintaining biological fitness of the group (Vasconcelos, Hollis et al. 2012).

Carballo et al (Carballo, Dzik et al. 2020) set out to clarify the mechanisms behind rescue behaviour. This study of 47 dogs was well designed to control for various potential mechanisms for rescue behaviour raised in previous studies, such as post-separation contact seeking (a feature of attachment bonds (Buttner 2016)), and using the dog’s name (dog responding to a conditioned stimulus). When comparing a stressed-owner condition to a calm-owner condition, dogs in the stressed owner condition experienced greater elevations in heart rate, but not cortisol, and exhibited more attempts at rescue behaviour (opening, or attempting to open the box in which the owner was trapped) than in the calm owner condition. This study supports the hypothesis that owner stress can induce dog stress, in this case demonstrated by increased heart rate, and induce a change in behaviour compared to non-stressed dogs. However, the researchers note that this behaviour could be explained by the dog’s desire to establish contact with the owner in order to reduce their own stress, rather than to reduce the owner’s stress. In this study no changes in dog baseline cortisol were detected, which may be explained by the opportunity the dogs had to perform an action to attenuate their stress – in this case establishing contact with the owner. These results are supported by the work of Van Bourg et al (Van Bourg, Patterson et al. 2020) who tested 67 dogs in a similar paradigm. They found that dogs were more active and displayed statistically significantly more stress behaviours in the distress test than in the control tests (reading test or a food task). However, as a significant proportion of dogs still released their trapped owners in the control condition, their overall results could not exclude the possibility that the rescue behaviour was motivated by social contact-seeking rather than emotional-contagion and empathy.

The work of Dzik et al (2021) provides support for rescue behaviour being driven by emotional contagion, but not empathy. They found that administering intranasal oxytocin to dogs reduced rescue behaviour (Dzik, Carballo et al. 2021). Since oxytocin is involved in stress-buffering, this suggests that recue behaviour is indeed driven by emotional contagion (dog stress), but not empathy (human stress). When the dogs experienced a reduction in contagious distress as a result of the oxytocin administration, they were no longer motivated to release the owner, despite the owner’s continuous distress signals.

In contrast, Custance and Mayer used a paradigm for studying empathy previously used in human infants (Radke-Yarrow and Zahn-Waxler 1984) to test empathy in dogs (Custance and Mayer 2012). The aim of this study was to differentiate between curiosity, egoistic attention- or comfort-seeking and expressions of genuine empathic concern in response to sounds of individuals crying. They controlled for environmental stress by testing 18 dogs in their own homes. The dogs were tested to see whether they would approach a distressed stranger (empathic response) or their owner (comfort-seeking response), and the emotional tone (body language) of the dogs’ approaches was also evaluated by independent observers, blinded to the study hypothesis, from video footage taken during the test. Variables were tested by comparing the dogs’ responses to distressed sounds (crying) by the owner, humming by the owner and the stranger, as well as normal talking as a control condition, and simple curiosity was controlled for by the presence of a silent witness in the room. They found that dogs directed significantly more person-oriented behaviours toward the person crying, regardless of identity (owner or stranger), and the majority of dogs that approached the crying person did so in a submissive manner, as opposed to curious, playful or calm. If the behaviour of the dogs in this study was motivated by a desire to reduce their own stress, they would have been more likely to approach the owner, rather than the crying stranger, suggesting the presence of empathy.

Meyers-Manor and Botten (Meyers-Manor and Botten 2020)replicated the Custance and Mayer (Custance and Mayer 2012) study but added laughing as an experimental condition, along with normal talking. They also added a measure of heart rate variability to assess emotional contagion occurring in the dogs. This study included 16 dogs, and replicated the findings of the previous study, demonstrating statistically significantly more person-oriented behaviours towards the crying human, whether owner or unfamiliar person, especially in dogs belonging to female owners. No significant change in behaviour was shown in the talking and laughing conditions. They further demonstrated that the dogs that demonstrated increased person-oriented behaviours in the crying condition also exhibited higher stress/arousal as measured by a reduction in HRV. This suggests that emotional contagion and empathy are plausible mechanisms behind the behavioural responses shown by dogs (Meyers-Manor and Botten 2020).

