Arnaud Aubert

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.

Differential Effects of Lipopolysaccharide on Pup Retrieving and Nest Building in Lactating Mice

Behavioral symptoms of sickness that develop in response to lipopolysaccharide (LPS) and proinflammatory cytokines include depressed locomotion, anorexia, and reduced social activities. The way maternal behavior is affected in response to cytokines has, however, not yet been investigated. We checked that lactating mice are sensitive to LPS by showing that LPS- (400 microg/kg, ip) injected mice ate and drank less than saline-injected mothers and displayed a decreased rectal temperature. At an ambient temperature of 22 degrees C, nest building was significantly decreased in LPS-treated mothers compared to saline-treated animals, whereas pup retrieving, while slower, was still present and globally as efficient as for saline-treated mice. In a second experiment, dams were either injected with physiological saline or LPS but were also exposed to a cold ambient temperature (6 degrees C) or kept in standard external condition (22 degrees C). LPS-treated mice exposed to cold expressed not only pup-retrieving but also nest-building activity. These differential results indicate that the behavioral expression of LPS-induced sickness depends on the priority of the behavior under consideration.

Mechanisms of the Behavioural Effects of Cytokines

Sickness behavior refers to the coordinated set of behavioral changes that develop in sick individuals during the course of an infection. A sick individual typically displays depressed locomotor activity and little or no interest in his physical and social environment. Body care activities are usually absent and ingestive behavior is profoundly depressed despite the increased metabolism that is necessary for the fever response. Since the initial demonstration in the late eighties that similar symptoms are induced in healthy subjects by peripheral and central injection of the proinflammatory cytokines that are released by activated monocytes and macrophages during the host response to infection, the mechanisms of cytokine-induced sickness behaviour have been the subject of intense research, carried out at several levels of investigation. The purpose of the present chapter is to review the results that have been obtained in this field during the last decade. At the behavioural level, there is now clear evidence showing that sickness behaviour is not the result of weakness and physical debilitation affecting the sick individual, but the expression of a central motivational state that reorganizes the organism’s priorities to cope with pathogenic microorganisms. At the organ level, this motivational aspect of sickness behavior is important since it implies that the endogenous signals of sickness are likely to act on the brain to activate a set of neural structures that are at the origin of the subjective, behavioural and physiological components of sickness. The presence of cytokine receptors in the brain is in accordance with this view.

Differential Effect of Lipopolysaccharide on Food Hoarding Behavior and Food Consumption in Rats

Experimental studies assessing the suppressing effect of lipopolysaccharide (LPS) on feeding behavior have focused exclusively on the ingestive component of this behaviour without taking into account its appetitive component. The appetitive sequence of feeding behavior regroups activities animals engage in to gain access to food without necessarily eating it. The objective of the present study was to compare the effects of LPS on food intake and food hoarding. Rats were given the possibility to access food during a 30-min daily session in an apparatus consisting of a cage connected to an alley with free food at its end. Subjects were tested under different motivational levels for food hoarding: a first group (FS) received a food supplement to maintain stable body weight while a second group (noFS) did not receive such a supplement. LPS (250 micrograms/kg i.p.) dramatically decreased total food intake in rats from both groups whereas food hoarding was much less affected in LPS-treated rats from the noFS group. This expression of a still salient secondary motivation in LPS-treated rats which did not receive any food supplement can be interpreted to suggest the expression of an anticipatory feeding behavior along with a reduced immediate appetite. In addition, LPS had no effect, in rats from the noFS group, on the amount of food eaten after transport to the refuge. LPS-treated animals still appear to be able to adjust their defensive behavioral strategies with regard to their needs and capacities. These findings support the adaptive value of the behavioral changes displayed by LPS-treated animals.

Cytokine Actions on Behavior

Sickness behavior refers to a coordinated set of behavioral changes that develop in sick individuals during the course of an infection. These changes are due to the effects of proinflammatory cytokines such as interleukin-1 (IL-1) and tumor necrosis factor alpha (TNF-α) on brain cellular targets and represent the expression of a well organized central motivational state. Based on the results of pharmacological and biochemical experiments, it is now apparent that sickness behavior is mediated by cytokines which are temporarily expressed in the brain in response to peripheral cytokines. Centrally released cytokines act on brain receptors which are identical to those characterized on immune cells. Primary afferent nerves represent the main communication pathway between peripheral and central cytokines. The sickness inducing effects of cytokines are downregulated by a number of endogenous neuropeptides and hormones, including vasopressin and glucocorticoids.

Compared effects of cold ambient temperature and cytokines on macronutrient intake in rats

To compare the effects of cold and cytokines on spontaneous dietary self-selection, rats (n = 14) were given free access to carbohydrate, protein and fat diets for 4 hours a day. After a 10-day period of habituation to this regimen, they were injected with physiological saline, IL-1 beta (4 micrograms/rat ip) or LPS (83 micrograms/rat ip) or exposed to cold (5 degrees C), the order of treatments being randomized. LPS- and IL-1 beta-treated rats ate less, but ingested relatively more carbohydrate and less protein whereas relative fat intake remained unchanged. In contrast, cold exposed rats slightly increased their food intake but in a non significant manner. They also increased their relative intake of fat but did not change their relative intake of carbohydrate and protein. These results are discussed with respect to the pyrogenic and metabolic effects of cytokines.

The taste of sickness: Lipopolysaccharide-induced finickiness in rats

Decrease in food intake is one of the most documented non-specific symptoms of inflammatory processes. However, attention has been mainly focused on quantitative analysis. The present paper reports studies undertaken to test the possible contribution of changes in taste processes in inflammatory-induced alteration of feeding behavior. In a first experiment, the effects of lipopolysaccharide-induced sickness were assessed on preference for saccharin and aversion for quinine in rats using the two-bottle test paradigm. In a second experiment, effect of lipopolysaccharide (LPS) on the behavioral reactivity to palatable, unpalatable and mixed solutions was analyzed using the taste-reactivity paradigm. Our results show that LPS decreased total fluid intake but did not change taste responses to unpalatable or palatable substances. However, LPS increased aversive reactions and decreased hedonic responses to mixed taste. These LPS-induced changes are interpreted as an increase in finickiness and are discussed in regard to their potential role in the adaptation of individuals to sickness.

Cytokines and Immune-Related Behaviors

Abstract Theodosius Dobzhansky noted that “nothing in biology makes sense except in the light of evolution”. The success of species evolution owes much to the complex set of adaptive responses, which they are able to mount when confronted with environmental changes. These changes are perceived through various sensory receptors and trigger a complicated array of physiological responses. As animals have always lived surrounded by pathogenic microorganisms and will continue to do so, invasion of tissues by either bacteria or viruses similarly initiates a set of adaptive responses involving not only the immune system but also the functionally linked nervous system. These responses include behavioral changes including sleepiness, hypophagia, and general withdrawal, and have been found to potentiate the efficiency of the immune system to clear off pathogens. These behavioral changes have been for long commonly considered as the inability to achieve normal activities resulting from a debilitation of the general physical state of the sick individual. On the contrary, sick animals retain the ability to express complex behaviors under specific circumstances. The expression of the behavioral repertoire remains flexible and therefore depends on changes in the situation the sick individual is facing. This flexibility can be interpreted in motivational terms and therefore open the gate to the further study of behavioral dynamics induced by inflammatory processes.