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.

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.

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.

Characterization of Phages YuuY, KaiHaiDragon, and OneinaGillian Isolated from Microbacterium foliorum.

Microbacterium foliorum is a Gram-positive bacteria found in organic matter. Three lytic bacteriophages, KaiHaiDragon, OneinaGillian, and YuuY, were isolated from M. foliorum strain NRRL B-24224. Phage YuuY in particular expresses a broad host range as it possesses the ability to infect closely related bacterial species Microbacterium aerolatum at a high plating efficiency. Characterization tests were performed on all three Microbacterium phage to assess morphology, genomic characteristics, pH and thermal stabilities, life cycle, and the type of receptor used for infection. All three phages showed similar pH stability, ranging from pH 5-11, except for KaiHaiDragon, which had a reduced infection effectiveness at a pH of 11. YuuY possessed a significantly higher temperature tolerance compared to the other Microbacterium phages as some phage particles remained viable after incubation temperatures of up to 80 °C. Based on the one-step growth curve assay, all three Microbacterium phages possessed a relatively short latent period of 90 min and an approximately two-fold burst size factor. Moreover, all three phages utilize a carbohydrate receptor to initiate infection. Based on bioinformatics analysis, YuuY, KaiHaiDragon and OneinaGillian were assigned to clusters EA10, EC, and EG, respectively.

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.

State-dependent judgement bias in Drosophila: evidence for evolutionarily primitive affective processes.

Affective states influence decision-making under ambiguity in humans and other animals. Individuals in a negative state tend to interpret ambiguous cues more negatively than individuals in a positive state. We demonstrate that the fruit fly, Drosophila melanogaster, also exhibits state-dependent changes in cue interpretation. Drosophila were trained on a Go/Go task to approach a positive (P) odour associated with a sugar reward and actively avoid a negative (N) odour associated with shock. Trained flies were then either shaken to induce a purported negative state or left undisturbed (control), and given a choice between: air or P; air or N; air or ambiguous odour (1 : 1 blend of P : N). Shaken flies were significantly less likely to approach the ambiguous odour than control flies. This 'judgement bias' may be mediated by changes in neural activity that reflect evolutionarily primitive affective states. We cannot say whether such states are consciously experienced, but use of this model organism's versatile experimental tool kit may facilitate elucidation of their neural and genetic basis.

Animal emotion: Descriptive and prescriptive definitions and their implications for a comparative perspective.

In recent years there has been a growing research interest in the field of animal emotion. But there is still little agreement about whether and how the word "emotion" should be defined for use in the context of non-human species. Here, we make a distinction between descriptive and prescriptive definitions. Descriptive definitions delineate the ways in which the word emotion is used in everyday life. Prescriptive definitions are used to pick out the set of events that scientific theories of emotion purport to explain. Picking out three prescriptive definitions, we show that the different ways in which emotions are defined correspond to processes that are distributed differentially across the animal kingdom. We propose that these definitions provide a useful starting point for investigating the varying emotional capacities of a wide range of animals, providing a basis for a new, comparative science of emotion.

Examining affective structure in chickens: valence, intensity, persistence and generalization measured using a Conditioned Place Preference Test.

When measuring animals' valenced behavioural responses to stimuli, the Conditioned Place Preference (CPP) test goes a step further than many approach-based and avoidance-based tests by establishing whether a learned preference for, or aversion to, the location in which the stimulus was encountered can be generated. We designed a novel, four-chambered CPP test to extend the capability of the usual CPP paradigm to provide information on four key features of animals' affective responses: valence, scale, persistence and generalization. Using this test, we investigated the affective responses of domestic chickens (Gallus gallus domesticus) to four potentially aversive stimuli: 1. Puffs of air; 2. Sight of (robotic) snake; 3. Sprays of water; 4. Sound of conspecific alarm calls. We found conditioned avoidance of locations associated with the air puffs and water sprays (Friedman's χ2 (3) = 13.323 p > .005; χ2 (3) = 14.235 p > .005), but not with the snake and alarm calls. The scale of the learned avoidance was similar for the air puff and water spray stimuli, but persistence and generalization differed. We conclude that the four chambered CPP test can have a valuable role to play in making multi-feature measurements of stimulus-generated affective responses, and we highlight the value of such measurements for improving our understanding of the structure of affect in chickens and other animals.

