A primer on the use of computational modelling to investigate affective states, affective disorders and animal welfare in non-human animals.

Objective measures of animal emotion-like and mood-like states are essential for preclinical studies of affective disorders and for assessing the welfare of laboratory and other animals. However, the development and validation of measures of these affective states poses a challenge partly because the relationships between affect and its behavioural, physiological and cognitive signatures are complex. Here, we suggest that the crisp characterisations offered by computational modelling of the underlying, but unobservable, processes that mediate these signatures should provide better insights. Although this computational psychiatry approach has been widely used in human research in both health and disease, translational computational psychiatry studies remain few and far between. We explain how building computational models with data from animal studies could play a pivotal role in furthering our understanding of the aetiology of affective disorders, associated affective states and the likely underlying cognitive processes involved. We end by outlining the basic steps involved in a simple computational analysis.

A mapping review of refinements to laboratory rat housing and husbandry.

Refining the housing and husbandry of laboratory rats is an important goal, both for ethical reasons and to allow better quality research. We conducted a mapping review of 1,017 studies investigating potential refinements of housing and husbandry of the laboratory rat to assess what refinements have, and have not, been studied, and to briefly assess whether there is evidence to support any impact on rat welfare. Among the many refinements studied, the majority involve changes to the cage, but some also involve alterations to the wider environment. The effects of these refinements were assessed using a range of readouts, many of which are difficult to interpret from a welfare perspective. Preference studies, which are easier to interpret, provide evidence that rats prefer complex environments, including shelters and multiple objects, which offer different areas/resources allowing the rat to engage in diverse behaviors. The reporting of methodology in papers was often poor, indicating that studies were potentially subject to biases. Given that many refinements co-occurred, it was often difficult to tease apart which ones were most beneficial for rat welfare. Effects of refinements were also moderated by a number of factors including age, sex, strain and photoperiod. Altogether our findings show that a one-size-fits-all approach to refinements is not appropriate, because different refinements will impact different rats in different ways. Our review has also produced a database of >1,000 articles that can be used for further and more detailed analyses. Our findings have also highlighted areas where future research is likely to be valuable, including refinements to rat transport, handling and the use of training.

Developing guidelines for pet rat housing through expert consultation.

BACKGROUND: Pet care guidelines play an important role in ensuring that owners are well informed about good husbandry practices, allowing them to provide the best care for their animals. However, the development of such guidelines is difficult when there is little appropriate empirical evidence on which to base guidelines, as in the case of pet rats. The consultation of multiple experts can help to surmount this challenge. METHODS: We developed a set of guidelines for pet rat housing by consulting with a group of experts, including veterinarians, veterinary nurses, animal welfare scientists and experienced pet rat owners. The consultation involved two rounds of online surveys (n = 13) and one online discussion (n = 8). RESULTS: The resulting guidelines cover a broad range of features within pet rat housing, including injury prevention, details of suitable refuges and substrates, and suitable cage sizing. The guidelines may evolve as more information about pet rats comes to light but may nonetheless provide a useful starting point for any future guidelines. CONCLUSIONS: At present, these guidelines may not only be useful for pet rat owners and those advising pet rat owners, such as veterinarians, but may also be useful in the design of housing, including for laboratory rodents.

Are Brachycephalic Dogs Really Cute? Evidence from Online Descriptions.

Brachycephalic dog breeds have become increasingly popular in recent years, despite showing a high incidence of conformation-related disorders and early mortality. It has been suggested that this popularity might be explained by public perceptions of these short-muzzled dogs as looking particularly infant-like or "cute." Here, the hypothesis that short-muzzled breeds are especially likely to be described as cute was investigated by analyzing the word contents of advertisements for dogs and puppies being sold online. The ages and breeds of dogs being advertised were considered, in addition to whether the text of each advertisement included the word "cute" or two associated words: "adorable" and "sweet." Analyses of the entire sample of advertisements (n = 43,312) indicated that younger dogs were more likely to be advertised as "cute" and "adorable," while older ones were more likely to be advertised as "sweet." Shortmuzzled, brachycephalic breeds (cranio-facial ratio < 0.5) were more likely to be advertised as "cute," with brachycephalic puppies under 6 months of age being particularly likely to be called "cute" and also "adorable." However, breed size had a larger and wider effect on word use in advertisements, with smaller dogs being advertised more frequently using all three words: "cute," "adorable," and "sweet." When data for adult dogs only were considered (n = 11,400), and continuous muzzle shortening and age data were used, a somewhat different and more complex pattern of results were found. Use of the words "cute" and "adorable" were not associated with degree of muzzle shortening among these adult dogs, but "sweet" was used more often in advertisements for longer-muzzled breeds. We conclude that the present dataset provides partial support for the assertion that short-muzzled dogs are described as more "cute" than longer-muzzled ones, but that small size is a better predictor of the use of "cute" and its synonyms.

