Investigating putative depression-like states in the domestic dog: Does greater time spent displaying waking inactivity in the home kennel co-vary with negative judgment of ambiguity?
Introduction
Captive and domestic animals are often described as inactive, with the implicit (e.g.Broom, 1998) or explicit implication that this reduced activity is a welfare problem (e.g.McPhee and Carlstead, 2010). On the other hand, compromised inactivity, such as sleep deprivation, is also a considerable welfare problem (Ferrara and De Gennaro, 2001). Inactivity has rarely been the focus of behavioural studies. Indeed, the affective states associated with greater (or suppressed inactivity) largely remain un-investigated in non-human animals (Fureix and Meagher, 2015). In this study, we focus on a specific form of inactivity; spending greater time awake but motionless (ABM) in the home environment, which, following a translational ‘from humans to animals’ rationale, has been hypothesised to reflect depression-like conditions in affected individuals (including horses, mice, dogs, non-human primates: reviewed in Fureix and Meagher, 2015).
In humans, clinical depression2 is a debilitating mood disorder diagnosed by the co-occurrence of affective, cognitive, behavioural and homeostatic symptoms, of which the two core features are a low, sad mood and anhedonia (World Health Organization WHO, 1994; American Psychiatric Association APA, 2013). Chronic stress plays a major role in triggering the disease, especially in vulnerable people with predisposing genetic factors and/or experience of aversive events during their early life (American Psychiatric Association APA, 2013; Hammen et al., 2009; Siegrist, 2008; Capsi et al., 2003). Cognitive changes are theorised to be involved in both the aetiology and maintenance of the illness. One such change is negative cognitive bias in processing information; e.g. judging ambiguity more negatively, paying more attention to, and remembering, negative information better (Beck, 1967; MacLeod and Byrne, 1996; Gotlib and Krasnoperova, 1998; Disner et al., 2011). Another cognitive feature of clinical depression is ‘learned helplessness’, where an individual comes to believe that desired outcomes are improbable and aversive outcomes likely, and no action on his/her part can alter this, and as such stops acting (Maier and Seligman, 1976; Abramson et al., 1978).
Importantly, clinically depressed people often show increased inactivity in various daily activities (Baker et al., 1971; APA, 2013), which includes a reduced engagement with doing activities they once enjoyed and chores that have to be done (Knowles, 1981), as well as decreased social (APA, 2013; Baker et al., 1971; Schelde, 1998) and physical activities (Lindwall et al., 2011; Seime and Vickers, 2006). There is evidence that spending greater time awake but motionless in the home environment is associated with signs of anhedonia in horses (Fureix et al., 2015) and ‘helpless’ responses in laboratory mice (Fureix et al., 2016), which reinforces the symptomatic similarities between human clinical depression and greater time spent displaying waking inactivity in animals. Moreover, exposure to chronic stress and/or traumatic events appears to trigger both waking inactivity in animals, at least in some individuals (e.g. mice: Tilly et al., 2010; Fureix et al., 2016; dogs: Fox, 1968; Seligman and Altenor, 1980) and human clinical depression, particularly in vulnerable people (APA, 2013; Hammen et al., 2009; Siegrist, 2008; Capsi et al., 2003).
The current study aims to test the hypothesis that elevated levels of waking inactivity in the home environment, in tandem with exposure to chronic stress and/or traumatic events, could reflect a depression-like condition in the domestic dog. Pet dogs can indeed become highly inactive and unresponsive when exposed to traumatic events, such as when deprived of their owners or after the loss of a social companion (Fox, 1968). This state is commonly referred to as the dog being ‘depressed’ or showing ‘depressive like behaviour’ (e.g.Konok et al., 2015; Yeates, 2016; Gosling et al., 2003), although this remains to be empirically confirmed. Learned helplessness, one of the cognitive features of clinical depression, has been shown in dogs (Seligman and Altenor, 1980; Maier and Seligman, 1976), and is a phenomenon typically accompanied by an overall decrease in activity (e.g.Mineka and Hendersen, 1985). Moreover, kennelled dogs, such as those housed in research, working dog facilities or rescue shelters, can be exposed to an array of chronic stressors including minimal exercise, lack of positive social interactions, disrupted routines, high noise levels and a lack of control over their environment (Maier and Seligman, 1976; Part et al., 2014; Polgár et al., 2019; Willen et al., 2019; Cobb et al., 2019). For shelter dogs in particular, such situations could be exacerbated by the potentially traumatic abrupt loss of their previous owners, with whom they may have formed strong attachments (Fox, 1968; Willen et al., 2019). Because the aetiology of human depression emphasises aversive life events and chronic stress as common triggers, and because of the chronic stressors and potential traumatic events dogs in rescue shelters are exposed to, we therefore propose that shelter dogs are a suitable model for testing the hypothesis that greater time spent displaying waking inactivity could reflect a depression-like condition in domestic dogs.