Exploring the similarities between risk factors triggering depression in humans and elevated in-cage "inactive but awake" behavior in laboratory mice.

Introduction: Depression is a human mental disorder that can also be inferred in non-human animals. This study explored whether time spent inactive but awake ("IBA") in the home-cage in mice was further triggered by risk factors similar to those increasing vulnerability to depression in humans (early life stress, genetic predispositions, adulthood stress). Methods: Eighteen DBA/2 J and 18 C57BL/6 J females were tested, of which half underwent as pups a daily maternal separation on post-natal days 2-14 (early-life stress "ELS") (other half left undisturbed). To assess the effect of the procedure, the time the dams from which the 18 subjects were born spent active in the nest (proxy for maternal behavior) was recorded on post-natal days 2, 6, 10 and 14 for 1 h before separation and following reunion (matched times for controls), using live instantaneous scan sampling (total: 96 scans/dam). For each ELS condition, about half of the pups were housed post-weaning (i.e., from 27 days old on average) in either barren (triggering IBA and depression-like symptoms) or larger, highly enriched cages (n = 4-5 per group). Time mice spent IBA post-weaning was observed blind to ELS treatment using live instantaneous scan sampling in two daily 90-min blocks, two days/week, for 6 weeks (total: 192 scans/mouse). Data were analyzed in R using generalized linear mixed models. Results: The dams were significantly more active in the nest over time (p = 0.016), however with no significant difference between strains (p = 0.18), ELS conditions (p = 0.20) and before/after separation (p = 0.83). As predicted, post-weaning barren cages triggered significantly more time spent IBA in mice than enriched cages (p < 0.0001). However, neither ELS (p = 0.4) nor strain (p = 0.84) significantly influenced time mice spent IBA, with no significant interaction with environmental condition (ELS × environment: p = 0.2861; strain × environment: p = 0.5713). Discussion: Our results therefore only partly support the hypothesis that greater time spent IBA in mice is triggered by risk factors for human depression. We discuss possible explanations for this and further research directions.

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.

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.

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.

Do greater levels of in-cage waking inactivity in laboratory mice reflect a spontaneous depression-like symptom? A pharmacological investigation.

We previously identified in laboratory mice an inactive state [being awake with eyes open motionless within the home cage; inactive but awake, 'IBA'] sharing etiological factors and symptoms with human clinical depression. We further test the hypothesis that greater time spent displaying IBA indicates a depression-like state in mice by investigating whether the antidepressant Venlafaxine, environmental enrichment, and their combination, alleviate IBA. Seventy-two C57BL/6J and 72 DBA/2J female mice were pseudo-randomly housed post-weaning in mixed strain-pairs in non-enriched (NE; 48 pairs) or in environmentally enriched (EE; 24 pairs) cages. After 34 days, half of the mice housed in NE cages were either relocated to EE cages or left in NE cages. For each of these conditions, half of the mice drank either a placebo or the antidepressant Venlafaxine (10 mg/kg). The 48 mice housed in EE cages were all relocated to NE cages and allocated to either the placebo (n = 24) or Venlafaxine (n = 24). IBA data were collected prior to and after environmental adjustment by trained observers blind to the pharmacological and environmental adjustment treatments. Data were analyzed using GLM models. NE cages triggered more IBA than EE cages (Likelihood-Ratio-Test Chi23 = 53.501, p < 0.0001). Venlafaxine and environmental enrichment appeared equally effective at reducing IBA (LRT Chi23 = 18.262, p < 0.001), and combining these approaches did not magnify their effects. Enrichment removal triggered IBA increase (LRT Chi21 = 23.050, p < 0.001), but Venlafaxine did not overcome the increase in IBA resulting from enrichment loss (LTR Chi21 = 0.081, p = 0.775). Theoretical implications for putative depression-like states in mice, and further research directions, are discussed.

