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. Summary of the multidisciplinary assesment Pierre Le Neindre, Emilie Bernard, Alain Boissy, Xavier Boivin, Ludovic Calandreau, Nicolas Delon, Bertrand Deputte, Sonia Desmoulin-canselier, Muriel Dunier, Nathan Faivre, et al.

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Pierre Le Neindre, Emilie Bernard, Alain Boissy, Xavier Boivin, Ludovic Calandreau, et al.. . Summary of the multidisciplinary assesment: Summary. [] INRA. 2017, 8 p. ￿hal-01736385￿

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Distributed under a Creative Commons Attribution - NonCommercial - ShareAlike| 4.0 International License ANIMAL CONSCIOUSNESS

SUMMARY OF THE MULTIDISCIPLINARY SCIENTIFIC ASSESSMENT-MAY 2017 Do ? Think? Have a story? Since antiquity, have contrasting answers to those questions. From the Nineteenth century onwards, on the of animals were enriched by scientific insights from evolutionary theory, , and cognitive . Meanwhile, animal consciousness remains controversial within the scientific community. In 2012, a group of leading felt the need to publish a manifesto entitled the “Cambridge Declaration on Consciousness” it states that “convergent evidence indicates that non- animals have the neuroanatomical, neurochemical, and neurophysiological substrates of conscious states along with the capacity to exhibit intentional behaviours”.

Current , including the outcome of this multidisciplinary scientific assessment, shows that animals possess a wide range of cognitive abilities associated with behaviours of varying complexity. The forms of consciousness observed in presuppose distinct cognitive abilities which are found in certain animals. Could it be concluded that animals possess some sort of consciousness similar, albeit not identical, to that of humans?

Research on levels and contents of consciousness in animals is emerging as a scientific topic of major interest due to its high level of complexity and associated controversies. Current scientific advances invite us to revisit ethical considerations regarding the relationships between humans and animals (domestic animals in particular).

In 2015, the societal and scientific context promoted Safety Authority (EFSA, in Parma, Italy), launched a reflection on animal consciousness and related key new multidisciplinary scientific assessment aiming . Following a previous INRA multidisciplina- to produce a critical updated review of literature on ry scientific assessment requested by the French mi- animal consciousness. The mandate recommended nistries of Agriculture and Research on “Animal ” focusing on farm animals. (2009), INRA, upon request of the European Food

Epistemological and philosophical issues of consciousness

Animal consciousness has been a research topic for minimize occurrence of pain in their life. Behind the philosophers for centuries. The philosophical ques- theme of animal lies the ethical issue of our tioning began as early as , continued with responsibility towards animals, that is, our responsi- Descartes and Rousseau, and today remains an ac- bility for their physical and mental well-. tive of research. Scientists began pondering on the issue much later and some were even very reluctant to consider it as a valid scientific issue. In What is consciousness in humans? the 19th century, naturalists such as Lamarck, Darwin As most research on consciousness has been, and and Romanes, and later comparative psychologists still is, conducted in humans, animal consciousness and ethologists such as Morgan and Griffin further cannot be explored without considering recent de- questioned the mental states of animals. Based on finitions and knowledge of human consciousness. their observations of behaviour, they came to the Human consciousness is typically defined as the conclusion that consciousness does occur in animals, subjective or phenomenal experience we have especially in . Research on biological and from our surrounding environment, own body psychological issues resulted more recently in several and/or own knowledge. We refer to this definition major conceptual innovations which established that when considering animal consciousness bearing in consciousness is the outcome of processes and that consciousness in humans is a subjective that it is a legitimate topic of scientific enquiry. and private experience communicated to others not only through but also through non-verbal We, as humans, are engaged in a continuous ex- means (i.e., behaviour). Although verbal language change of , services, and affectivity with provides adult humans with a domestic species (farm or experimental animals, or whose level of sophistication is unavailable to any pets). A certain kind of relationship can also at other species, animals – just as humans - rely on other occur with wild animals. Whatever their role is, we forms of non-verbal communication from which we need to understand their mental to ensure we can, to a certain extent, infer the properties of their treat them well, we respect their well-being and we consciousness.

