Sickness and behaviour in animals: a motivational perspective

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Abstract

Proinflammatory cytokines, produced by the activated immune system, induce a whole set of non-specific symptoms in the infected individual (i.e. hypophagia, adipsia, reduced social interest). However, evidence summarised in this review shows that behavioural changes induced by cytokines are not merely the consequence of a degraded state but reflect motivational reorganisation. If the set-up of these new priorities is expressed by a general decrease in behavioural activities (e.g. immobility, sleepiness), the sick individual remains nevertheless an open system still able to respond to environmental stimuli. If these cues are evaluated as relevant to the new priorities (e.g. cues from scattered pups or cues from nest material when ambient temperature is low), the sick individual interrupts sickness behaviour in order to respond specifically to the cues (e.g. retrieving of the pups or nest building). Once this is done, there is a return to recuperative behaviour. These findings represent a primary characterisation of biobehavioural action of immune stimuli, and they open new perspectives to facilitate further progress in our understanding of cytokine effects on behaviour.

Introduction

Animals acutely sick from systemic protozoan, bacterial or viral infections, commonly display a whole set of non-specific symptoms. Among the most reliable symptoms are changes in body temperature, increase in slow wave sleep, uneasiness, loss of interest for daily activities and reduction in food intake [1], [2]. For most physicians and veterinarians, these non-specific symptoms, and in particular the behavioural changes, are traditionally interpreted as the inability to achieve normal activities resulting from a debilitation of the general physiological state of the sick individual.

This conception of infectious diseases has led to neglect the fact that throughout their evolutionary history, all species have been exposed to and have successfully resisted the noxious effects of various invading micro-organisms and are the products of an “arms race” [3], [4]. Indeed, for the most part, the scientific literature dealing with behavioural adaptation, including ultimate and proximate causation, mainly focuses attention on healthy individuals. In their natural environment, animals are challenged by numerous pathogens that can originate infectious or inflammatory illnesses. It seems therefore reasonable to hypothesise that animals would have various physiological and behavioural mechanisms to fight illness and promote recovery.

Nevertheless, considering the host-pathogen relationship, various studies have pointed out the emergence of immune strategies in mammals in order to fight infection [5], [6]. Moreover, the large amount of data indicating a dense cross-talk between neuroendocrine and immune systems suggests the evolution of non-immune (e.g. behavioural) strategies to serve the same purpose. This supposition is reinforced by the fact [2] that sick animals are submitted to a situation in which their integrity is heavily compromised, either through the bypass of their immune resources or by over-delaying the expression of basic life-supporting behaviours.

However, despite highlighting the bi-directional immune-neuroendocrine communications, the study of behavioural patterns in sick animals has not received much attention, presumably because of its triviality. Almost all behavioural studies in the field of the neurobiology of cytokines use behaviour as a dependent variable to determine which cytokines are neurologically active, and what underlying receptor mechanisms may be involved. The approach that is proposed here is different. It considers sickness behaviour as an independent variable that deserves to be studied as such, in order to determine the way it is organised and regulated at the behavioural level. The understanding of sickness behaviour per se should provide basic knowledge on a little studied natural animal behaviour.

Our alternative hypothesis is that the behavioural modifications accompanying the course of infection or inflammation (e.g. lethargy, adipsia, hypophagia, and social disinterest), reflect the expression of motivational reorganisation, specifically devoted to counter the pathogenic micro-organisms. On this view, motivation is defined as a central state that orientates the perception and actions of the sick animal [7].

Section snippets

Host response to infection and inflammation

Response of the organism to disturbances of its homeostasis during viral, bacterial, or parasitic infection, and tissue injury is called acute phase response [8]. It consists of both a local and systemic reaction. The local reaction is dominated by inflammation. It involves many different cell types, including phagocytic cells, lymphocytes and endothelial cells. Interactions between these different cell types are mediated by soluble factors known as cytokines. The systemic reaction is mediated

Sickness behaviour as an adaptive response to infection and inflammation

Hart [2] convincingly argued that the behavioural features of sick animals are not maladaptive responses or side-effects of the pathogen-induced debilitation. Rather, he proposed that these changes form a co-ordinated ensemble termed sickness behaviour. This concept refers to a behavioural strategy intended to support the metabolic and physiological changes that occur in the infected organism and which help to fight the pathogen. For example, cytokine-induced hypophagia can be interpreted as a

Conclusion

The results briefly reviewed here support the theoretical position of sickness as sustaining a motivational system. Thus, the data show that sick animals cannot be considered as incapacitated and that they can express complex behaviours. Moreover, we have seen that this behavioural expression is flexible and depends on changes in the situation. This flexibility can be interpreted in motivational terms. The sick animal develops new behavioural priorities geared to increase the efficiency of its

Acknowledgements

The preparation of this manuscript has been supported by Foundation IPSEN.

References (51)

  • R Yirmiya

    Endotoxin produces a depressive-like episode in rats

    Brain Res

    (1996)
  • M Maes et al.

    Relationships between inteleukin-6 activity, acute phase proteins, and function of the hypothalamic-pituitary-adrenal axis in severe depression

    Psychiat Res

    (1993)
  • A Sluzewska et al.

    Indicators of immune activation in major depression

    Psychiat Res

    (1996)
  • A Aubert et al.

    Differential effects of lipopolysaccharide on pup retrieving and nest building in lactating mice

    Brain Behav Immun

    (1997)
  • A Aubert et al.

    Differential effect of lipopolysaccharide on food hoarding behaviour and food consumption in rats

    Brain Behav Immun

    (1997)
  • J.I Glendinning

    Is the bitter rejection response always adaptive?

    Physiol Behav

    (1994)
  • N.K Dess

    Saccharin's aversive taste in rats: evidence and implications

    Neurosci Biobehav Rev

    (1993)
  • R Dantzer et al.

    Cytokines actions on behaviour

  • B.L Hart

    Biological basis of the behaviour of sick animals

    Neurosci Biobehav Rev

    (1998)
  • R.M Anderson et al.

    Regulation and stability of host parasite population interactions

    J Animal Ecol

    (1979)
  • R Dawkins et al.

    Arms race between and within species

    Proc R Soc B

    (1979)
  • E.W Ewald

    Evolutionary biology and the treatment of signs and symptoms of infectious disease

    J Theor Biol

    (1980)
  • J.W Templeton et al.

    Natural disease resistance in domestic animals

    J Am Vet Med Assoc

    (1988)
  • R.C Bolles

    Theory of motivation

    (1967)
  • I Kusher

    The acute phase response: From Hippocrates to cytokine biology

    Eur Cytokine Net

    (1991)
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