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.     

Operant model of frustrated expected reward in mice

One aspect of the addictive process that has not been thoroughly investigated is the consequence of the frustrated state occurring when the drug is not available. The present study aimed to validate a novel operant model of frustrated expected reward in mice. C57BL/6J mice were trained in operant conditioning maintained by chocolate-flavoured pellets or cocaine. After the completion of high rates of responding on a progressive ratio schedule, the reward was unexpectedly withheld. The consequences of this frustrated behaviour on anxiety, aggressiveness, perseveration, extinction and reinstatement were investigated. Mice exposed to the frustrated event perseverated in the operant responses and showed increased aggressiveness in the resident-intruder test. These animals also showed higher rates of cue-induced reinstatement of drug seeking. The present study provides a reliable operant model in mice to evaluate a frustrated state following reward unavailability. This animal model could be useful to study the behavioural and neurochemical consequences related to the emotional states generated during the omission of a highly expected reward.     

Health and Welfare in Animals and Humans

This paper contains a brief comparative analysis of some philosophical and scientific discourses on human and animal health and welfare, focusing mainly on the welfare of sentient animals. The paper sets forth two kinds of proposals for the analysis of animal welfare which do not appear in the contemporary philosophical discussion of human welfare, viz. the coping theory of welfare and the theory of welfare in terms of natural behaviour. These proposals are scrutinized in the light of some similar theories dealing with human health and quality of life. My conclusion is that the coping theory and the natural behaviour theory are not in themselves adequate for the characterization of welfare, either for humans or for sentient animals. I contend, finally, that, in the light of the previous discussion, there are good arguments for a particular set of analyses of both animal and human welfare, viz. the ones that are based on the notions of preference satisfaction and positive subjective experiences.     

Neuroethology of reward and decision making

Ethology, the evolutionary science of behaviour, assumes that natural selection shapes behaviour and its neural substrates in humans and other animals. In this view, the nervous system of any animal comprises a suite of morphological and behavioural adaptations for solving specific information processing problems posed by the physical or social environment. Since the allocation of behaviour often reflects economic optimization of evolutionary fitness subject to physical and cognitive constraints, neurobiological studies of reward, punishment, motivation and decision making will profit from an appreciation of the information processing problems confronted by animals in their natural physical and social environments.     

Animals in flow – towards the scientific study of intrinsic reward in animals

The concept of flow, a state of complete absorption in an intrinsically rewarding activity, has played a pivotal role in advancing notions of human well-being beyond minimising suffering towards promoting flourishing and thriving. While flow has played a fundamental role in human positive psychology, it has not yet been explored in non-human animals, leaving an enormous void in our understanding of intrinsic motivation in animals. As ethology and related fields keep progressing in uncovering complex cognitive and affective capacities of non-human animals, we propose the time is ripe to translate the concept of flow to animals. We start by embedding flow in the topic of intrinsic motivation and describe its impact on positive human psychology and potentially positive animal welfare. We then disambiguate flow from related concepts discussed in the animal literature. Next, we derive experimental approaches in animals from the canonical characteristics of flow in humans and provide guidelines for both inducing and assessing flow by focusing on two characteristics that do not necessarily depend on self-report, namely resistance to distraction and time distortion. Not all aspects of the human flow experience are (yet) translatable, but those that are may improve quality of life in captive non-human animals.     

Wanting,liking and welfare: The role of affective states in proximate control of behaviour in vertebrates

