Berry M. Spruijt

Assessment of positive emotions in animals to improve their welfare

It is now widely accepted that good welfare is not simply the absence of negative experiences, but rather is primarily the presence of positive experiences such as pleasure. However scientific investigation of positive emotions has long been neglected. This paper addresses two main issues: first, it reviews the current state of scientific knowledge that supports the existence of positive affective states in animals and, second, it suggests possible applications of this knowledge that may enhance quality of life under animal management conditions. In the first part of the paper, recent advances in psychology and neuroscience are reviewed to provide pragmatic frameworks based on cognitive processes (such as positive anticipation, contrast and controllability) for further investigations of positive emotions in animals. Thereafter, the neurobiological bases of positive emotions are highlighted in order to identify behavioral and physiological expressions of positive experiences in animals. Monitoring both the autonomic nervous system (via heart rate and its variability) and the immune system could offer relevant tools to better assess emotional states in animals, complementary to classical adrenocortical measures. In the second part of the paper, useful strategies for enhancing positive experiences (such as physical, social and cognitive enrichment or putative genetic selection) are outlined. Then this paper emphasizes practical applications for assessing and promoting positive emotions that may help in providing animals with a better quality of life. Play, affiliative behaviors and some vocalizations appear to be the most promising convenient indicators for assessing positive experiences in laboratory and farm animals under commercial conditions.

A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems

In this review we attempt to link the efficiency by which animals behave (economy of animal behaviour) to a neuronal substrate and subjective states to arrive at a definition of animal welfare which broadens the scope of its study. Welfare is defined as the balance between positive (reward, satisfaction) and negative (stress) experiences or affective states. The state of this balance may range from positive (good welfare) to negative (poor welfare). These affective states are momentary or transient states which occur against the background of and are integrated with the state of this balancing system. As will be argued the efficiency in behaviour requires that, for instance, satisfaction is like a moving target: reward provides the necessary feedback to guide behaviour; it is a not steady-state which can be maintained for long. This balancing system is reflected in the brain by the concerted action of opioid and mesolimbic dopaminergic systems. The state of this system reflects the coping capacity of the animal and is determined by previous events. In other words, this integrative approach of behavioural biology and neurobiology aims at understanding how the coping capacity of animals may be affected and measured. We argue that this balancing system underlies the economy of behaviour. Furthermore we argue that among other techniques anticipation in Pavlovian conditioning is an easy and useful tool to assess the state of this balancing system: for estimating the state of an animal in terms of welfare we focus on the conditions when an animal is facing a challenge.

Play is indispensable for an adequate development of coping with social challenges in the rat

In this study, young rats were deprived of early social interactions during weeks 4 and 5 of life. Different behavioral tests were conducted in adulthood to study the behavioral responses of rats lacking early social experiences. Juvenile deprivation resulted in decreased social activity and an altered sexual pattern, but did not affect locomotor activity or the performance in the elevated plus maze. Furthermore, behavioral and neuroendocrine responses of juvenile isolated rats were dramatically altered when they were confronted with territorial aggression. Juvenile deprived rats did not readily display a submissive posture in response to the resident and showed no immobility behavior after being returned to the residents territory, while their plasma corticosterone and adrenaline concentrations were significantly increased compared to nonisolated controls. In contrast, behavioral responses in the shock prod test were not affected by previous isolation. The results suggest that early social experiences are vital for interactions with conspecifics later in life, i.e., aggression, sexual, and social interactions.

Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment.

Behavioural experience (e.g. chronic stress, environmental enrichment) can have long‐lasting effects on cognitive functions. Because activity‐dependent persistent changes in synaptic strength are believed to mediate memory processes in brain areas such as hippocampus, we tested whether behaviour has also long‐lasting effects on synaptic plasticity by examining the induction of long‐term potentiation (LTP) and long‐term depression (LTD) in slices of hippocampal CA1 obtained from rats either 7–9 months after social defeat (behavioural stress) or 3–5 weeks after 5‐week exposure to environmental enrichment. Compared with age‐matched controls, defeated rats showed markedly reduced LTP. LTP was even completely impaired but LTD was enhanced in defeated and, subsequently, individually housed (during the 7–9‐month period after defeat) rats. However, increasing stimulus intensity during 100‐Hz stimulation resulted in significant LTP. This suggests that the threshold for LTP induction is still raised and that for LTD lowered several months after a short stressful experience. Both LTD and LTP were enhanced in environmentally enriched rats, 3–5 weeks after enrichment, as compared with age‐matched controls. Because enrichment reduced paired‐pulse facilitation, an increase in presynaptic release, facilitating both LTD and LTP induction, might contribute to enhanced synaptic changes. Consistently, enrichment reduced the number of 100‐Hz stimuli required for inducing LTP. But enrichment may also actually enhance the range of synaptic modification. Repeated LTP and LTD induction produced larger synaptic changes in enriched than in control rats. These data reveal that exposure to very different behavioural experiences can produce long‐lasting effects on the susceptibility to synaptic plasticity, involving pre‐ and postsynaptic processes.

Defeat followed by individual housing results in long-term impaired reward- and cognition-related behaviours in rats.

In contrast to the well-documented acute effects on behavioural sensitivity, chronic effects that persist for weeks or even months after the cessation of the stressor received relatively little attention. This study aimed at the long-term effects of a severe stressor, i.e. social defeat followed by individual housing. Defeated and subsequently individually housed animals displayed impaired social memory, decreased social interaction and diminished anticipation for a sucrose solution for up until a period of 3 months after defeat. Remarkably, social housing counteracted the defeat-induced effects. The impaired capability to anticipate for a reward was discussed in relation to anhedonia, an important symptom of human depression. Moreover, the disturbed memory, the chronic nature of the effects, and the therapeutic effects of social housing, suggest that the defeat model may serve as a potential model for human psychopathology.