Affect and physiology: the measurable effects of negatively valenced inter-specific interactions on canine physiological variables

Brain activation

Brain activation patterns can also provide data on how the valence of dog-human interactions affect dog physiology. Using fMRI, Thompkins et al studied the brain activation patterns of dogs when presented with images and videos of both familiar as well as unfamiliar humans expressing positive, negative as well as neutral emotional cues. They found activation of the amygdala, caudate and hippocampus. While the amygdala and hippocampus demonstrate emotional activation, activation of the caudate suggests reward centre activation in response to familiar human faces. This indicates that human faces have social relevance to dogs, as the researchers were able to correlate familiarity bias in a behavioural task with the magnitude of differential activation to familiar and emotionally salient faces in the amygdala, caudate, and hippocampus of the dog brain (Thompkins, Lazarowski et al. 2021). This provides a potential mechanism underlying dogs’ propensity for social referencing shown towards humans.

A brain hemisphere bias in dogs has been observed with the perception of the valence of emotions communicated by humans. It is thought that the right hemisphere dominates for the perception of negative or arousing emotions while the left hemisphere is favoured when perceiving positive or familiar emotions. Left hemisphere bias has been observed with happy vocalizations in dogs, but surprisingly, happy faces have been associated with a right hemisphere (negative) bias in dogs. This suggests that there could be a discordance, for some animals, between the valence of the human emotion expressed and the way it is perceived by dogs. For example, some dogs could perceive happy human faces negatively (Jardat and Lansade 2022).

Human-dog interactions also affect canine cognition. Sumegi et al (2014) which showed that stress improved canine working memory performance. In a study of 52 dog/handler dyads, they found that while stress in both humans and dogs improve working memory, manipulating human stress alone changes dog working memory performance, providing further evidence for the phenomenon emotional contagion (Sümegi 2014).

Heart rate variability (HRV)

Heart rate variability (HRV) can be used as a measure of dogs’ affective states, and is considered a particularly useful measure, as changes develop rapidly, and can be measured in real time. One of the arguments in support of this method of assessing emotional contagion as opposed to behavioural methods, is that it clarifies the potential physiological mechanisms driving behaviour change (Silva, Bessa et al. 2012, Carballo, Dzik et al. 2020).

Meyers-Manor et al demonstrated that dogs experience increased heart rates in response to the sound of human babies crying (Meyers-Manor and Botten 2020). Katayama et al (2019) assessed the effect of induced owner stress on the heart rate variability of 14 dogs. In this fairly small cross-over trial, they found that owner HRV was positively correlated with HRV in their dogs, and that this association increased with both duration of ownership and average time the dog-human dyad spent together. The researchers also found that female dogs demonstrated a higher susceptibility for this type of stress contagion than male dogs. However, the authors do not state how many dogs of each sex were in the final sample, so it is difficult to draw a conclusion from this result (Katayama, Kubo et al. 2019).

Cortisol

Cortisol is commonly used as a biomarker to evaluate stress in an individual. Salivary cortisol is a convenient way of measuring acute stress, while hair cortisol concentration is a practical measure of long-term cortisol activity, or chronic stress. Yong and Ruffman (Yong and Ruffman 2014) demonstrated both humans and dogs experienced an increase in salivary cortisol after listening to the sounds of babies crying, but no increase in control conditions such as the sound of a human infant babbling, or computer-generated white noise. This study applied a variety of statistical analyses to control for confounding factors such as demographics, previous exposure to children, discordancy of the sounds, sex and hormonal status. The only significant variable was found to be the crying sound.

The nature of the relationship between dog and owner appears to be have a mediating effect on dog stress. Dogs with strong attachment bonds to their owners, tend to have lower baseline cortisol levels, while dogs that have insecure-ambivalent attachments with their owners demonstrate poor cortisol variability. This is further influenced by owner personality, as even dogs with strong attachment bonds with owners tend to demonstrate poor cortisol variability, and therefore poor stress adaptation, if the owners score high in Neuroticism. (Kotrschal, Schöberl et al. 2009, Schöberl, Wedl et al. 2012). Sundman et al (2019) demonstrated increased HCC in dogs belonging to owners scoring high in neuroticism, openness and conscientiousness, suggesting that the cumulative effect of poor stress buffering in these dyads leads to a higher overall cortisol accumulation (Sundman, Van Poucke et al. 2019). Incongruent emotional cues from humans also appear to increase dog stress. It has been shown that non-genuine play – where a human handler attempts to initiate play with a dog in a directive way, using commands to instruct the dog to perform play-like activities, rather than through genuine affective play signalling cues – increases salivary cortisol concentrations in dogs (Horváth, Dóka et al. 2008).