We evaluated this hypothesis in shelter dogs by testing for an association between greater time spent inactive ‘awake but motionless’ in the home-pen and a core symptom of human clinical depression; a low, sad mood (APA, 2013), using negative judgment of ambiguity as a proxy. Negative cognitive biases in processing information can be displayed by people reporting negative affect; including clinical depression; e.g. in the form of making more negative judgment about ambiguous events and stimuli (reviewed in Paul et al., 2005). Similar affect-related biases in judging ambiguity have also been evidenced in non-human animals (Mendl et al., 2009; Gygax, 2014; Paul et al., 2005; Pryce and Seifritz, 2011; Mendl et al., 2010b), including in dogs (Mendl et al., 2010a; ;, 2010b), hence the use of this cognitive measure as a proxy of affective states. We used an established paradigm commonly used to assess judgment cognitive bias in dogs (Kis et al., 2015; Mendl et al., 2010a, 2010b), and we predicted that the dogs spending greater time inactive ‘awake but motionless’ in their home-pen would display the least positive judgment of ambiguity.
Section snippets
Ethics
The University of Bristol Animal Welfare Ethical Review Board approved the study in January 2016 (UB/15/072), and the study complied with the Animals (Scientific Procedures) Act 1986, EU directive 2010/63/EU and UK Home Office code of practice. The Head of Companion Animals Department, the Chief Veterinary Officer and the Chief Scientific Officer granted permission to approach RSPCA shelters in July 2016. Dog husbandry and care were under the management of the shelter staff.
Subjects
Subjects were 20
Awake but motionless (ABM) data
Being awake but motionless was displayed for a median time of 2.8% of the scans (1st quartile: 0.75%, third quartile: 4.75%), with clear variation between individual dogs (from 0 to 20.4% of scans).
Number of trials required to reach learning criterion in the cognitive judgment bias test (training phase)
The mean number of training trials taken to reach learning criterion in the cognitive judgment bias test was 43 (SD ± 18, median 43.5), with considerable individual variation (from 12 to 83 trials). There was a significant difference in time taken to reach learning criterion according to the origin
Discussion
This study aimed to test the hypothesis that greater time spent displaying waking inactivity in the home environment could reflect a depression-like condition in kennelled domestic dogs. We tested this hypothesis in shelter dogs by investigating the association between greater time spent inactive ‘awake but motionless’ in the home-pen (ABM) and negative judgment of ambiguity (a proxy for low mood, e.g.Mendl et al., 2009; Gygax, 2014; Paul et al., 2005; Pryce and Seifritz, 2011). Results show
Conclusions
This study aimed to test the hypothesis that greater time spent displaying waking inactivity in the home environment could reflect a depression-like condition in domestic dogs. We tested this hypothesis in shelter dogs by investigating the association between greater time spent inactive ‘awake but motionless’ in the home-pen and negative judgment of ambiguity (a proxy for low mood, a core symptom of human clinical depression). Results incidentally demonstrated an effect of the dog’s origin on
Declaration of Competing Interest
We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.
Acknowledgments
The authors are grateful to Sandra Vuillermet (and her invaluable patience) and Dr Giuliana Miguel-Pacheco for their help in extracting the data from footage; to Ilana Kelland for her help with data collection during the pilot study; to Olivier Friard and Marco Gamba for their free open-source BORIS software; and to one anonymous reviewer for his/her constructive comments on the manuscript. Naomi D. Harvey would also like to thank Professor Francoise Wemelsfelder for her time in training her in
References (71)
- et al.
Depressive disease - Classification and clinical characteristics
Compr. Psychiatry
(1971) - et al.
Responses of shelter and pet dogs to an unknown human
J. Vet. Behav. Clin. Appl. Res.
(2010) - et al.