Animals choose a course of action countless times each day. To do so, they need to prioritise their behaviour within a set of alternative actions and decide which of these actions to perform at any one time and for how long, that is, determine when the behaviour has reached its desired effect. This process has classically been called the proximate behavioural control mechanism. Several aspects contribute to this process: internal and external stimuli, the emotions that they elicit, motivation (wants), behavioural goals, valuation, decision‐making and its modulation by mood, and the assessment of behavioural outcomes (liking). I will address all these aspects in the form of an integrated conceptual model. In the process of behavioural control, options need to be valued, and I will refer to evidence showing that an affective hedonic process in respect to (future) reward and punishment heavily affects this value. Moreover, I view motivation, the force that finally drives a specific behavioural output, as being primarily influenced by affective states or even corresponding fully to them. Given the feedback in behavioural control by (dis‐)liking outcomes of behaviour, I reason that in respect to welfare it is more important for animals to reach proximate goals than to avoid negative stimuli. All behavioural choices are modulated, and I show how mood, a long‐term affective state, can cause such modulation. Proximate control of behaviour takes place in the brain, and I will briefly discuss how current and future brain research may elucidate how the brain computes these processes. Furthermore, the inclusion of affective states in the conceptual model raises the question of the subjective experience of animals, and I will address some of the important open questions in this area of research. I will conclude that neural studies cannot currently provide a detailed and general theory on the algorithms of proximate behavioural control. In parallel to further developing these approaches, I propose to strengthen a refined ethological approach with a focus on the states of “wanting” and “liking” in ecologically meaningful circumstances and with a strong ontogenetic (within species) and comparative (between species) component. I consider this ethological approach to be a highly promising step in understanding proximate behavioural control.     

Frustrative reward omission increases aggressive behaviour of inferior fighters

Animals use aggressive behaviour to gain access to resources, and individuals adjust their behaviour relative to resource value and own resource holding potential (RHP). Normally, smaller individuals have inferior fighting abilities compared with larger conspecifics. Affective and cognitive processes can alter contest dynamics, but the interaction between such effects and that of differing RHPs has not been adjudged. We investigated effects of omission of expected reward (OER) on competing individuals with contrasting RHPs. Small and large rainbow trout (Oncorhynchus mykiss) were conditioned to associate a light with reward. Thereafter, the reward was omitted for half of the fish prior to a contest between individuals possessing a 36–40% difference in RHP. Small control individuals displayed submissive behaviour and virtually no aggression. By contrast, small OER individuals were more aggressive, and two out of 11 became socially dominant. Increased aggression in small OER individuals was accompanied by increased serotonin levels in the dorsomedial pallium (proposed amygdala homologue), but no changes in limbic dopamine neurochemistry were observed in OER-exposed individuals. The behavioural and physiological response to OER in fish indicates that frustration is an evolutionarily conserved affective state. Moreover, our results indicate that aggressive motivation to reward unpredictability affects low RHP individuals strongest.     

Dynamics of betting behavior under flat reward condition

One of the missions of the cognitive process of animals, including humans, is to make reasonable judgments and decisions in the presence of uncertainty. The balance between exploration and exploitation investigated in the reinforcement-learning paradigm is one of the key factors in this process. Recently, following the pioneering work in behavioral economics, growing attention has been directed to human behaviors exhibiting deviations from the simple maximization of external reward. Here we study the dynamics of betting behavior in a simple game, where the probability of reward and the magnitude of reward are designed to give a "zero" expected net reward ("flat reward condition"). No matter how the subject behaves, there is on average no change in one's resources, and therefore every possible sequence of action has the same value. Even in such a situation, the subjects are found to behave not in a random manner, but in ways showing characteristic tendencies, reflecting the dynamics of brain's reward system. Our results suggest that brain's reward system is characterized by a rich and complex dynamics only loosely coupled with external reward structure.     

Animal Welfare at the Group Level: More Than the Sum of Individual Welfare?

Currently assessment and management of animal welfare are based on the supposition that welfare status is something experienced identically by each individual animal when exposed to the same conditions. However, many authors argue that individual welfare cannot be seen as an ‘objective’ state, but is based on the animal’s own self-perception; such perception might vary significantly between individuals which appear to be exposed to exactly the same challenges. We argue that this has two implications: (1) actual perceived welfare status of individuals in a population may vary over a wide range even under identical environmental conditions; (2) animals that appear to an external observer to be in better or poorer welfare condition may all in fact perceive their own individual status as the same. This would imply that optimum welfare of a social group might be achieved in situations where individual group members differ markedly in apparent welfare status and perceive their own welfare as being optimal under differing circumstances. Welfare phenotypes may also vary along a continuum between self-regarding and other-regarding behaviour; a variety of situations exist where (social) individuals appear to invest in the welfare of other individuals instead of maximising their own welfare; in such a case it is necessary to re-evaluate individual welfare within the context of a social group and recognise that there may be consequences for the welfare of individuals, of decisions made at the group level or by other group members.     