Buttner et al (Buttner, Thompson et al. 2015) investigated whether changes in handler cortisol levels before and after competition were correlated with changes in the cortisol levels in their dogs. They found a positive correlation in cortisol elevation, especially in dogs belonging to male handlers, that appeared to be unrelated to affiliative/punitive behaviours exhibited by the handler. However the authors note that the elevation in dog cortisol levels may be a function of arousal related to the intense activity, which is a variable relevant to both handler and dog, and as such, the increase in cortisol measured in the dogs post-competition may not be attributable to handler factors. The authors further did not note any association between handler behaviour towards the dog and the elevated cortisol measures, but do note that body cues by handlers may be subtle and imperceptible to the researchers, but still salient to the dog who is familiar with the handler’s body language. This is especially plausible since the handlers were aware that they were being observed, and may have taken care to not display overt punitive behaviours towards their dog. Because the authors were unable to control for arousal states in the dog related to the activity itself, it is our opinion, this article does not in fact provide the evidence for hormonal synchronisation that it purports.

Table 2

Included articles evaluating physiological aspects of emotional contagion
DATE	AUTHOR	POPULATION	PHYSIOLOGICAL MEASURE	CONCEPT	CONTEXT	TYPE OF EVIDENCE
DATE	AUTHOR	Dogs in a human-animal dyad	PHYSIOLOGICAL MEASURE	Human behaviour and emotion influence dogs' assessment of a situation both cognitively and emotionally	Must relate to how interaction with a human mediates the dog's experience of a situation (dog-centred)	TYPE OF EVIDENCE
2021	Thompkins et al	Pet dogs	Brain activation	Human-dog attachment bonds have cognitive effects	Familiar and emotionally salient faces activate dog brain areas associated with reward and emotion processing	Experimental
2022	Jardat et al	Domestic dogs	Brain activation	Perceiving human emotions; interpreting human attentional states; referential communication; social learning with humans	Animal sociocognitive abilities irt humans	Review
2014	Sumegi et al	Pet dogs	Brain activation	Emotional contagion influences working memory in dogs	Owner stress improves dog's performance in a spatial working memory task	Experimental
2019	Katayama et al	Pet dogs	Heart rate variability	Emotional contagion in dogs is facilitated by duration of ownership and sex	Emotional contagion occurrs in the human-animal dyad	Experimental
2012	Silva et al	Pet dogs	Heart rate variability	Dogs show yawn contagion to the sound of human yawning	Yawn contagion is more pronounced when exposed to familiar humans' yawns	Experimental
2020	Carballo et al	Human-dog dyads	Heart rate variability	Dogs exhibit rescue behaviour in response to stressed, trapped owners more than calm owners	Emotional contagion motivates rescue behaviour in dogs	Experimental
2020	Meyers-Manor et al	Pet dogs	Heart rate variability	Dogs show more approach behaviour to humans in distress while themselves exhibiting signs of distress	Emotional contagion occurrs in the human-animal dyad	Experimental
2014	Yong et al	Pet dogs	Cortisol	The sound of human infants crying evoke a behavioural response in dogs	Dogs demonstrate increased submissive and attentive behaviours in response to human infant crying sounds	Experimental
2009	Kotrschal et al	Working dogs	Cortisol	Owner personalty mediates dog baseline cortisol, and affects working ability	Owner gender and personality influences dog cortisol and dyadic practical functionality.	Experimental
2012	Schoberl et al	Pet dogs	Cortisol	Owner personality, relationship with the dog, and attachment bonds influence stress buffering	Dog-owner relationship mediates dog cortisol in stressful tasks	Experimental
2019	Sundman	Pet dogs	Cortisol	Dogs mirror the stress of their owners	Human personality traits neuroticism, conscientiousness, and openness significantly affected dog cortisol	Experimental
2008	Horvath	Working dogs	Cortisol	Affiliative and disciplinary behavior of human handlers during play	Human play style affects stress in dogs as measured by cortisol	Experimental
2015	Buttner	Pet Dogs in competition	Cortisol	Human cortisol increases = dog cortisol increases independant of explicit human behaviour	Human stress = dog stress	Experimental
2020	Wojtas	Pet dogs	Cortisol	There a strong relationship between salivary cortisol between rescue dogs and their handlers	The hormonal (cortisol) relationship was stronger for females and female dogs than for males and male dogs	Experimental
2015	Nagasawa	Pet dogs	Oxytocin	We tested the hypothesis that an oxytocinmediated positive loop exists between humans and dogs	Gazing behaviour between humans and dogs increase dog urinary oxytocin	Experimental
2019	Cimarelli	Human-dog dyads	Oxytocin	Dyadic relationship mediates stress-coping	Affiliative relationships buffer against stress, but does not have to be human-dog	Experimental
2022	Helsly	Pet dogs	Oxytocin	Owner stress = dog stress, owner behaviour mediates dog behaviour and affect	Emotional contagion and social referencing influence canine affect and behaviour	Experimental