That brachycephalic look: Infant-like facial appearance in short-muzzled dog breeds.

Brachycephalic dog breeds are highly popular, yet their conformation-related disorders represent a major welfare concern. It has been suggested that the current popularity of such breeds can be explained by their cute, infant-like facial appearances. The concept of 'kindchenschema' refers to the observation that certain physical features of infant humans and other animals can automatically stimulate positive and nurturant feelings in adult observers. But the proposal that brachycephalic dogs possess heightened 'kindchenschema' facial features, even into adulthood, has never been formally investigated. Here, we hypothesised that relative muzzle shortening across a range of breeds would be associated with known 'kindchenschema' facial features, including a relatively larger forehead, larger eyes and smaller nose. Relative fronto-facial feature sizes in exemplar photographs of adult dogs from 42 popular breeds were measured and associated with existing data on the relative muzzle length and height-at-withers of the same breeds. Our results show that, in adulthood, shorter-muzzled breeds have relatively larger (taller) foreheads and relatively larger eyes (i.e. area of exposed eyeball relative to overall face area) than longer-muzzled breeds, and that this effect is independent of breed size. In sum, brachycephalic dog breeds do show exaggeration of some, but not all, known fronto-facial 'kindchenschema' features, and this may well contribute to their apparently cute appearance and to their current popularity as companion animals. We conclude that the challenge of addressing conformation-related disorders in companion dogs needs to take account of the cute, 'kindchenschema' looks that many owners are likely to be attracted to.

Bridging the Gap: Human Emotions and Animal Emotions.

Our experiences of the conscious mental states that we call emotions drive our interest in whether such states also exist in other animals. Because linguistic report can be used as a gold standard (albeit indirect) indicator of subjective emotional feelings in humans but not other species, how can we investigate animal emotions and what exactly do we mean when we use this term? Linguistic reports of human emotion give rise to emotion concepts (discrete emotions; dimensional models), associated objectively measurable behavioral and bodily emotion indicators, and understanding of the emotion contexts that generate specific states. We argue that many animal studies implicitly translate human emotion concepts, indicators and contexts, but that explicit consideration of the underlying pathways of inference, their theoretical basis, assumptions, and pitfalls, and how they relate to conscious emotional feelings, is needed to provide greater clarity and less confusion in the conceptualization and scientific study of animal emotion.

Online Dog Sale Advertisements Indicate Popularity of Welfare-Compromised Breeds.

Kennel club registrations have been used in a number of studies to estimate ownership levels and fashion trends among dog breeds. They cannot, however, give a complete overview of the contemporary trade in pet dogs, and additionally, may be particularly poor at monitoring trends among some welfare-vulnerable breeds. Here, we compared data from online advertisements for the UK sales of single-breed dogs over an 18-month period, with equivalent data (including for prior and subsequent years) from the UK Kennel Club. Kennel Club registration rates and breed popularity rates online were positively correlated. However, some breeds, including the Jack Russell terrier, Border collie and Chihuahua were considerably over-represented in online advertisements when compared with Kennel Club registrations, indicating a hidden market for certain breeds. In addition, the online dataset provided information on the sale and re-homing of adult dogs, showing high rates of adult homing of the Staffordshire bull terrier, Siberian husky and Rottweiler. We conclude that online pet-sales websites are an important and complementary source of data about the market in, and popularity of, a wide range of dog breeds.

Effects of dehorning on population productivity in four Namibia sub-populations of black rhinoceros (Diceros bicornis bicornis).

