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?

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Highlights

  • This study aimed to test whether greater time spent displaying waking inactivity could reflect a depression-like condition in domestic dogs.

  • We tested whether shelter dogs that spent more time ‘awake but motionless’ in the home-pen would also show negative judgment of ambiguity.

  • Stray dogs completed training for the judgement bias task quicker than dogs from other origins, but all dogs exhibited highly positive judgements.

  • As such, there were no associations between time spent ‘awake but motionless’ and the dogs’ judgement of ambiguity.

  • We discuss why such ‘optimism’ may have been (e.g. sensitivity to access stimulation, probe test trial numbers) & further research directions.

Abstract

Exposure to chronic stressors and/or traumatic events can trigger depression-like forms of waking inactivity in non-human species (mice, horses, primates) as well as clinical depression in humans. This study aimed 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. We tested this hypothesis in shelter dogs by investigating the association between greater time spent inactive ‘awake but motionless’ (ABM) in the home-pen and a core symptom of human clinical depression; low mood, using negative judgment of ambiguity as a proxy. Subjects were 20 dogs from across three shelters (10F:10 M, aged 3.8 years ± SD 2.0; 45% seized as part of legal cases, 30% found as strays, 25% relinquished to the shelters). Time spent ABM was determined from 6 h of video per dog (one daily 2-h period recorded across three consecutive days, following a day and time period blocked design). To measure judgment of ambiguity, dogs were trained in a location discrimination task that a bowl either contained food (positive location) or was empty (negative location). Dogs were tested with one negative, one positive, and one ambiguous (equidistant to the two training positions) trial. Negative judgment of ambiguity manifests as longer latencies to reach the ambiguous bowl. We created a positive expectancy score by adjusting the latency in the ambiguous trial to the latency to approach the negative and positive locations (higher scores indicating bias towards expecting more positive outcomes). Time spent ABM was compared against positive expectancy scores using a multivariable GLM. Dogs were ABM for a median of 2.8% of the scans (Q1: 0.75%, Q3: 4.75), with clear inter-individual variation (0–20.4%). In the cognitive judgment bias, stray dogs reached the learning criterion faster than those of other origins (ANOVA: F19 = 4.03, p = 0.037; Kaplan-Meier survival analyses, Chi22 = 7.88, p = 0.019). During the test trials, all latencies statistically differed from each other (Negative > Ambiguous > Positive, Friedman test Chi-square(2) = 33.90, p = <0.001). Cognitive expectancy scores however exhibited minimal variation and an exaggerated right-skew distribution, showing a strong bias towards expecting a positive outcome at the ambiguous location in most of the dogs, and showed no association (p> 0.05) with time spent ABM, therefore the hypothesis was not supported. We discuss reasons for observing such general ‘optimistic’ tendencies in this study, as well as further research directions.

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

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      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).

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    1

    Present address: Royal Canin Research Centre, 30470 Aimargues. France.

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