Table 3

Included articles evaluating adaptive aspects of emotional contagion
DATE	AUTHOR	POPULATION	ADAPTIVE MEASURE	CONCEPT	CONTEXT	TYPE OF EVIDENCE
		Dogs in a human-animal dyad		Human behaviour and emotion influence dogs' assessment of a situation both cognitively and emotionally	Must relate to how interaction with a human mediates the dog's experience of a situation (dog-centred)
2011	Deputte et al	Pet dogs	Approach behaviour	Adult vs non-adult dogs' responses to human emotional faces	Dogs’ capacity for using human affect for social referencing emerges early in life.	Experimental
2018	Fugazza et al	Pet dogs	Approach behaviour	Human affective state influences approach behaviour in puppies	Emotional contagion establishes a foundation for intraspecific social referencing	Experimental
2009	Elgier et al	Pet dogs	Approach behaviour	Dogs have a preference for social cues, but this is mediated by reinforcement history	Dog's behaviour is mediated by social cues and reinforcers	Review
2016	Flom et al	Pet dogs	Approach behaviour	Negative human affect reduces canine exploratory behaviour	Emotional contagion mediates canine social referencing	Experimental
2012	Merola et al	Pet dogs	Approach behaviour	Dog look referentially to familiar humans in novel situations, and adjust approach behaviour based on valence	The valence of human cues in novel situations influence dog behaviour	Experimental
2012	Merola et al	Pet dogs	Approach behaviour	Dog look referentially to unfamiliar humans in novel situations, and adjust approach behaviour based on valence	The valence of human cues in novel situations influence dog behaviour	Experimental
2015	Yong et al	Pet dogs	Approach behaviour	Dogs make use of referential communication by a stranger	Happy expressions increase object focus, fearful expressions increase human-directed attention	Experimental
2013	Merola	Pet dogs	Approach behaviour	Dog look referentially to humans in novel situations, and adjust approach behaviour based on human cue valence	The valence of human cues in novel situations influence dog behaviour	Experimental
2015	Merola	Working dogs	Approach behaviour	Trained dogs rely more on human referential information compared to untrained dogs	Reliance on human referential communication is learnt	Experimental
2016	Duranton	Pet dogs	Approach behaviour	Dogs take cues from owners when about the safety of a situation	Dogs exhibit social referencing	Experimental
2020	Salamon et al	Pet dogs	Approach behaviour	Dog approach behaviour in a frightening situation is influenced by owner behaviour and vocal intonation	Human behaviour and expressions are a source of social communication for dogs	Experimental
2021	Mehrkam	Pet dogs	Play	Social play was significantly higher during conditions in which an attentive owner was present	Owner attention facilitates social play in dogs	Experimental
2009	Kotrschal	Working dogs	Task performance	Owner personality mediates dog baseline cortisol, and affects working ability	Owner gender and personality influences dog cortisol and dyadic practical functionality.	Experimental

Wojtas et al (Wojtaś, Karpiński et al. 2020) examined 41 Canine search and Rescue dog/handler teams to evaluate the correlations in salivary cortisol values between handlers and their dogs. They found a positive correlation between handler and dog stress levels as measured by salivary cortisol changes, which was stronger for both female handlers and female dogs. They also found an association between cortisol level and task performance, suggesting that cortisol variation had a cognitive effect. Whether the cognitive effect of increased dog or handler cortisol is positive or negative in terms of task completion appears to be dependant on the nature of the task.

Oxytocin

Interactions with humans also has the potential to improve stress buffering in dogs as mediated by oxytocin. Gazing has been linked to oxytocin release in dogs, with dogs engaging in gazing behaviour more often within a dog-human dyads compared to intraspecific dyads. The more stressed dogs are, the more frequently they attempt to make eye contact with owners. Increased gazing at humans appears to be an additional stress relieving mechanism not present in intraspecific dyads (Nagasawa, Mitsui et al. 2015, Cimarelli, Marshall-Pescini et al. 2019, Helsly, Priymenko et al. 2022).

Interspecific play also has the potential to mediate stress through its effect on oxytocin (Payne, Boot et al. 2015). During genuine play, based on mimicry and emotional alignment, dogs experience a reduction in cortisol and may experience an increase in oxytocin, as intranasal oxytocin administration tends to facilitate play initiation, as well as prolong the duration of play, which correlates with human studies where oxytocin has been shown to enhance motor mimicry (Duffy and Chartrand 2015, Pavarini, Sun et al. 2019).

Affect and environmental adaptation: how does the valence of human-dog interactions influence a dog's ability to deal with novel (and potentially frightening) situations?