Behaviour as a tool in the assessment of animal welfare

A central issue in animal welfare research is how to assess the welfare state of animals objectively and scientifically. I argue that this issue can be approached by asking two key questions: 1) is the animal physically healthy and 2) does the animal have what it wants? Behaviour is used to answer both of these questions. In the assessment of physical health, it can be used for clinical and pre-clinical diagnosis. In the assessment of what animals want, it has a major role through choice and preference testing. It is particularly important that applied ethologists develop methods for assessing welfare in situ--in the places where concern for animal welfare is greatest such as on farms and in zoos.     

The Science of Animal Suffering

Can suffering in non‐human animals be studied scientifically? Apart from verbal reports of subjective feelings, which are uniquely human, I argue that it is possible to study the negative emotions we refer to as suffering by the same methods we use in ourselves. In particular, by asking animals what they find positively and negatively reinforcing (what they want and do not want), we can define positive and negative emotional states. Such emotional states may or may not be accompanied by subjective feelings but fortunately it is not necessary to solve the problem of consciousness to construct a scientific study of suffering and welfare. Improvements in animal welfare can be based on the answers to two questions: Q1: Will it improve animal health? and Q2: Will it give the animals something they want? This apparently simple formulation has the advantage of capturing what most people mean by ‘improving welfare’ and so halting a potentially dangerous split between scientific and non‐scientific definitions of welfare. It can also be used to validate other controversial approaches to welfare such as naturalness, stereotypies, physiological and biochemical measures. Health and what animals want are thus not just two of many measures of welfare. They provide the definition of welfare against which others can be validated. They also tell us what research we have to do and how we can judge whether welfare of animals has been genuinely improved. What is important, however, is for this research to be done in situ so that it is directly applicable to the real world of farming, the sea or an animal’s wild habitat. It is here that ethology can make major contributions.     

Invited review: The evolution of cattle bioacoustics and application for advanced dairy systems

Vocalisations are commonly expressed by gregarious animals, including cattle, as a form of short- and long-distance communication. They can provide conspecifics with meaningful information about the physiology, affective state and physical attributes of the caller. In cattle, calls are individually distinct meaning they assist animals to identify specific individuals in the herd. Consequently, there is potential for these vocalisations to be acoustically analysed to make inferences about how individual animals or herds are coping with their external surroundings, and then act on these signals to improve feed conversion efficiency, reproductive efficiency and welfare. In the case of dairy farming, where herd sizes are expanding and farmers are becoming more reliant on technologies to assist in the monitoring of cattle, the study of vocal behaviour could provide an objective, cost effective and non-invasive alternative to traditional measures of welfare. The vocalisations of cattle in response to calf separation, social isolation and painful husbandry procedures, alongside changes to feeding and oestrous activity are here reviewed. For future application of sound technology, research is first necessary to analyse the acoustic structure of cattle vocalisations and determine the specific information they encode. This review draws together the latest research in field of cattle bioacoustics highlighting how the source–filter theory and affective state dimensional approach can be adopted to decode this information and improve on-farm management.     

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.     

Play behaviour in nonhuman animals and the animal welfare issue

The mission of defining animal welfare indicators is methodologically difficult, limited, and possibly impossible. A promising alternative, however, to evaluate suitable environmental conditions is the assessment of play behaviour. In the present review, we summarise the general aspects of play behaviour in nonhuman animals and propose its use as a potential indicator of animal welfare. Play behaviour probably occurs in most vertebrates and some invertebrates, but predominately in mammals. It is also more frequent in young males and is associated with the environmental context in which animals find themselves. Animals play if they are healthy and well-fed, but not if they are under stressful conditions or if they are in a stressful state. We can therefore use the prevalence of play behaviour as an indicator of suitable environmental conditions, considering the specificity associated with the above-mentioned modifying factors.     