2 The review done on human consciousness followed tential neural correlates of consciousness described, a two-dimensional analysis focused on level and defined as the neural mechanisms that are both ne- content. The level of consciousness refers to states of cessary and sufficient to bring about conscious expe- vigilance ranging from being in a to being fully rience. awake. The content of consciousness refers to the sub- jective experience associated with the of Two of the main theories of consciousness pu- internal and external sensory information, as well as blished so far are presented as a way to make cognitive processes that do not involve perception, of published empirical results; they both consider and to metacognitive processes (that are defined as consciousness as an emerging resulting the ability to consciously monitor and control one’s from interactions between nervous structures: own mental states). It is important to that le- vel and content of consciousness are related, as rich i) the , which suggests that contents of consciousness are usually observed du- consciousness involves the broadcasting of infor- ring , except for dreaming and specific mation by parieto-frontal , throughout the neurological disorders. After defining the levels and brain, to all the other nervous structures and particu- contents of consciousness, the contrastive approach larly telencephalic cortex (Figure 1). was presented as the main empirical method to study them. It relies on a comparison of behavioural ii) the integrated which assu- and neural responses measured under high vs. low mes that the of consciousness is the capacity levels or contents of consciousness. Based on this of the different nervous structures to integrate infor- contrastive approach, several behavioural markers mation. of consciousness in humans were reviewed, and po-

Figure 1 : schematic representations of interactions between telencephalic neurons in a conscious versus non-conscious according to the “global workspace theory” . (from Dehaene et al., 2006)

Side views of the human brain (frontal section on the left, occipital on the right)

NON-CONSCIOUS STATE CONSCIOUS STATE

neuronal structures in telencephalic cortex involved in the of conscious state (associated with increasing activities)

Top-down connections originating from parieto-frontal neurons

Other intra-cortical connections

3 Consciousness in animals

Some levels of consciousness in animals have Two kinds of are widely used in animals to already been acknowledged, notably by conside- study : those that evaluate metacogni- ring /awakeness as a modulator of the level of tive monitoring (the ability to judge one’s own state consciousness. There are however strong scientific of knowledge: the animal could in pushing buttons arguments in favour of extending such to express a positive or negative answer, or that it does the contents of consciousness, including perceptual, not know the answer, as tested with , poultry emotional, cognitive, and metacognitive capacities. or , see box 1) and those that are designed There are at least three issues that make this task a to measure metacognitive control (the ability to seek challenging one : information when lack of knowledge has been de- tected: ask for more information before answering). i) The absence of language in ani- Those are suggesting that some animal mals can be overcome by developing appropriate performances meet the criteria for metacognitive behavioural tests and comparative analysis of brain responses that appear homologous to conscious res- responses ; ponses in humans in functionally similar conditions. This was for instance observed in pigeons and hens. ii) The term ‘animals’ includes a large diversity of species, and , living in dif- ferent environments. In that context, one might an- Box1 ticipate that consciousness may take different forms among species ; Example of an experimental procedure to test animal metacognition iii) Most of the reported studies have not been originally designed to analyse consciousness in animals. Nevertheless, they can be discussed in In this experience, an (here a star) is first submit- relation to it. ted to an animal. The latter obtains a reward when, during the test phase, it finds, within a wider list of items, the one already been presented beforehand. The properties of animal consciousness The animal may choose not to go through the test and obtain a lower reward by conducting a simple action such as pressing a button. They have been analysed along five main domains:

Emotions are defined as modulators of cognitive Submission Delay Search for the Reward of an object object capacities involving changes in , judge- ment , or . The empirical proof that emotional responses occur in animals does not im- ply that they are systematically associated with consciousness. However, many animals, including fish, are capable of the same evaluation processes as those to trigger conscious emotions in hu- The authors observed that some animals (, pri- mans. For instance, studies on expectations of reward mates) systematically and properly engage in the task in sheep and pig clearly show that animals not only when it is an easy one. But when the task is made more respond to the intrinsic of a reward but also ac- difficult (by increasing the delay between the submis- cording to their previous experience with the reward. sion and the test phases or by increasing the number of Moreover, some animals such as cow and sheep, do tested items), they tend to decline more the task and experience and share with others a wide range of opt for the action which is assured to yield the less im- portant reward. emotions that might be consciously experienced. Such results show that some non humans animals have Metacognition is defined as “cognition about metacognitive skills and are able to assess the level of cognition”. That is the ability to monitor and their knowledge. It seems that they know whether or control one’s own cognitive processes. It is thou- not they know. ght to be a crucial component of -.