Human-directed social referencing

The process by which dogs use affective and behavioural information from humans to form their understanding of a situation is referred to as social referencing. Dogs’ capacity for recognising human affective information and using it as social referencing information emerges early in life. Deputte and Doll (2011) showed that non-adult dogs react more to human emotional faces than to control facial expressions, but that only adult dogs will react in different ways to the valence of the facial expression (Deputte and Doll 2011). This suggests that, while dogs can recognise different human facial expressions, their behavioural responses to facial expressions may be mediated by associative learning rather than emotional contagion. In contrast, Fugazza et al (2019) tested the effect of human affective cues in 48 8-week old puppies on approach behaviour when exposed to a novel stimulus. During the test, the puppies demonstrated referential looking towards the human. Not only did positive human affective cues increase the puppies’ approach behaviour towards the novel object, they also retained this effect during later trials where no human or conspecific was present. The approach behaviour of the puppies in the positive human condition was similar to the secure-base behaviour exhibited by the puppies in the presence of the mother, but which was not demonstrated in the presence of unfamiliar conspecifics (Fugazza, Moesta et al. 2018).

In a review by Elgier et al, they concluded that dogs show a preference for human-directed social referencing, even in the presence of competing physical cues such as odour cues, which one would expect to be more salient to dogs. Dogs also employ mimicry of human behaviour in problem solving tasks (Elgier, Jakovcevic et al. 2009). When evaluating dogs’ referential communication towards humans, it is essential to consider the effect of conditioning on such observed behaviours. Referential communication behaviours such as gazing and point following can be modulated by whether they are reinforced or not. Dogs exhibit highly flexible and adaptive learning abilities and will discontinue behaviours that no longer produce a desired outcome. Despite this, Elgier et al demonstrated that dogs will allow a social referencing cue (pointing) to override a conditioned stimulus (baited marker) in a choice discrimination test. This shows that dogs’ social referencing behaviour is not only a product of previous reinforcement of human cues. The addition of affective information to human pointing cues does not appear to influence point-following behaviour, although it does seem to influence dogs’ exploratory behaviour – dogs understand the pointing cue, but the valence of affective information in addition to the cue determines their confidence in following the cue. (Flom and Gartman 2016).

The impact of human affective behaviour on novel object approach behaviour in dogs was further explored in two studies by Merola et al. In the first study, which included 58 dogs of a heterogenous sample, the researchers evaluated dogs’ responses to a novel, scary object in depending on either neutral, positive or negative affective behaviour demonstrated by the owner. They found that dogs that were less confident, as assessed in a neutral test, engaged in significantly more referential looking towards the owner (p = 0.002). Dogs in the negative group spent significantly more time exhibiting static behaviour, interacting with the owner and maintaining close proximity with the owner compared to the dogs in the positive group. Dogs in the positive group demonstrated more exploratory behaviour. Explicit approach or avoidance behaviour by the owner significantly influenced the dogs’ reaction to the ambiguous object. (Merola, Prato-Previde et al. 2012) To assess whether dogs would respond in similar ways to affective information from strangers, Merola et al repeated this test paradigm on a group of 54 dogs, but included the use of a stranger as informant. They found that the degree to which dogs relied on affective cues from strangers was fairly similar to the owner-directed referential communication previously demonstrated (Merola, Prato-Previde et al. 2012). Yong and Ruffman also evaluated the use of referential communication by dogs in the presence of a novel object, this time using only a stranger as the informant. 114 dogs were exposed allocated to either a happy, fearful or neutral test condition group. The procedure for the ‘neutral’ test condition selected by the researchers involved the informant mimicking a chicken – flapping her arms and making clucking noises – and it could be argued that this is an unfamiliar and confusing behaviour to dogs, rather than a neutral behaviour. This is reflected in the results of this study showing no difference in the dogs’ responses to the novel object in the fear and ‘neutral’ conditions. They found that the dogs directed more attention towards the novel object in the ‘happy’ test condition, while directing more attention (referential looking) towards the experimenter in the ‘fear’ and ‘neutral’ test conditions, supporting the data by Merola et al that dogs will engage in referential communication with strangers when faced with a novel situation, allowing their actions to be mediated by the valence of the human’s emotional cues (Yong and Ruffman 2015).

Comparing pet and trained dog populations, Merola et al found similar levels of referential looking between groups, although in terms of approach behaviour, higher levels of training appear to increase the dogs dependency on owner information, with the trained dog group demonstrating less exploratory behaviour, with the trained dogs displaying more stress signals in the absence of information from their owner, despite positive affective cues provided by a stranger (Merola, Marshall-Pescini et al. 2013). It appears that with increased levels of training comes a higher level of dependency on referential information provided by the owner, even in the presence of a positive stranger.