Decision-making under uncertainty: biases and Bayesians.

Animals (including humans) often face circumstances in which the best choice of action is not certain. Environmental cues may be ambiguous, and choices may be risky. This paper reviews the theoretical side of decision-making under uncertainty, particularly with regard to unknown risk (ambiguity). We use simple models to show that, irrespective of pay-offs, whether it is optimal to bias probability estimates depends upon how those estimates have been generated. In particular, if estimates have been calculated in a Bayesian framework with a sensible prior, it is best to use unbiased estimates. We review the extent of evidence for and against viewing animals (including humans) as Bayesian decision-makers. We pay particular attention to the Ellsberg Paradox, a classic result from experimental economics, in which human subjects appear to deviate from optimal decision-making by demonstrating an apparent aversion to ambiguity in a choice between two options with equal expected rewards. The paradox initially seems to be an example where decision-making estimates are biased relative to the Bayesian optimum. We discuss the extent to which the Bayesian paradigm might be applied to the evolution of decision-makers and how the Ellsberg Paradox may, with a deeper understanding, be resolved.

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.

An integrative and functional framework for the study of animal emotion and mood.

A better understanding of animal emotion is an important goal in disciplines ranging from neuroscience to animal welfare science. The conscious experience of emotion cannot be assessed directly, but neural, behavioural and physiological indicators of emotion can be measured. Researchers have used these measures to characterize how animals respond to situations assumed to induce discrete emotional states (e.g. fear). While advancing our understanding of specific emotions, this discrete emotion approach lacks an overarching framework that can incorporate and integrate the wide range of possible emotional states. Dimensional approaches that conceptualize emotions in terms of universal core affective characteristics (e.g. valence (positivity versus negativity) and arousal) can provide such a framework. Here, we bring together discrete and dimensional approaches to: (i) offer a structure for integrating different discrete emotions that provides a functional perspective on the adaptive value of emotional states, (ii) suggest how long-term mood states arise from short-term discrete emotions, how they also influence these discrete emotions through a bi-directional relationship and how they may function to guide decision-making, and (iii) generate novel hypothesis-driven measures of animal emotion and mood.

Animal affect and decision-making.

The scientific study of animal affect (emotion) is an area of growing interest. Whilst research on mechanism and causation has predominated, the study of function is less advanced. This is not due to a lack of hypotheses; in both humans and animals, affective states are frequently proposed to play a pivotal role in coordinating adaptive responses and decisions. However, exactly how they might do this (what processes might implement this function) is often left rather vague. Here we propose a framework for integrating animal affect and decision-making that is couched in modern decision theory and employs an operational definition that aligns with dimensional concepts of core affect and renders animal affect empirically tractable. We develop a model of how core affect, including short-term (emotion-like) and longer-term (mood-like) states, influence decision-making via processes that we label affective options, affective predictions, and affective outcomes and which correspond to similar concepts in schema of the links between human emotion and decision-making. Our framework is generalisable across species and generates questions for future research.

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.

Towards a comparative science of emotion: Affect and consciousness in humans and animals.

The componential view of human emotion recognises that affective states comprise conscious, behavioural, physiological, neural and cognitive elements. Although many animals display bodily and behavioural changes consistent with the occurrence of affective states similar to those seen in humans, the question of whether and in which species these are accompanied by conscious experiences remains controversial. Finding scientifically valid methods for investigating markers for the subjective component of affect in both humans and animals is central to developing a comparative understanding of the processes and mechanisms of affect and its evolution and distribution across taxonomic groups, to our understanding of animal welfare, and to the development of animal models of affective disorders. Here, contemporary evidence indicating potential markers of conscious processing in animals is reviewed, with a view to extending this search to include markers of conscious affective processing. We do this by combining animal-focused approaches with investigations of the components of conscious and non-conscious emotional processing in humans, and neuropsychological research into the structure and functions of conscious emotions.