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Animal Emotions

Hans Erhard

erhard@agroparistech.fr

Emotion – What’s that?

• intense but short-living affective response to an event, materialised in specific body changes.

• a behavioural component (a posture or an activity)

• an autonomic component (visceral and endocrine responses)

• a subjective component (emotional experience or feeling)

– which leads to subsequent adjustment of the behavioural and autonomic response

Dantzer, 1988

Problem: two definitions of ‘emotion’

• definition 1:

– strictly observable physiological and behavioural changes that occur under particular circumstances such as the appearance of a predator

• definition 2:

– the subjective conscious experience (fear) that we know we experience under conditions of danger

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

behaviour

physiology

emotion 2 emotion 1

Why does it matter?

• animal welfare, animal rights, human responsibility rests on: – kinship (similarity between people and animals, reincarnation?) – consciousness, cognitive abilities – emotions

• Jeremy Bentham (1748-1832) • English philosopher • a utilitarian

– right and wrong are determined by their contribution to overall ‘utility’

• a liberal who wrote for equal rights for women, abolition of slavery and ‘animal rights’:

• “the question is not, can they reason nor can they talk, but can they suffer”.

Animal well-being

• suffering

• implies that animals are capable of subjective, sentient experience

• Niko Tinbergen (1951): – “Although...the ethologist does not want to deny the

possible existence of subjective phenomena in animals, he claims that it is futile to present them as causes, since they cannot be observed by scientific methods”

– -> it is ‘unscientific’ !

How can we know if animals have emotions?

Conceptual framework for an objective study of emotions in animals relating to their cognitive processing (Désiré & Boissy)

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Dawkins: Different approaches to the problem:

• the functional approach

• the mechanistic approach

• combination of the two

• learning

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

1. The functional approach • examining the role of emotions in human behaviour

• then asking whether the function is the same in humans and non-humans

• possibility to apply Darwinian ideas to emotions and ask how emotions (in us and in other species) contribute to an organism's fitness.

• Fear, for example, is adaptive

– functions to increase fitness both in motivating an animal

• to remove itself from danger

• to avoid similar situations in the future

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

functional mechanistic combination

1. The functional approach

• Oatley and Jenkins (1998):

– appraisal

– action readiness

– physiological changes, facial expression, behavioural action

• Problem: so general it applies to plants and robots

functional mechanistic combination

Cuscuta europaea – Dodder, Cuscute d’Europe

Resource choice in Cuscuta europaea. C K Kelly Proc Natl Acad Sci U S A. 1992. 89(24): 12194–12197.

- appraisal of nutritional status of the host BEFORE feeding

- coiling when host of high nutritional status (accept) -grow away when host of low nutritional status (reject) either plants have emotions, or approach is not sufficiently specific

functional mechanistic combination

Emotions make us ‘move’? There is a difference between wanting

and liking K.C. Berridge

Measuring hedonic impact in animals and infants: microstructure of affective taste

reactivity patterns

Neuroscience and Biobehavioral Reviews 24 (2000) 173–198

functional mechanistic combination

Berridge 2000

Measuring hedonic impact

functional mechanistic combination

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Brain systems that mediate the hedonic impact of taste. These ‘liking’ brain systems have been identified by affective neuroscience studies that employed taste reactivity measures.

Berridge 2000

functional mechanistic combination

‘False hedonic candidates’ that fail to mediate hedonic impact (even if they mediate some other aspect of reward). These ‘wanting’ brain systems mediate the motivation to eat, but they do not cause hedonic or aversive shifts in taste reactivity patterns.

Berridge 2000

functional mechanistic combination

Wanting, linking and addiction

Incentive-sensitization model of addiction Schematic model of how ‘wanting’ to take drugs may grow over time independently of ‘liking’ for drug pleasure as an individual becomes an addict.

Berridge et al. Current Opinion in Pharmacology 2009, 9:65–73

functional mechanistic combination

2. Mechanistic approach

• physiological and behavioural changes when humans feel happy, sad etc

• do similar changes take place in non-human animals?