4 Processing of past and . cols and species studied, there is an agreement that is defined in humans as memory of autobiographi- many animals, are not only automatically reacting to cal events. It has been demonstrated by assessing the behaviour of conspecifics, but also use their past whether various animal species, especially primates, social experience and ongoing relationships to adjust corvids and , can characterize what, where their behaviour to reach immediate goals. This capa- and when, or in which context, they experience city requires mastery of sophisticated means of per- specific events. The characteristics of episodic-like ception, integration, , and communication, memory studied in animals have many similarities all of which are probably linked to consciousness. to episodic memory in humans, in both behavioural and neurobiological aspects. Moreover, recent stu- Human-animal relationships : With the recent in- dies of primates, corvidae and weasels indicate that tensification of studies on domestication and animal they can future actions independently of their welfare, human-animal have become a to- current motivational state and their innate tendency pic of scientific enquiry. Several studies developed to express certain behaviours, such as migratory be- in animals such as primates, dogs or sheep suggest haviour (box 2). that they are able to mobilize cognitive and emotio- nal abilities when interacting with humans to build a Social behaviour. Many animals live in groups of mental and functional representation of their human variable composition and size. Their group structure partners. Studies involving human-animal relations depends on social cognitive abilities. , par- highlight the potential role of an animal’s subjective ticularly among sheep and cattle, need to perceive experience of humans. Moreover, these studies show and recognise each other to build a reliable and pro- that distinct human individuals are differentially tracted relationship. Several examples of social beha- perceived by animals. The outcome is adapted, pre- viour were analysed. They address issues related to dictable and consistent emotional and behavioural the , which is the ability to infer the responses ranging from avoidance to bonding. This knowledge, and emotions of other animals indicates that conscious, rather than strictly prede- and underlying behaviours such as deception or em- termined and automatic processes, may emerge in pathy. Due to a wide variety of experimental proto- the development of human-animal relationships.

Box 2 Episodic memory in pig? from Kouwenberg et al., 2009

This is based on the fact that pigs prefer to (s) Less familiar explore unfamiliar objects depending on location and context. Objects A and B are presented to pigs as in the 150 More familiar sequence below :

100 A B 1st exposure phase : grey floor, object A on left side, objet B on right side

50 nd B A 2 exposure phase : white floor, object B on left side, objet A on right side

0 A A Test phase (4 trials) : white floor, object A on both right and left sides Trial 1 Trial 2 Trial 3 Trial 4

Mean spent by pigs exploring the less versus the more familiar object in the course of four trials. Pigs were exposed to objects A and B as well as white and grey floor backgrounds the same number of times. This experiment shows that pigs possess episodic memory Nevertheless, during the test phase, object A located on skills. This is borne out by their capacity to memorize the the left side is less familiar due to its left side location “what”, “where” and “when and in what situation” com- against a white floor background. It is this one that pigs ponents essential to episodic memory. preferentially explored.

5 Towards a neurobiological approach of animal consciousness A clear limitation of our current knowledge comes from the low number of species so far investigated, among which Following the review of empirical evidence regarding very few farm animals. The species considered, however, consciousness along the five domains described be- cover a broad spectrum from to vertebrates, fore, current studies explore the neural correlates it seems therefore reasonable to cautiously generalize our conclusions beyond the study cases. of consciousness in animals. A given dimension of consciousness is unlikely to be related to a single brain structure or neural network, as illustrated by research on and evolutionary process of humans. There are few comparative studies providing a direct mapping of behavioural performances of animals consciousness on specific neural substrates. In , recent evi- dence indicates that telencephalic cortical areas sharing Such heterogeneity of conscious processes in animals is rich connections with other parts of the brain may be not surprising when one considers the variety of challen- involved in consciousness. In birds and fish, such cortical ges which can be encountered in life and the accordingly considerable diversity of solutions evolved to adapt to areas are not present but functionally-related structu- contrasting physical, biotic and social environments. The res like the telencephalic or the mesencephalic question, in that context, is whether the cognitive abilities tectum may enable the animal to experience conscious engendering consciousness are the result of evolutionary content. The role of mid-brain nuclei, which are pre- processes. sent in all vertebrates, should also be stressed. In any They could also be the result of convergence in case caution is required when excluding the presence which has occurred in species not related phylogenetically, of consciousness in species that do not have the same thus having different neuronal structures, but facing equal brain structures as mammals, because different neural environmental constrains. may mediate comparable processes. The constant need to adjust to the environment might Review on the functional elements and the contents of ani- have exerted a selective pressure for consciousness to emerge, provided relevant brain develop- mal consciousness ments occur. Then the link between behavioural correla- tes of consciousness with specific neural structures across Several aspects of animal behavioural and cognitive ca- phyla seems difficult to assess. pacities allow us to sustain the of the occurrence of consciousness in animals and to sketch its content. Overall, Although a clear demonstration of an evolutionary role this leads us to conclude that these cognitive processes for consciousness is still lacking, one possibility is that indicate the of different forms of consciousness consciousness may have evolved because it provides a with variable degrees of complexity. As for humans, animal competitive advantage, allowing flexible answers to the consciousness might be best described as the emerging various challenges the animal should face. The precision product of interactions between different functional layers of the mental representations of the environment is crucial constituted by perceptual, attentional, mnesic, emotional for the animal to be able to choose the appropriate beha- and evaluative competences which revolve around a cen- viour to a given situation. tral node supporting core regulations involved in vigilance After reviewing current evidence on the role of and central rhythms. Upon the perception of a of consciousness in adaptive processes, the issue of its evo- interest, several of these layers are activated and interact lutionary emergence across different animal phyla was to ultimately produce interpretations and raised. Conceived as a global workspace to cope with the which are externalized through the expression of conscious complexities of life, consciousness may be seen as a fun- actions. Thus, processes related to consciousness allow damental feature of animals which appeared and evolved the emergence of responses which have greater com- independently in different phyla and multiple times. plexity and content than the simple combination or ad- dition of responses of separate systems.

