Oliver Burman

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.

Dogs showing separation-related behaviour exhibit a ‘pessimistic’ cognitive bias

Summary Up to five million pet dogs in the UK (∼50% of the population) may, at some stage of their lives, perform undesirable separation-related behaviour (SRB) when left home alone [1], including vocalising, destruction and toileting [2]. Some owners perceive their dog to be ‘fine or even ‘happy when performing SRB [3], a few seek professional help [1], and others relinquish the dog [4]. Given the magnitude of the issue and the varied perceptions and behaviour of owners, the underlying emotional (affective) states of dogs showing SRB, and hence their welfare, requires elucidation. Whilst most dogs are believed to be anxious when showing SRB [1,2], it is uncertain whether their background affective state (mood) when they are not separated is also negative [1]. Here we use a new ‘cognitive bias measure of animal affect to show that dogs which exhibit high levels of SRB in a separation test also appear to have a more negative underlying mood.

A spatial judgement task to determine background emotional state in laboratory rats (Rattus norvegicus)

Humans experiencing different background emotional states display contrasting cognitive (e.g. judgement) biases when responding to ambiguous stimuli. We have proposed that such biases may be used as indicators of animal emotional state. Here, we used a spatial judgement task, in which animals were trained to expect food in one location and not another, to determine whether rats in relatively positive or negative emotional states respond differently to ambiguous stimuli of intermediate spatial location. We housed 24 rats with environmental enrichment for 7 weeks. We removed the enrichment from half the animals prior to the start of training to induce a relatively negative emotional state, whereas we left it in place for the remaining rats. After 6 training days, the rats successfully discriminated between the rewarded and the unrewarded locations in terms of an increased latency to arrive at the unrewarded location, with no housing treatment difference. The subjects then underwent 3 days of testing in which three ambiguous ‘probe’ locations, intermediate between the rewarded and the unrewarded locations, were introduced. There was no difference between the treatments in the rats judgement of two of the three probe locations, the exception being when the ambiguous probe was positioned closest to the unrewarded location. This result suggests that rats housed without enrichment, and in an assumed relatively negative emotional state, respond differently to an ambiguous stimulus compared to rats housed with enrichment, providing evidence that cognitive biases may be used to assess animal emotional state in a spatial judgement task.

Anxiety-induced cognitive bias in non-human animals

As in humans, cognitive biases in the way in which animals judge ambiguous stimuli may be influenced by emotional state and hence a valuable new indicator of animal emotion. There is increasing evidence that animals experiencing different emotional states following exposure to long-term environmental manipulations show contrasting biases in their judgement of ambiguous stimuli. However, the specific type of induced emotional state is usually unknown. We investigated whether a short-term manipulation of emotional state has a similar effect on cognitive bias, using changes in light intensity; a treatment specifically related to anxiety-induction. Twenty-four male rats were trained to discriminate between two different locations, in either high (H) or low (L) light levels. One location was rewarded with palatable food and the other with aversive food. Once the rats had shown spatial discrimination, by running significantly faster to the rewarded location, they were tested with three ambiguous locations intermediate between the rewarded and aversive locations, and their latency to approach each location recorded. Half the rats were tested in the same light levels as during training, the remainder were switched. Rats switched from high to low light levels (putatively the least negative emotional manipulation) ran significantly faster to all three ambiguous probes than those rats switched from low to high light levels (putatively the most negative manipulation). This suggests that the judgement bias technique might be useful as an indicator of short-term changes in anxiety for non-human animals.

A guide to defining and implementing protocols for the welfare assessment of laboratory animals: eleventh report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement.

The refinement of husbandry and procedures to reduce animal suffering and improve welfare is an essential component of humane science. Successful refinement depends upon the ability to assess animal welfare effectively, and detect any signs of pain or distress as rapidly as possible, so that any suffering can be alleviated. This document provides practical guidance on setting up and operating effective protocols for the welfare assessment of animals used in research and testing. It sets out general principles for more objective observation of animals, recognizing and assessing indicators of pain or distress and tailoring these to individual projects. Systems for recording indicators, including score sheets, are reviewed and guidance is set out on determining practical monitoring regimes that are more likely to detect any signs of suffering. This guidance is intended for all staff required to assess or monitor animal welfare, including animal technologists and care staff, veterinarians and scientists. It will also be of use to members of ethics or animal care and use committees. A longer version of this document, with further background information and extra topics including training and information sharing, is available on the Laboratory Animals website.

