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«October 2009 SCIENTIFIC COORDINATOR Pierre Le Neindre, Senior research scientist, INRA (French National Institute for Agricultural Research) ...»

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One question posed to breeders is whether reared species have the ability to "perceive" the emotional states of other animals reared with them. In the specific case of negative emotions triggered by noxious stimuli, the question is whether or not the perception and interpretation of distress signals (postural visual cues, olfactory cues, vocalizations) can alter the behaviour of the animals receiving the signals. Experimental data in mice show that the response to pain may vary with the status of the individuals present (familiar, unfamiliar, dominance relationship...) and is modulated by a genetic component. It is the same for the existence of specific reactions to distress calls by the offspring of the species. This has probably led some authors to prematurely adopt the idea that there is a form of empathy in some species. In this interpretation, the emphasis is placed on the role of emotional reactivity among conspecifics. It should be remembered that the concept of empathy comes from observations initially made with primates. If we want to extend this capability to all animals, especially to farm livestock, this will require confirmation based on experiments with each species. Extending the proposition that empathy exists in all animals (especially in farm livestock) requires confirmation based on experiments with each species.

Modulation by inter-species relationships: the incidence of the human-animal relationship on the expression of pain in animals Several review articles show how animals and humans develop inter-individual relationships, especially in the case of experimental animals and farm species. Recently, the cognitive abilities involved in communication between humans and animals (dogs, horses) have received particular interest, e.g. the existence of reciprocal attention between humans and animals. The subjective interpretation of the situation determines the animal’s reaction. This is particularly true for their emotional perception of humans. Animal fear of humans has been studied in particular because of its effects on animal behaviour, physiology, and production capacity. Pain, as a perception of a physical threat, may be influenced by the human-animal relationship, especially if animals are afraid of humans. This fear is genetically inheritable but it is also influenced by the individual’s previous experience. Thus, the animal can easily associate the pain due to a specific veterinary or farm procedure with the presence of a specific person and remember it.

Fear is an emotion that is defined as the perception of a real or potential danger and which prepares the animal to face it. However, fear is not the only emotional state that can be investigated and which may affect the responses of animals to humans and to painful procedures. Animals can indeed perceive certain situations positively and have positive emotions in the presence of humans. These situations may improve the human-animal relationship and enhance approach responses towards humans. Some types of human contact may generate positive emotions in animals. For instance, studies have shown that tactile interactions, mimicking positive allogrooming between animals, diminish heart rate and induce relaxation postures, and facilitate contact with the animals. The presence of humans in such conditions can reduce pain perception by animals. Studies on this topic, however, are still scarce.

Pain in the mammalian foetus In order to feel pain, all animals must: i) have fully functional neural structures allowing the detection of noxious stimuli from the environment or from within the body, their transmission to brain structures and their expression as sensations ii) be able to reach a state of awareness iii) be able to identify the characteristics, the intensity and the duration of noxious or stressful stimuli in order to perceive them at the cognitive and emotional levels as an aversive experience. While for mammals, adults and their fully-grown young are generally considered as sentient beings, the question remains for young that are still neurologically immature and foetuses.

In a review on the physiological characteristics of foetal sheep, New Zealand scientists put forward the theory that the sensory environment in utero maintains the foetus in a state close to permanent sleep, in other words, the individual would be unconscious. They concluded that states of awareness and alertness are not reached until shortly after birth. During the birth process, profound changes in auditory, visual, tactile and thermal sensory inputs trigger the process of awareness and the onset of consciousness, making the young a sentient being.

34 Expertise scientifique collective "Douleurs animales" 2.4.2. Concepts associated with pain in animals Definition of suffering in animals Some researchers suggest that suffering may be experienced when the conditions imposed on the animals prevent them from “fulfilling their life project” or in other words performing the natural behavioural pattern of their species.

The needs of a species are considered as covered when their behavioural repertoire can be expressed entirely.

Experimental data indicate that when animals are prevented from displaying some behaviours, their natural drive for action evolves into tension that pushes them to react in an unsuitable manner, that may cause frustration and discomfort. This is the case for animals reared in restricted and impoverished environments in which they cannot display all the behaviours that are typical of their species. Such a state of psychological distress, which is not associated with tissue damage, may result in the animal developing stereotypies, which are repetitive acts expressed without apparent objectives. In other cases, apathy or resignation dominate in an attitude reflecting the individual’s lack of interest in or concern about the surrounding events, illustrated by the absence of a reaction.





This type of psychological suffering is beyond the scope of the present assessment.

Definitions of animal welfare The European Community has been emphasising the ethical importance of animal welfare over the last twenty years by presenting it as a political concern and a collective cultural preoccupation. This impetus has been paralleled by a steady increase in research on welfare, both at national and European levels.

There have been many attempts to provide a definition of animal welfare. One of the first refers to a state of harmony between the animal and its environment. This equilibrium should lead to full mental and physical health, but the definition does not specify exactly what harmony is.

A second definition, widely adopted by scientists working on animal welfare, focuses on the adaptability of a species. It specifies that a high level of welfare is reached when adaptation to the environment can be achieved at low cost to the animal, e.g. without significant energy expenditure. On the other hand, if the adaptation processes require the animal to rely heavily on its reserves (e.g., extremely low temperatures, allocated space limiting the expression of some behaviours or generating social aggression) then the level of welfare is considered to be low.