Vocal behaviour in cattle: the animal's commentary on its biological processes and welfare

The vocalizations of cattle provide conspecifics with meaningful information about the caller. If we can learn how to interpret this information correctly, it could be used to improve management and welfare assessment. Vocalization may be viewed as a subjective commentary, by an individual, on its own internal state. The vocal behaviour of cattle is potentially a useful indicator of their physiological and psychological functioning.In the first part of this article we ask what information is exchanged using auditory cues. Vocalizations provide information on the age, sex, dominance status and reproductive status of the caller. Calves can recognize their mothers using vocal cues but it is not clear whether cows recognize their offspring in this way. Vocal behaviour may play a role in estrus advertisement and competitive display by bulls. Under experimental conditions involving pain or social isolation, vocal response is useful as an indicator of welfare, if properly used. Unlike commonly used physiological measures, it can be recorded non-invasively and varies on a number of quantitative and qualitative dimensions.In the second part we review methodological approaches to the study of vocal behaviour and their application in cattle welfare research. Methods may focus on the actions of the vocalizing animal and the conditions which elicit vocal behaviour, the response of an animal to hearing another's vocalizations, or interactions between sender and receiver.We argue that vocal behaviour in cattle may be valuable in welfare studies if the endogenous, exogenous and developmental factors influencing its expression can be more thoroughly investigated and understood.     

Humor modulates the mesolimbic reward centers

Humor plays an essential role in many facets of human life including psychological, social, and somatic functioning. Recently, neuroimaging has been applied to this critical human attribute, shedding light on the affective, cognitive, and motor networks involved in humor processing. To date, however, researchers have failed to demonstrate the subcortical correlates of the most fundamental feature of humor-reward. In an effort to elucidate the neurobiological substrate that subserves the reward components of humor, we undertook a high-field (3 Tesla) event-related functional MRI study. Here we demonstrate that humor modulates activity in several cortical regions, and we present new evidence that humor engages a network of subcortical regions including the nucleus accumbens, a key component of the mesolimbic dopaminergic reward system. Further, the degree of humor intensity was positively correlated with BOLD signal intensity in these regions. Together, these findings offer new insight into the neural basis of salutary aspects of humor.     

Effect of Post-Weaning Individual Housing on Autonomic Responses in Male Rats to Sexually Receptive Female Rats

Post-weaning individual housing induces significant alterations in the reward system of adult male rats presented with sexually receptive female rats. In this study, we examined the effects of post-weaning individual housing on autonomic nervous activity in adult male rats during encounters with sexually receptive female rats to assess whether different affective states depending on post-weaning housing conditions are produced. Changes in heart rate and spectral parameters of heart rate variability indicated that in post-weaning individually housed male rats, both sympathetic and parasympathetic activity increased with no change in the sympathovagal balance, while in post-weaning socially housed male rats, both sympathetic and parasympathetic activity decreased with a predominance of parasympathetic activity. These two patterns of shifts in sympathovagal balances closely resembled changes in autonomic nervous activity with regard to classical appetitive conditioning in male rats. The autonomic changes in male rats housed individually after weaning corresponded to changes associated with the reward-expecting state evoked by the conditioned stimulus, and the autonomic changes observed in male rats housed socially after weaning corresponded to changes associated with the reward-receiving state evoked by the unconditioned stimulus. These results suggest that different affective states were induced in adult male rats during sexual encounters depending on male–male social interactions after weaning. The remarkable change caused by post-weaning individual housing may be ascribed to alteration of the reward system during sexual encounters induced by deficiency of intermale social communication after weaning.     