The black rhinoceros (rhino) (Diceros bicornis) is critically endangered, with poaching being one of several threats to the species' survival. Many reserves across several countries, including Namibia, South Africa, and Zimbabwe, now dehorn their rhinos in an attempt to reduce poaching. Historical data collected by the Namibian Ministry of Environment, Forestry, and Tourism and Save the Rhino Trust were used to investigate whether dehorning has an effect on age at first reproduction (AFR), inter-calving interval (ICI), birth sex ratios, calf survival, cause of death, and lifespan. These were assessed in four Namibian sub-populations (hereafter referred to as 'populations') of black rhino (denoted A, B, C, and D) which have undergone varying levels of dehorning. No significant difference was found in any of the variables between dehorned and horned individuals. Population was a significant predictor of AFR (LRT = 7.433, p = 0.024) and ICI (LRT = 13.281, p = 0.004), although pairwise comparisons only found populations A and B to be significantly different (AFR: z = -2.736, p = 0.017, ICI: z = -3.705, p = 0.001). Additionally, a significantly higher number of males than females were born in population D (p = 0.021, CI = 0.544, 0.960). The main cause of death across all individuals was poaching, although there was no significant difference in the proportion of rhinos poached between dehorned and horned individuals (X 2 = 0.638, p = 0.424, n = 265). No evidence was found to suggest that dehorning has any effect on AFR, ICI, birth sex ratios, calf survival, or lifespan in the black rhino, which is reassuring in the continued use of dehorning as an anti-poaching technique in this species.

Evaluating Pain and Analgesia Effectiveness Following Routine Castration in Rabbits Using Behavior and Facial Expressions.

Prevention of pain in rabbits is a priority for both welfare and validity of scientific data. We aimed to determine if the rabbit grimace scale (RbtGS) could be used as a viable, rapid assessment tool in two breeds of rabbit, Dutch belted (DB) and New Zealand white (NZW), following orchidectomy, as an adjunct to behavioral analysis. All animals received analgesia. Rabbits were filmed and their behavior was recorded at multiple time points pre- and post-orchidectomy. Observers then scored specific pain associated behaviors for analysis. Time matched footage was also scored using the rabbit grimace scale (RbtGS). Following surgery, rabbits showed significant increases in the duration spent displaying key pain associated behaviors at 1 and 5 h post-surgery. DB rabbits that received low dose meloxicam (0.2 mg/kg) showed significantly more pain behaviors at 1 and 5 h post-surgery compared to those administered a combination of higher dose meloxicam (0.6 mg/kg) and a lidocaine/bupivacaine local infusion. DB rabbits showed an increase in RbtGS score at both 1 and 5 h post-surgery. In the NZW rabbits, an increase in RbtGS score was only observed at 1 h post-surgery. Using behavioral analysis as the gold standard for comparison, the RbtGS was an effective means of determining when rabbits are painful following orchidectomy. Higher dose meloxicam (0.6 mg/kg) combined with local anesthetic was a more effective method of reducing pain, compared to lower dose meloxicam (0.2 mg/kg) alone.

Using Primary Reinforcement to Enhance Translatability of a Human Affect and Decision-Making Judgment Bias Task.

Good translatability of behavioral measures of affect (emotion) between human and nonhuman animals is core to comparative studies. The judgment bias (JB) task, which measures "optimistic" and "pessimistic" decision-making under ambiguity as indicators of positive and negative affective valence, has been used in both human and nonhuman animals. However, one key disparity between human and nonhuman studies is that the former typically use secondary reinforcers (e.g., money) whereas the latter typically use primary reinforcers (e.g., food). To address this deficiency and shed further light on JB as a measure of affect, we developed a novel version of a JB task for humans using primary reinforcers. Data on decision-making and reported affective state during the JB task were analyzed using computational modeling. Overall, participants grasped the task well, and as anticipated, their reported affective valence correlated with trial-by-trial variation in offered volume of juice. In addition, previous findings from monetary versions of the task were replicated: More positive prediction errors were associated with more positive affective valence, a higher lapse rate was associated with lower affective arousal, and affective arousal decreased as a function of number of trials completed. There was no evidence that more positive valence was associated with greater "optimism," but instead, there was evidence that affective valence influenced the participants' decision stochasticity, whereas affective arousal tended to influence their propensity for errors. This novel version of the JB task provides a useful tool for investigation of the links between primary reward and punisher experience, affect, and decision-making, especially from a comparative perspective.

Pet rat welfare in the United Kingdom: The good, the bad and the ugly.