Depending on the animal species or external factors consi- dered, consciousness may fluctuate from: Conscious perception of sensory signals relative to pain i) low contents: involving fewer brain structures and lower levels of complexity as well as limited associative The recognition of a conscious processing of sensory in- learning capacities, formation relative to pain by animals and humans, raises questions regarding the consequences of the perception ii) to high contents: involving numerous brain and the processing of pain by animals. structures and complex integrative processes, more deci- sion making processes, numerous functional layers, highly Recent knowledge on perception should be taken into ac- flexible associative learning. This make conscious action count from an ethical point of view when considering the and learning possible. use of animals by humans.

6 Among sensory information arising from the body, pain Future research has a particularly high potential to interrupt attention or modify behaviour. Pain represents a nociceptive1 sensa- Because research in the field of animal consciousness was tion associated with a negative affective sensation. Most until now focused on a small number of species of mam- animal species, including birds and fish, are equipped to mals and birds, it would be desirable to fill these gaps by detect and react to noxious stimuli. Mammalian animals widening the field of investigation to a larger range of share with humans most of the brain structures involved species, in particular vertebrates, including fish. in the conscious perception of pain including its negative affective component. Avian and fish have homologs To improve our of the mechanisms of their of mammalian brain structures that are likely to enable mental functioning, experimental protocols strive to them to experience pain consciously. While invertebrates distinguish between those behavioural and physiological obviously react to noxious stimulus as well, presence of answers of animals, that stem from conscious behaviour subjective negative affective experience related to pain from those associated with acquired automatisms (which is still debated in invertebrates which are much less stu- can be complex). died. Thus, current knowledge suggests that at least ver- tebrates are equipped with nervous systems that support Experiments uncovering analyse on the one hand, the conscious processes of complex information, including contents of consciousness, and on the other hand, the negative emotions caused by noxious stimuli. levels of consciousness, are needed. It would also be use- ful to study why, and to what extent, certain cognitive Ethical issues capacities, that allow the presence of elaborate contents of consciousness, are found among phylogenetically un- This current knowledge has to be taken into account related species and/or among species with very different when considering ethical issues related to humans use neuronal structures? of animals, or relationships. Most philosophical theories in animal consider that , referring to the As regards farm animals, a better understanding of their capacity to experience and , constitutes mental world, the way they represent themselves and a relevant criteria when considering the moral status of their world and how they relate to their environment animals. Beyond sentience, which is the minimal level of would enrich our thinking on how to improve their well- consciousness, our understanding of consciousness occu- being and the way they are handled. pies a pivotal role in defining what to animals and the different aspects of their mental life. While sentience It would therefore be useful to explore high cognitive may be widespread among animals, more elaborate skills involved in self-consciousness, consciousness of contents of consciousness have only been documented an individual’s own knowledge and of other individuals’ across a small range of species, among primates, corvidae, knowledge (theory of mind), including an individual’s ca- rodents and ruminants. Such higher contents need in par- pacity for , metacognition, consciousness of time ticular autobiographic memory, or episodic memory. Be- (the ability to distinguish present past and future), as well cause animals with autobiographic memory, as observed as attention, memorization and motivation. Such research in primates, corvidae and rodents, can have and should also include studies of the so-called positive fee- goals that extend into the past and the future, they can lings. be negatively affected by aversive experience. The diffe- rent levels and contents of consciousness documented in The study of the development of the forms of consciousness animals should give rise to commensurate ethical consi- at a young age is particularly important for farm animals, derations, especially regarding domestic animals used in which have generally a brief life. It would be advisable to farming, research, , sports or companionship. develop the understanding of the impact of the events being up from the first days to first weeks of life.