In a study by Duranton et al published in 2016, social referencing by dogs was tested by evaluating how human approach behaviour influenced dog approach behaviour when faced with an unfamiliar person (Duranton, Bedossa et al. 2016). The study included 52 dogs. The dogs and their owners were placed in a familiar room, and the dog was free to move around the entire space. During the test phase, an unfamiliar person entered the room. Depending on the predefined test condition, the owner would take three steps towards the stranger (approach condition), remain stationary (neutral condition), or take three steps backwards, away from the stranger (retreat condition). No other verbal or affective cues were given by either human. In the retreat as well as the neutral condition, dogs looked at the stranger sooner and spent more time interacting with their owner. These findings are consistent with previous findings in dogs exposed to unfamiliar objects (Merola, Prato-Previde et al. 2012). The authors postulated that the neutral condition, in the absence of any other affective information, might have been interpreted by the dogs as ‘freezing’, a well-documented threat response in dogs (Stellato, Flint et al. 2017). This study supports the hypothesis that, as in infants, social referencing in dogs is present and constant across situations, and that social referencing can be intraspecific. Salamon et al 2020 replicated these results in a similar test setup with 53 dogs, but with the addition of reassuring/worrying vocal cues to match the approach/retreat behaviour (Salamon, Száraz et al. 2020).

Owner stress, dog stress and environmental adaptation

Merkham and Wynne (2021) found that dogs were 15 times more likely to initiate intraspecific social play when an attentive owner was present. The authors propose several mechanisms for this, but highlight the role of stress and physiological arousal. Play is a strategy employed by dogs to regulate social stress. As dogs are also reliant on humans to meet their biological needs, the presence of the caregiver is associated with access to social and biological reinforcers. Therefore, when dogs experience physiological stress, play may serve as a way to gain caregiver attention to increase the likelihood of provision of food and other resources. (Mehrkam and Wynne 2021).

Owner-dog attachment bonds and stress may have an effect on the ability of the human-dog dyad to adopt new behaviours. Kotrschal et al (2009) found that dogs with a strong dyadic attachment bond with an owner scoring high in Neuroticism – an attachment bond associated with low baseline stress - scored lower in novel task performance (Kotrschal, Schöberl et al. 2009). In contrast, stress appears to improve canine working memory performance (Sümegi 2014). The differences in the effect of stress on task performance may be related to the type of task at hand, a memory task vs a problem-solving task, as well as suggesting a potentially deleterious effect of long-term baseline stress on cognitive function.

Dogs are able to discriminate human facial, vocal and postural affective information, and demonstrate a behavioural response, which is more pronounced on the negative axis. Basic behavioural synchrony reflects subconscious neurobiological processes that occur instinctively, and are socially modulated. Yawn contagion indicates that state matching can occur between dogs and humans as function of emotional contagion, but does not appear to have any adaptive function. Rapid mimicry, on the other hand, is driven by a reward feedback loop where social congruence stimulates reward centres in the brain through the mirror neuron system. This form of emotional contagion does not involve perspective taking (empathy), but is instead an adaptive, pro-social reflex that facilitates the maintenance of social bonds. This is demonstrated functionally by the use of mimicry in play behaviour, which is a fundamental social bonding and learning activity. Play further has a function in reducing stress, and is often used as a measure of animal welfare. However, as it has been shown that dog play is mediated by a human audience effect, and mimicry is a foundation for play, it is likely that human negative affect and aversive behaviour will have a suppressive effect on canine play, creating a negative feedback loop between owner belief and dog behaviour. This will have a significant negative judgement bias effect on the reporting of canine welfare, as well as being detrimental to the social bond between human and dog. The effect of caregiver belief on ratings of canine welfare, specifically pain, was demonstrated by Conzemius et al (2012), who showed a placebo effect on improved lameness ratings of up to 44.8% in dogs enrolled on a NSAID drug trial – a figure well above the accepted minimally clinically meaningful improvement in pain (Conzemius and Evans 2012). This highlights the potential impact of considering pet owner judgement biases in any canine pain intervention.