BACKGROUND: To date, despite the substantial literature investigating how rats prefer to be kept in captivity, no research has been conducted to assess the housing, husbandry and health of pet rats. METHODS: To better understand the United Kingdom's pet rat population and the welfare issues they face, we conducted an online survey of pet rat owners. The survey included questions about the owner and their opinions about pet rats, and about their rats' health, husbandry and housing. RESULTS: The results, from 677 complete responses, highlighted areas of rat care that were "good", "bad" and "ugly" (i.e. likely to be highly detrimental to welfare). The good was that many rats were provided with a social companion and enrichment; the bad was that we could not be certain whether rats had a sufficiently nutritious diet or sufficient opportunities to explore or adequate nesting substrate; and the ugly included cases of exposure of rats to predator species within the home and a generally high prevalence of disease. CONCLUSIONS: We conclude that there is much cause for concern about the welfare of pet rats in the United Kingdom.

Dissecting the links between reward and loss, decision-making, and self-reported affect using a computational approach.

Links between affective states and risk-taking are often characterised using summary statistics from serial decision-making tasks. However, our understanding of these links, and the utility of decision-making as a marker of affect, needs to accommodate the fact that ongoing (e.g., within-task) experience of rewarding and punishing decision outcomes may alter future decisions and affective states. To date, the interplay between affect, ongoing reward and punisher experience, and decision-making has received little detailed investigation. Here, we examined the relationships between reward and loss experience, affect, and decision-making in humans using a novel judgement bias task analysed with a novel computational model. We demonstrated the influence of within-task favourability on decision-making, with more risk-averse/'pessimistic' decisions following more positive previous outcomes and a greater current average earning rate. Additionally, individuals reporting more negative affect tended to exhibit greater risk-seeking decision-making, and, based on our model, estimated time more poorly. We also found that individuals reported more positive affective valence during periods of the task when prediction errors and offered decision outcomes were more positive. Our results thus provide new evidence that (short-term) within-task rewarding and punishing experiences determine both future decision-making and subjectively experienced affective states.

Reward and punisher experience alter rodent decision-making in a judgement bias task.

The influence of affective states on decision-making is likely to be complex. Negative states resulting from experience of punishing events have been hypothesised to generate enhanced expectations of future punishment and 'pessimistic'/risk-averse decisions. However, they may also influence how decision-outcomes are valued. Such influences may further depend on whether decisions at hand are germane to the rewards or punishers that induced the affective state in the first place. Here we attempt to dissect these influences by presenting either many or few rewards or punishers of different types (sucrose vs air-puff; 50 kHz vs 22 kHz ultrasonic vocalisations) to rats, and investigating their subsequent decisions in a judgement bias task that employed sucrose and air-puff as decision outcomes. Rats that received many sucrose pellets prior to testing were more risk-averse than those receiving many air-puffs. Ultrasonic vocalisations did not alter decision-making. Computational analysis revealed a higher weighting of punishers relative to rewards (in agreement with findings from a separate behavioural task) and a bias towards the risk-averse response following pre-test sucrose compared to pre-test air-puff. Thus, in this study reward and punisher manipulation of affective state appeared to alter decision-making by influencing both expectation and valuation of decision-outcomes in a domain-specific way.

Optimism, pessimism and judgement bias in animals: A systematic review and meta-analysis.

Just as happy people see the proverbial glass as half-full, 'optimistic' or 'pessimistic' responses to ambiguity might also reflect affective states in animals. Judgement bias tests, designed to measure these responses, are an increasingly popular way of assessing animal affect and there is now a substantial, but heterogeneous, literature on their use across different species, affect manipulations, and study designs. By conducting a systematic review and meta-analysis of 459 effect sizes from 71 studies of non-pharmacological affect manipulations on 22 non-human species, we show that animals in relatively better conditions, assumed to generate more positive affect, show more 'optimistic' judgements of ambiguity than those in relatively worse conditions. Overall effects are small when considering responses to all cues, but become more pronounced when non-ambiguous training cues are excluded from analyses or when focusing only on the most divergent responses between treatment groups. Task type (go/no-go; go/go active choice), training cue reinforcement (reward-punishment; reward-null; reward-reward) and sex of animals emerge as potential moderators of effect sizes in judgement bias tests.