Conclusion The nature of the relationships of animals with the hu- mans who raise them should also be studied in domesti- Animals of diverse species display a diversity of various cated species. abilities in terms of consciousness. Some research could be inspired by studies on humans, This multidisciplinary scientific assessment does not both at the level of the concepts and of methods of inves- equate the contents of consciousness described in hu- tigation. In particular, technologies studying neurobiolo- mans with those occurring in animals. However, the ove- gical mechanisms, such as functional imaging, could be rall picture provided by this collection of behavioural, co- adapted to animals when it is technically possible. gnitive and neurobiological studies supports the that, high content of consciousness does occur in some of the species studied so far.

1. Relative to the perception of stimulations generating pain 7 Scientific assessment method

The analysis of the available scientific and philosophical academic knowledge was based mainly on published li- terature, after an extensive bibliographic search partly retrieved from the Web of ScienceTM Core Collection (WOS) database. The report ends with a total of 659 references, 75% of which from international scientific journals, and 33% of which were published after 2010; it also references 60 books, including philosophy books.

Assessment organisation The other experts are listed in alphabetic order: Alain BOISSY (INRA Theix), Xavier BOIVIN (INRA Theix), Lu- This multidisciplinary scientific assessment was pro- dovic CALANDREAU (INRA Nouzilly), Nicolas DELON duced upon request of AHAW unit of the European (New York University), Bertrand DEPUTTE* (Emeritus Food and Safety Authority (EFSA) (contract number Veterinary School Maisons-Alfort), Sonia DESMOU- EFSA/INRA/2015/01). INRA’s Delegation for Scientific LIN-CANSELIER (CNRS Nantes), Nathan FAIVRE* (CNRS Expertise, Foresight and Advanced Studies (DEPE), a Paris), Martin GIURFA (CNRS Toulouse), Jean-Luc GUI- division of INRA in Paris headquarters, coordinated CHET (Beauvais University ), Léa LANSADE (INRA-IFCE the work of seventeen French experts from different Nouzilly), Raphaël LARRÈRE (INRA Paris), Pierre MOR- scientific fields (biologists, cognitivists and philoso- MÈDE* (INRA Toulouse), Patrick PRUNET* (INRA Ren- phers) and of various affiliations. The report followed nes), Benoist SCHAAL (CNRS Dijon), Jacques SERVIÈRE INRA’s guidelines. (INRA Paris), Claudia TERLOUW* (INRA Theix). *: chapter coordinators Scientific coordination was provided by Pierre LE NEINDRE, INRA Director of research, together with Members of the review committee: Robert DANTZER Muriel DUNIER (DEPE project leader, INRA Paris), the (University of Texas, MD, Anderson Cancer Center, bibliographic search was done by Emilie BERNARD Houston, USA), Linda KEELING (University of Uppsala, (INRA Rennes) and the budget management by Kim Sweden), David LINDSAY (University of Perth, Austra- GIRARD (DEPE, INRA). lia) and Virginie MICHEL (ANSES, Ploufragan, France).

For further details :

The multidisciplinary scientific assessment report has been published in theEFSA Journal on Wiley http://www.efsa.europa.eu/en/publications and on the INRA website.

INRA multidisciplinary scientific assessment on Animal” pain : identifying, understanding and mini- mising pain in farm animals” (2009) Pierre Le Neindre, Raphaël Guatteo, Daniel Guémené, Jean-Luc Guichet, Karine Latouche, Christine Leterrier, Olivier Levionnois, Pierre Mormède, Armelle Prunier, Alain Serrie, Jacques Servière. The full report (242 pp in French), 98 pp summary and 8 pp synopsis

Conception - graphisme : Elodie CARL - graphisme Conception are available on the INRA website

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