Heart rate variability and saliva cortisol assessment in shelter dog: Human– animal interaction effects
Appl. Anim. Behav. Sci.
(2010) Welfare, stress, and the evolution of feelings
Stress and Behavior Advances in the Study of Behavior
(1998)Do dogs show an optimistic or pessimistic attitude to life?: A review of studies using the’ cognitive bias’ paradigm to assess dog welfare
- et al.
A spatial judgement task to determine background emotional state in laboratory rats, Rattus norvegicus
Anim. Behav.
(2008) - et al.
Using judgement bias to measure positive affective state in dogs
Appl. Anim. Behav. Sci.
(2011) - et al.
How much sleep do we need?
Sleep Med. Rev.
(2001) - et al.
What can inactivity reveal about affective states in non-humans? A review
Appl. Anim. Behav. Sci.
(2015) - et al.
Investigating anhedonia in a non-conventional species: do some riding horses Equus caballusdisplay symptoms of depression?
Appl. Anim. Behav. Sci.
(2015)
Stereotypic behaviour in standard non-enriched cages is an alternative to depression-like responses in C57BL/6 mice
Behav. Brain Res.
Biased information processing as a vulnerability factor for depression
Behav. Ther.
The A to Z of statistics for testing cognitive judgement bias
Anim. Behav.
Oxytocin induces positive expectations about ambivalent stimuli (cognitive bias) in dogs
Horm. Behav.
Higher dopamine release induced by less rather than more preferred reward during a working memory task in the primate prefrontal cortex
Behav. Brain Res.
Food-related aggression in shelter dogs: A comparison of behavior identified by a behavior evaluation in the shelter and owner reports after adoption
Appl. Anim. Behav. Sci.
Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms
Appl. Anim. Behav. Sci.
Physiological, physical and behavioural changes in dogs (Canis familiaris) when kennelled: Testing the validity of stress parameters
Physiol. Behav.
Measuring emotional processes in animals: the utility of a cognitive approach
Neurosci. Biobehav. Rev.
Assessing the welfare of kennelled dogs—a review of animal-based measures
Appl. Anim. Behav. Sci.
A translational research framework for enhanced validity of mouse models of psychopathological states in depression
Psychoneuroendocrinology
Reinforcer effectiveness in dogs -The influence of quantity and quality
Appl. Anim. Behav. Sci.
Cognitive bias in the chick anxiety–depression model
Brain Res.
Part II: learned helplessness
Behav. Res. Ther.
Middle-aged mice with enrichment-resistant stereotypic behaviour show reduced motivation for enrichment
Anim. Behav.
Cross sectional study comparing behavioural, cognitive and physiological indicators of welfare between short and long term kennelled domestic dogs
Appl. Anim. Behav. Sci.
Wolves outperform dogs in following human social cues
Anim. Behav.
The performance of stray dogs (Canis familiaris) living in a shelter on human-guided object-choice tasks
Anim. Behav.
Enrichment centered on human interaction moderates fear-induced aggression and increases positive expectancy in fearful shelter dogs
Appl. Anim. Behav. Sci.
Quality of life and animal behaviour
Appl. Anim. Behav. Sci.
Learned helplessness in humans - critique and reformulation
J. Abnorm. Psychol.
Diagnostic and Statistical Manual of Mental Disorders
Depression: Clinical, experimental and theoretical aspects
Incentive contrast in domestic dogs (Canis familiaris)
J. Comp. Psychol.
Cited by (10)
What can associations between emotional states and management-based measures teach us about shelter dogs’ welfare?
2023, Journal of Veterinary BehaviorNegative expectations and vulnerability to stressors in animals
2021, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Other studies have reported no relationship between negative expectations and other behavioural changes believed to reflect depressive-like states. For instance, Harvey et al. (2020) found no relationship in dogs between the time spent awake but motionless and negative expectations. The authors suggested that their findings may be explained by methodological issues with the judgment bias task (i.e., very little variation observed with most dogs being optimistic).
The effect of repeated testing on judgement bias in domestic dogs (Canis familiaris)
2023, Animal CognitionPreliminary validation of a novel tool to assess dog welfare: The Animal Welfare Assessment Grid
2022, Frontiers in Veterinary Science
- 1
Present address: Royal Canin Research Centre, 30470 Aimargues. France.