Spatial localization in the Morris water maze in rats : acquisition is affected by intra-accumbens injections of the dopaminergic antagonist haloperidol

Previous studies (G. E. Ploeger, B. M. Spruijt, & A. R. Cools, 1992) showed that low doses of systemically injected haloperidol affected spatial learning in the Morris water maze. This study investigated effects of intra-accumbens injections of haloperidol on spatial learning. To control for motivation and sensorimotor coordination, the researchers trained the rats to escape onto a visible platform. Low doses (50-100 ng) of haloperidol impaired spatial learning, whereas escaping on a visible platform was undisturbed. The 500-ng dose of haloperidol completely blocked acquisition because of combined learning and motor impairments. Retrieval of an acquired escape response was unaffected by 500 ng haloperidol. The data show that mesolimbic dopaminergic activity is involved in the acquisition of spatial localization. The results are related to studies demonstrating the involvement of the nucleus accumbens in cue-directed behaviors.

Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats

The present study was undertaken to assess the motivational aspects of social behaviour in juvenile and adult rats using the conditioned place preference (CPP) test and anticipatory behaviour for social contact. In addition, the consequences of social isolation during different periods of age on the motivational properties of sucrose-drinking and adult social behaviour were studied. Social play and adult social contact could be used as incentives for place preference conditioning and for inducing conditioned hyperactivity (anticipation) in rats. Both social activities have motivational properties for individually housed rats, whereas group-housing dramatically reduced the motivational aspects of adult social contact. In contrast, sucrose-drinking appears to have motivational aspects independent of the housing condition. Adult social behaviour could not induce a CPP in juvenile isolated rats, suggesting that juvenile isolation during 4 5 weeks reduced the motivational aspects of adult social contact. It seems likely that no CPP was established as a result of the reduced level of social behaviour during the conditioning sessions. Additionally, juvenile isolation during 4-5 weeks appeared to also decrease the motivational properties of sucrose-drinking in maturity, because the intensity of anticipation in response to sucrose was significantly suppressed. Thus, the data suggest that juvenile isolation during 4-5 weeks decreases the motivational properties of both social contact and sucrose-drinking in later life.

Novel approach to the behavioural characterization of inbred mice: automated home cage observations.

Here we present a newly developed tool for continuous recordings and analysis of novelty‐induced and baseline behaviour of mice in a home cage‐like environment. Aim of this study was to demonstrate the strength of this method by characterizing four inbred strains of mice, C57BL/6, DBA/2, C3H and 129S2/Sv, on locomotor activity. Strains differed in circadian rhythmicity, novelty‐induced activity and the time–course of specific behavioural elements. For instance, C57BL/6 and DBA/2 mice showed a much faster decrease in activity over time than C3H and 129S2/Sv mice. Principal component analysis revealed two major factors within locomotor activity, which were defined as ‘level of activity’ and ‘velocity/stops’. These factors were able to distinguish strains. Interestingly, mice that displayed high levels of activity in the initial phase of the home cage test were also highly active during an open‐field test. Velocity and the number of stops during movement correlated positively with anxiety‐related behaviour in the elevated plus maze. The use of an automated home cage observation system yields temporal changes in elements of locomotor activity with an advanced level of spatial resolution. Moreover, it avoids the confounding influence of human intervention and saves time‐consuming human observations.

Standard housed rats are more sensitive to rewards than enriched housed rats as reflected by their anticipatory behaviour.

The present study was designed to investigate the effects of potentially stressful standard housing conditions for laboratory rats on the sensitivity to rewards as reflected by their anticipatory behaviour for sucrose. This anticipatory response is evoked in a conditioning paradigm in which a sucrose reward is repeatedly announced by a stimulus. The underlying neurocircuitry of this anticipatory response in expectation of a reward involves mesolimbic dopaminergic systems of which it is known that they can be sensitised by stressors. The results show that the anticipatory response for the sucrose reward is stronger in the standard housed animals which indicates that these animals are more sensitive to the reward than the enriched animals. From this, it is concluded that standard housed rats are stressed which is likely to be caused by deprivation of the ability to satisfy behavioural needs in these impoverished housing conditions.

μ- and κ-opioid receptor-meiated opioid effects on social play in juvenile rats

Previously, morphine has been shown to influence social play behavior in rats on two levels. An increasing effect on social play was interpreted as an effect on the rewarding aspects of social play. A lower dose of morphine abolished the effects of an unfamiliar environment on social play, supposedly by affecting the integration of environmental stimuli. In the present study the effects of receptor-specific opioid drugs on social play and measures of social behavior unrelated to play were investigated. Fentanyl, a μ-opioid receptor agonist, seemingly mimicked both effects of morphine. The μ-opioid receptor antagonist, β-funaltrexamine, decreased social play, although a low dose of this drug increased it. BUBUC (Tyr-d-Cys(StBu)-Gly-Phe-Leu-Thr(OtBu)) and naltrindole, a δ-opioid receptor agonist and δ-opioid receptor antagonist, respectively, had no effects on social behavior. The κ-opioid receptor agonist, U50,488H (trans-3,4-dichloro-N-methyl-N-[2-(1-pyrrolidinyl)-cyclohexyl]-benzenea-cetamide), dose dependently suppressed all measures of social behavior. The κ-opioid receptor antagonist, nor-binaltorphimine, abolished the effects of an unfamiliar environment on social play. These studies suggest that the opioidergic effect on social play is mediated through μ- and κ-opioid receptor systems.