Overt displays of human stress/distress causes stress in dogs. This triggers a behavioural response by dogs involving actions that are interpreted by human observers as also distressed, an observation that appears to further support the existence of human-dog emotional contagion. In such distress conditions, dogs tend to experience an increase in heart rate and lower heart rate variability, indicating physiological stress. Behaviourally, dogs display an increase in human-oriented behaviours in such distress conditions. Interestingly, it is only when the sound of human distress is separated from human behavioural cues of distress (babies crying) that dogs experience an increase in cortisol. This emphasises the primitive nature of emotional contagion in dogs. Behavioural displays of distress by humans appear to affect dogs differently, as they are able to attempt behaviours to establish contact with the owners, therefore having a physical outlet for their stress-induced affective state. It has been shown that moderate physical exercise will lower cortisol levels (Hill, Zack et al. 2008, Budde, Machado et al. 2015). It is clear that human distress does trigger a stress response in dogs, especially where there is a close social bond, and that dogs will respond in human-oriented ways to reduce their own levels of distress. This increases the likelihood that humans experiencing negative affective states are likely to observe behaviours in their dogs that are typically associated with distress, and interpreted as indicators of pain.

Play behaviour audience effect This could be significant, if an accepted indicator of a dog’s welfare such as play may be mediated by the attentional state of the human observer. If a human observer is not providing opportunities for safe play due to uncertainty around how much play is safe for dogs that are believed to be in pain, they are less likely to observe playful episodes. The data on human-directed social referencing by dogs suggests the important role of positive human behaviour and affective cues in mediating how dogs adapt to novel situations.

Dogs have a capacity for recognising human affective information, and using it for social referencing. Dogs learn by association and will begin to avoid or appease sad/angry human faces. Dogs will also use human vocal intonation, facial expressions and approach behaviour to evaluate the safety of a novel situation and mediate their exploratory behaviour, often showing a stronger response to human referential cues than more salient sensory or physical cues. Dogs also tend to experience inconsistent or novel human behaviour, without affective context, as aversive. This clearly demonstrates that the way in which human affect drives their own behaviour in a particular context will have a direct effect on the way that dogs perceive a novel experience. The way in which humans respond to the behaviour of dogs may influence the perceived affiliative responses by the dog towards the human, as dogs appear to prefer humans who synchronise their behaviour with them. When a dog is experiencing a painful episode, owners often change their behaviour towards the dog, usually restricting their activity and sharing fewer activities with them. This change from familiar to unfamiliar human behaviour is likely to be confusing for the dog, but will also limit the opportunities for human-dog behavioural synchronisation – like going for walks or playing – which may adversely affect the human-dog attachment bond and create social stress.

This has implications for pain intervention programmes, which regularly require dogs to learn interact with unfamiliar equipment, and learn novel movement patterns. If an owner expresses uncertainty or negativity in such situations, this may negatively impact the dog’s ability to adapt.

This highlights the need for owner involvement in rehabilitation programmes, in order to reduce stress associated with the process, especially where dogs have a close bond with the owner (trainer).

Owner personality affects dogs’ stress levels as well as stress-buffering capacity, and also affects their behaviour and cognitive function. Higher owner trait anxiety appears to be associated with higher anxiety-related behaviours in their dogs. This is possibly an effect induced by “pet-parenting style” such as over-protective behaviours and socialisation, rather than a function of emotional contagion. This is supported by data showing that owners scoring high in Neuroticism have stronger attachment bonds, and that this is actually correlated with lower baseline cortisol, demonstrating that strong human-dog attachment bonds can have a stress-buffering effect. However, these type of high attachment dyads tend to cope less well with novel tasks, and trigger higher levels of acute stress in dogs in situations where the owner is stressed, with the dogs showing lower cortisol variability. Consequently, these dyads have less capacity to adapt to stressful changes. Failure to adapt is likely to result in higher levels of pain-related functional disability, while chronic stress will have a direct effect on pain through increasing peripheral and central sensitisation, which can lead to neuropathic pain.

Owner and dog sex also appears to have an effect on human-dog emotional contagion. Dogs belonging to female owner demonstrate more person-oriented behaviours in response to human crying sounds. This may be a learnt response, as dogs belonging to women are more likely to have been regularly exposed to overt displays of sadness (Brebner 2003), and been rewarded for approach behaviour by social interaction such as petting. Female dogs appear to show greater sensitivity to owner stress as measured by heart rate, which correlates with sex differences observed in human responses to distress (Messina, Cattaneo et al. 2016). Female handler/female dog dyads show the greatest combined increase in salivary cortisol during a stressful task, suggesting an overall lower capacity to adapt to stress. Female dogs of female owners scoring high on Neuroticism are therefore most at risk not only of experiencing negative emotional contagion, but also of displaying behaviours consistent with distress and poor welfare. A dog with osteoarthritis in this type of dyad will be at greater risk of developing pain-related functional disability.