Laughing Rats Are Optimistic

Emotions can bias human decisions- for example depressed or anxious people tend to make pessimistic judgements while those in positive affective states are often more optimistic. Several studies have reported that affect contingent judgement biases can also be produced in animals. The animals, however, cannot self-report; therefore, the valence of their emotions, to date, could only be assumed. Here we present the results of an experiment where the affect-contingent judgement bias has been produced by objectively measured positive emotions. We trained rats in operant Skinner boxes to press one lever in response to one tone to receive a food reward and to press another lever in response to a different tone to avoid punishment by electric foot shock. After attaining a stable level of discrimination performance, the animals were subjected to either handling or playful, experimenter-administered manual stimulation – tickling. This procedure has been confirmed to induce a positive affective state in rats, and the 50-kHz ultrasonic vocalisations (rat laughter) emitted by animals in response to tickling have been postulated to index positive emotions akin to human joy. During the tickling and handling sessions, the numbers of emitted high-frequency 50-kHz calls were scored. Immediately after tickling or handling, the animals were tested for their responses to a tone of intermediate frequency, and the pattern of their responses to this ambiguous cue was taken as an indicator of the animals'' optimism. Our findings indicate that tickling induced positive emotions which are directly indexed in rats by laughter, can make animals more optimistic. We demonstrate for the first time a link between the directly measured positive affective state and decision making under uncertainty in an animal model. We also introduce innovative tandem-approach for studying emotional-cognitive interplay in animals, which may be of great value for understanding the emotional-cognitive changes associated with mood disorders.     

My pigs are ok,why change? – animal welfare accounts of pig farmers

Intensive pig production systems are a source of stress, which is linked to reduced animal welfare and increased antimicrobial use. As the gatekeepers of the welfare of the animals under their care, farmers are seen as the stakeholder responsible for improving animal welfare. The aim of this study was to explore the knowledge and attitudes of pig farmers towards pig welfare and the impact of such attitudes on farmers' selection of management strategies on the farm. We conducted in-depth semi-structured interviews with 44 pig farmers in one of the main pig producing regions of Brazil. Interviews covered knowledge and attitudes towards pig sentience and behaviour and welfare-related issues commonly observed in intensive pig farms (belly-nosing, fights, tail-biting, diarrhoea and castration without pain control) and farmers' conception and attitudes towards pig welfare. We identified many management and animal-based indicators of poor welfare, such as the use of painful and stressful management practices and use of environments that limit the expression of natural behaviours. However, most farmers were satisfied with animal welfare standards at their farms. Farmers' perceptions are aligned with their understanding of animal welfare. Although they identified all the dimensions that impact the welfare of a pig on a farm (affect, biological functioning and naturalness), their social reality, industry demands and available advice pushed them to perceive their range of action limited to biological and environmental aspects of the animals that do not necessarily benefit affective state. This precluded farmers from making associations between good health and the animal's ability to express a full behavioural repertoire, as well as from viewing abnormal behaviours as problems. The negative consequences for the welfare of the animals were commonly alleviated by routines that relied on constant use of medication, including high dependence on antibiotics. Expressions of estrangement from the production chain were common voices among the participants. This suggests that farmers may not be sufficiently informed or engaged in responding to consumers' expectations and commitments made by companies, which can pose a severe economic risk for farmers. The findings of this study indicate that economic, technical and social factors restrict farmers' autonomy and their ability to perform their role as stewards of animal welfare. (Re)connecting different human, animal and environmental interests may be a step to changing this scenario.     

Attitudes of Dairy Farmers toward Cow Welfare in Relation to Housing,Management and Productivity

ABSTRACT

The quality of stockmanship contributes to the human–animal relationship, animal welfare and productivity. Attitudes can affect the way farmers treat their animals, the environment they provide the animals with, and even their own job satisfaction through the feedback received from the animals. Farmers' perceptions of animals have also been shown to have an impact on productivity. We investigated 161 Finnish dairy farmers' attitudes toward improving animal welfare through an attitude questionnaire that used the Theory of Planned Behavior as a theoretical framework. The theory states that personal attitude, subjective norms, and perceived behavioral control, together shape an individual's behavioral intentions and behaviors. To study the relationship between attitudes, animal welfare, and milk production, we used environment-based animal welfare indicator data consisting of categorized housing and management parameters, and mean milk production data. Non-parametric partial correlation analyses and regression analyses revealed that perceiving the measures to improve animal welfare to be important and easy were positively, although weakly, related to higher animal welfare standards/indicators, while no connection with production was established. Contrary to our expectations, sources of subjective norms, such as an agricultural adviser, were mostly negatively linked with animal welfare indicators and even with production. The farmers considered taking care of their own well-being as the most important way of improving animal welfare, and intending to do so was weakly but positively linked with animal welfare indicators. Any causal relationships, however, cannot be derived from the data.