Sensitivity to reward loss as an indicator of animal emotion and welfare

The scientific study of animal emotion is an important emerging discipline in subjects ranging from neuroscience to animal welfare research. In the absence of direct measures of conscious emotion, indirect behavioural and physiological measures are used. However, these may have significant limitations (e.g. indicating emotional arousal but not valence (positivity versus negativity)). A new approach, taking its impetus from human studies, proposes that biases in information processing, and underlying mechanisms relating to the evaluation of reward gains and losses, may reliably reflect emotional valence in animals. In general, people are more sensitive to reward losses than gains, but people in a negative affective state (e.g. depression) are particularly sensitive to losses. This may underlie broader findings such as an enhanced attention to, and memory of, negative events in depressed individuals. Here we show that rats in unenriched housing, who typically exhibit indicators of poorer welfare and a more negative affective state than those in enriched housing, display a prolonged response to a decrease in anticipated food reward, indicating enhanced sensitivity to reward loss. Sensitivity to reward reduction may thus be a valuable new indicator of animal emotion and welfare.

The effects of enhancing cage complexity on the behaviour and welfare of laboratory rats

This experiment was carried out to investigate the long-term effects of enhancing cage complexity on behavioural measures of welfare in laboratory rats. We housed 72 rats in groups of four in either enriched or unenriched cages for six weeks. Scan and focal animal sampling were conducted in both the light and dark phase of the second, fourth and sixth weeks. Results revealed that rats in the enriched cages showed longer durations of sleep behaviour, and low levels of agonistic behaviour compared to rats in the unenriched cages. Results importantly demonstrated that the behavioural changes observed in the enriched environment were due to the presence of the enrichments themselves in the cages (indirect effects) and not due merely to rats interacting with the enrichment items in their environment. Thus, enhancing the complexity of conventional laboratory cages can promote behaviour such as longer bouts of sleep that is likely to be indicative of good welfare, and diminish levels of behaviour such as aggression that is likely to lead to poor welfare.

Short-term social memory in the laboratory rat: its susceptibility to disturbance.

Adult rats presented with a juvenile conspecific for 5 min on two occasions, separated by a 15-min inter-exposure interval (IEI), investigated the reintroduced juvenile significantly less in the second encounter. It is suggested that this was because the adult rats remembered the identity of the juvenile, because when a novel juvenile was introduced for the second encounter, no such reduction in investigation was observed. When the rats were either handled, placed in a smaller, novel, cage, or introduced to a new juvenile midway through the IEI, investigation of the reintroduced juvenile did not decrease. This indicated that memory of that juvenile had been disrupted. However, a simple change of cage during the IEI had no disruptive effect on memory. These results suggest that routine husbandry procedures can disrupt short-term social memory, which may lead to an increase in aggression due to a failure of recognition. This has implications for the welfare of captive social animals.

The effects of environmental context on laboratory rat social recognition.

Moving an animal from the environmental context in which it has learned a particular task to an entirely different context can reduce performance. We investigated the effect of switching environmental contexts on the ability of adult laboratory rats, Rattus norvegicus, to recognize and habituate to repeated presentations of juvenile conspecifics. Adults were exposed to juveniles for four periods of 5 min, separated by a 15-min interval. Rats either received all four exposures in the same context, or the first three in one context and the fourth in a different context. Half the rats in this latter group were familiarized with both contexts prior to testing, the other half had no experience of either. In all groups, the adults reduced their investigation of the juveniles over the three initial exposures. Mild aggression increased over the same period for the context-unfamiliar rats. A significant reduction in investigation by these rats between the third and fourth exposures, when the context was changed, suggested that the context switch further increased habituation to the juveniles. However, the context-familiar rats showed no such change, indicating that the changes observed for the context-unfamiliar rats were due to the effect of context novelty. This was supported by the finding that, during the first exposure, context-familiar adults investigated juveniles more and were more aggressive than those for which the contexts were novel. These results suggest that familiar contextual cues play only a minor role in the short-term social memory of laboratory rats. Copyright 1999 The Association for the Study of Animal Behaviour.

Housing conditions affect rat responses to two types of ambiguity in a reward–reward discrimination cognitive bias task

Highlights • We investigated how an unpredictable housing treatment (UHT) influenced measures of rat affect.• Control rats showed more anxiety-like behaviour in open-field and elevated plus maze tests than UHT rats.• Controls also made more ‘pessimistic’ decisions in an automated cognitive bias task.• Our go/go reward–reward task was learnt faster than previous automated go/go tasks.• We developed a new ambiguity test that may probe biases in attentional processes.