For any individual experiencing chronic osteoarthritis pain, their change in physical ability can be difficult to adapt to, and failure to adapt is the main cause of functional disability in these patients. If human emotions and behaviour have a mediating effect on dog behaviour by means of emotional contagion, this will have an affect the dog’s ability to adapt to new situations and experiences, such as chronic pain.

In this review, we wanted to explore emotional contagion in human-dog dyads, in order to better understand how this phenomenon may mediate the experience of chronic pain in dogs.

We conclude that human affective states do demonstrably influence the emotional experiences of dogs, which in turn are reflected in their behaviour and ability to adapt to novel situation and experiences. Negative human affective cues seem to have a greater impact on dogs’ behaviour than positive cues, and trigger behaviours in dogs that are both instinctive (automatic) as well as learnt. Dog behaviours associated with negative human affect are consistent with behaviours identified as signalling distress, such as avoidance, gazing and appeasement. As human caregivers of domestic dogs rely on behavioural observations to assess pain, this tendency of dogs to adapt behaviourally to negative human affect may have a biasing effect on evaluation of canine pain, which can potentially result become a negative feedback loop of canine distress behaviour and negative owner judgements.

This sensitivity to human affective states are mediated primarily by the strength of the attachment bond, but also owner personality and gender. The effects of emotional contagion in the human-dog dyad have neurobiological consequences, with direct effects on baseline cortisol, cortisol variability, heart rate variability and possibly oxytocin levels. These physiological factors are all implicated in the development of chronic pain (Vachon-Presseau, Roy et al. 2013, Tracy, Ioannou et al. 2016, Woda, Picard et al. 2016, Xin, Bai et al. 2017). Mimicry, a component of emotional contagion, as well as the recognition of emotionally valenced human facial expressions also differentially activates of the limbic system, and modifies the regulatory activity of the HPA axis, dysregulation of which is implicated the development of chronic pain (Blackburn-Munro and Blackburn-Munro 2003). It is therefore plausible that negative emotional contagion from human to dog can contribute to the experience of chronic pain in dogs through these adverse physiological effects.

Dogs are reliant on human referential information, both behavioural as well as affective, to inform their response to novel and frightening situations. This reliance becomes stronger as strength of attachment bonds and level of training (which likely also increases he attachment within the dyad) increases. It can be argued that pain is a novel, frightening experience for a dog. The relatively small size of the canine prefrontal cortex, compared to primate brains, does not allow for similar levels of cognitive control over lower-level automatic processes that mediate sensory analysis and memory storage (Miller, Freedman et al. 2002), and there is insufficient shared language between human and dogs to explain pain to dogs. Domestic dogs’ responses to the affective and behavioural cues by humans during their experience of pain, will influence their emotional response to the experience and their ability to adapt physiologically and cognitively. The effectiveness of their behavioural and physiological adaptation will have implications for the level of endogenous pain regulation as well as the level of functional disability experienced.

Certain human-dog dyads will be at greater risk of having an amplified aversive response and long-term failure to adapt, and therefore functional disability. It appears that dogs belonging to female owners, especially individuals with high trait-anxiety and Neuroticism, may be at greater risk of experiencing a greater overall negative adaptive state. This risk could be even higher for female dogs in such dyads. Identifying human-dog dyads at risk during early pain interventions may be critical in reducing overall morbidity in dogs from chronic pain.

From this review, it is clear that, at least in domestic dog populations, any veterinary interventions aimed at managing pain cannot be completely effective without addressing dysfunction in the human-dog dyad, as the mediating effect of the human on canine physiological and cognitive functioning is significant. In order to reduce functional disability in canine chronic pain, interventions will need to include an assessment of the risk of negative bias in the dog owner, and provide for interventions that can address negative pain beliefs and poor self-efficacy in the human element of the dyad.

Ethical Approval

Ethical approval for the study was obtained from the Human research Ethics Committee of the Faculty of Health Sciences of the University of Cape Town: HREC REF 548/2022

Competing interests

The Authors of this paper have no competing interests.

Authors' contributions

Ms AM van der Walt is the primary researcher, and Prof R Parker was the second reviewer of the data.

Funding

No funding was received for this study.

Availability of data and materials

The data used in this review can be requested from the corresponding author.

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No competing interests reported.

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Emotional contagion in the human/dog dyad - physiological and cognitive consequences, and implications for pain management: A scoping review

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Introduction

Methods

Results

Yawn Contagion

Mimicry

Behavioural response to human facial and auditory emotional cues

Behavioural responses to human displays of stress/distress

Brain activation

Heart rate variability (HRV)

Cortisol

Oxytocin

Human-directed social referencing

Owner stress, dog stress and environmental adaptation

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