Another definition, formulated for practical on-farm usage, assembles the criteria characterising farm animal welfare into major components. This approach puts emphasis on the environmental conditions and the level of care that all farmers should comply with. Thus animal welfare depends on the respect of five basic rules (Five

Freedoms):

• Freedom from thirst and hunger - by covering basic needs to maintain full health and vigour,

• Freedom from discomfort - by providing an appropriate environment,

• Freedom from pain, injury, and disease - by prevention or rapid diagnosis and treatment,

• Freedom to express normal behaviour - by providing sufficient space, proper facilities and a satisfactory social environment,

• Freedom from fear and distress - by ensuring conditions and treatment which avoid mental suffering.

More recently, the World Organisation for Animal Health (l’Office international de la santé animale: OIE) stated that “animal welfare is the result of a complex public organization with multiple components comprising scientific, ethical, economical and political dimensions." This definition, less focused on the animal than the previous ones, emphasizes the complexity of the human factors which determine the living conditions of the animals, including during transport.

Expertise scientifique collective "Douleurs animales" 35 2.4.3. Examples of transposition to non-mammalian species Factors in a phylogenetic approach to pain Humans have always been taken as a reference to understand what pain could be in a given animal species. This approach necessitates the combined use of criteria concerning the neural structures involved and the behavioural and cognitive abilities.

As a matter of fact, the criteria found in the literature depend on the authors’ scientific discipline. Thus, neurobiologists focus on behavioural, cognitive and neuro-anatomical features, while many ethologists and specialists in animal welfare favour the behavioural and emotional aspects, using only occasionally information on neural cues, or cognitive, sensory and motor performances.

Comparative anatomy of the brain (homology between species e.g., presence or absence of frontal, telencephalic, limbic, cingulate cortices...) and the comparisons of behavioural abilities between species suggest that non-human mammals feel pain. In contrast, the issue about the existence of pain is still debated in birds, fish and marine molluscs like cephalopods.

We will limit this section to key data that support the hypothesis for the existence of well-characterised pain, in contrast to nociception which is defined as a more restricted sensation lacking the emotional dimension and consciousness. The methodological difficulties that helped the experimental validation of a given position on nociception, emotion and awareness of sensation will be reported as will the scientific controversies.

Whether there may be forms of mental representation of the body’s state other than those described for mammals remains to be tested.

–  –  –

Table 1. Summary of the existence of perceptual phenomena associated with the concept of pain in the six categories of animals presented in this assessment, based on current state of knowledge Existence of pain in birds Comparative Anatomy Structures homologous to those involved in nociception in mammals are found in birds.

In particular, electrophysiological studies conducted in chickens and pigeons have shown that their nociceptors have similar properties to those found in mammals. The neural mechanisms described at the level of the spinal cord do not differ significantly from what is known in mammals, however, our current state of knowledge of birds is not as extensive as for mammals.

36 Expertise scientifique collective "Douleurs animales" Birds display strong behavioural and physiological responses (activation of the HPA axis and sympathetic system) when submitted to frightening situations, conditions of food frustration or social separation. Fear responses have been particularly well described. They are associated with an activation of brain structures quite similar to those described in mammals, and include the posterior pallial amygdala and the archipallium, which could be homologous to the mammalian amygdala, the nucleus of the stria terminal and the paraventricular nucleus of the hypothalamus. These activation processes do not rely on the type of stimulus but on the way the situation is assessed. In particular they are modulated by previous experience. The mechanisms involved in memory have also been studied, especially in the case of conditioned fear. Conditioned fear is an emotion provoked when an animal is put in an environment that has been previously associated with an aversive experience (e.g. electrical shock). As in mammals, conditioned fear activates the hippocampus in birds.

Neurobiological studies performed on pigeons have shown that situations generating nociception also trigger significant emotional responses, and the brain structures involved in these responses are similar to those reported in mammals. Chickens and pigeons that have been trained with a classical aversive conditioning protocol using tone-shock associations, later display exacerbated fear behaviour and an increased heart rate when they hear the sound alone. This response is blocked by lesions of the archipallium which, like the amygdala in mammals, is involved in the onset and the control of emotions. It appears that in birds the nociception system and the associated memory processes activate upper brain structures involved in the expression of emotions.

Nonetheless, it has been shown that cortical decerebration of chickens does not inhibit the protective postural behaviour of leg bending to avoid standing on a foot when it is made sore by intra-plantar injection of urate crystals.

This suggests that some of the protective behaviour is controlled at the level of the brainstem, thus, in the absence of any conscious emotional component.

Behaviours Very soon after hatching, birds display escape responses when confronted by a noxious stimulation. In response to a nociceptive stimulation, birds exhibit defensive behaviours and attempts to escape. If they cannot put an end to their aversive experience, they are overcome with exhaustion and apathy. Changes in posture are often observed in birds, with the appearance of limping and, as the severity of the lameness increases, a total reluctance

to move or inability to stand. Phasic changes in behaviour are observed in animals subjected to feather plucking:

initially, the animals are reactive, try to escape (jump up, flap their wings), or vocalize, while later on, they crouch down and remain motionless suggesting a state of resignation.



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