Pharmacological manipulations of judgement bias: A systematic review and meta-analysis.

Validated measures of animal affect are crucial to research spanning numerous disciplines. Judgement bias, which assesses decision-making under ambiguity, is a promising measure of animal affect. One way of validating this measure is to administer drugs with affect-altering properties in humans to non-human animals and determine whether the predicted judgement biases are observed. We conducted a systematic review and meta-analysis using data from 20 published research articles that use this approach, from which 557 effect sizes were extracted. Pharmacological manipulations overall altered judgement bias at the probe cues as predicted. However, there were several moderating factors including the neurobiological target of the drug, whether the drug induced a relatively positive or negative affective state in humans, dosage, and the presented cue. This may partially reflect interference from adverse effects of the drug which should be considered when interpreting results. Thus, the overall pattern of change in animal judgement bias appears to reflect the affect-altering properties of drugs in humans, and hence may be a valuable measure of animal affective valence.

Rabbit relinquishment through online classified advertisements in the United Kingdom: when, why, and how many?

To identify implicit causes of companion rabbit relinquishment, this study investigated whether there was annual and seasonal variation in the number of advertisements and ages of rabbits posted as free or for sale on classified websites in the United Kingdom. The number of advertisements posted decreased from 2014 to 2016. There was an increase in the number of advertisements for free rabbits in winter compared with other seasons, which could be a result of caregivers' reduced willingness to interact with their rabbits and carry out husbandry during periods of inclement weather. Rabbits advertised as free were older than rabbits advertised for sale, and rabbits relinquished due to human-related reasons were older than those relinquished because of rabbit-related factors. It is recommended that further research is undertaken to elucidate whether providing education to prospective rabbit caregivers regarding the life span of rabbits and their substantial husbandry requirements, especially in winter, would deter the purchase of rabbits by caregivers unable or unwilling to care for them in the long term.

Author Correction: Assessing animal affect: an automated and self-initiated judgement bias task based on natural investigative behaviour.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Assessing animal affect: an automated and self-initiated judgement bias task based on natural investigative behaviour.

Scientific methods for assessing animal affect, especially affective valence (positivity or negativity), allow us to evaluate animal welfare and the effectiveness of 3Rs Refinements designed to improve wellbeing. Judgement bias tasks measure valence; however, task-training may be lengthy and/or require significant time from researchers. Here we develop an automated and self-initiated judgement bias task for rats which capitalises on their natural investigative behaviour. Rats insert their noses into a food trough to start trials. They then hear a tone and learn either to stay for 2 s to receive a food reward or to withdraw promptly to avoid an air-puff. Which contingency applies is signalled by two different tones. Judgement bias is measured by responses to intermediate ambiguous tones. In two experiments we show that rats learn the task in fewer sessions than other automated variants, generalise responses across ambiguous tones as expected, self-initiate 4-5 trials/min, and can be tested repeatedly. Affect manipulations generate main effect trends in the predicted directions, although not localised to ambiguous tones, so further construct validation is required. We also find that tone-reinforcer pairings and reinforcement or non-reinforcement of ambiguous trials can affect responses to ambiguity. This translatable task should facilitate more widespread uptake of judgement bias testing.

Dissociating the effects of alternative early-life feeding schedules on the development of adult depression-like phenotypes.

Early-life adversity is associated with increased vulnerability to depression in humans, and depression-like phenotypes in animals. However, different types of adverse experience may leave different signatures in adulthood. We experimentally manipulated the Amount of food delivered to European starling nestlings and the begging Effort required to obtain food during early development. Here, we report behavioural data in adulthood from a task that assessed sensitivity to shifts in reward magnitude characteristic of depression-like low mood. Birds that had experienced Hard Effort were more food motivated than birds that had experienced Easy Effort. Both Effort and Amount affected sensitivity to shifts in reward magnitude: Hard Effort birds showed an enhanced negative contrast effect following loss of reward ('disappointment'), and Lean Amount birds failed to show a normal positive contrast effect following gain in reward (a lack of 'elation'). Therefore, the feeding schedule experienced for just 10 days in early life caused enduring effects on feeding motivation and sensitivity to reward loss/gain consistent with human depression. Furthermore, the contrast effects were specific to different types of adversity. These results highlight the importance of early-life feeding schedules in the development of depression-like phenotypes.