• argument by analogy

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

functional mechanistic combination

Frustration in chickens or: to not get what you want

• adult Brown Leghorn fowls were deprived of food and then frustrated by presenting food under a Perspex cover

• frustration caused a large increase in four indices of aggression in hens

• with any pair of hens only one showed an increase in aggressiveness (the dominant one)

• when frustrated, cockerels showed a large increase in overt aggression towards hens which they usually dominate passively

• aggression is elicited with repeated exposure to frustration

• aggression following frustration increases with food deprivation time preceding frustration.

Duncan & Wood-Gush 1971

functional mechanistic combination

To have or not to have ...

• dairy cows, given food from box

• after 7 h of fasting, box with food was offered

– open, giving access to food (12 cows)

– covered by Plexiglas, perforated to allow smell (12 cows)

• behaviour shown by x of 12 ‘no food’ cows:

– vocalisation 5

– head shaking 6

– tongue rolling 4

– aggression 10

Sandem, Braastad, Bøe, 2002. Eye white may indicate emotional state on a frustration–contentedness axis in dairy cows . Applied Animal Behaviour Science: 79: 1-10

functional mechanistic combination

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Frustration and satisfaction

The percentage of white in the eyes of fed and food deprived cows during a 6 min test (mean±S.E.). straight line: a neutral situation, i.e. when no specific stimulus is introduced to the cow dotted line: food continuous line: no food.

Sandem, Braastad, Bøe, 2002

functional mechanistic combination

• physiological and behavioural changes when humans feel happy, sad etc

• do similar changes take place in non-human animals?

• 3 systems:

– cognitive/verbal

– autonomic (heart rate, temperature, hormone levels)

– behaviour/expressive (behaviour, facial expressions)

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

functional mechanistic combination

• physiological changes linked to required action

– afraid and running away

– excited and running towards

• multiple routes to action:

– breathing either automatically or consciously

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

functional mechanistic combination

3. Combination of functional and mechanistic approach

• we can see if the animal is running away or towards

• but can we really know if they perceive the stimulus as negative or positive?

• behaviour can have evolved as automatic response

- - > learning (reinforcement learning; operant conditioning)

behaviour linked to arbitrary stimuli

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

functional mechanistic combination

Reinforcement learning

• “the ability to change behaviour as a result of experience so that behaviour is controlled by completely arbitrary stimuli, quite unlike anything that natural selection could have built into the organism.” (Dawkins, 2000)

• reward or punishment system:

– reward makes me feel good

– punishment makes me feel bad

• link with fear, very old brain regions

Marian Stamp Dawkins (2000), Animal Minds and Animal Emotions, Amer. Zool., 40:883–888

functional mechanistic combination

Neural Pathways underlying Fear Conditioning

• convergence of the CS and US pathways onto single cells in the lateral nucleus of the amygdala (LA) • the LA then connects with the CE both directly and by way of other amygdala regions (not shown). • outputs of the CE then control the expression of fear responses, including freezing behavior and related autonomic nervous system (e.g., blood pressure and heart rate) and endocrine (pituitary-adrenal hormones) responses. • CE central nucleus; CG, central gray; LH, lateral hypothalamus; PVN, paraventricular hypothalamus. From Medina et al. (2002).

Phelps & LeDoux, 2005

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• subjective conscious experience?

• not only electric shocks, but other component

• emotion?

Learned helplessness

• inescapable shock can lead to ‘learned helplessness’

• animals will not show escape behaviour when in a threatening situation

• model for depression

Environment of newly hatched chicks

• When held gently in human hands, newborn chicks exhibit a comfort response consisting of the cessation of vocalizations and eye closure.

• These effects are weakened by opiate receptor blocking agent naloxone, indicating internal opioids help mediate contact comfort responses

Panksepp 2005

Playtime

de Jonge et al 2008. Applied Animal Behaviour Science 115: 138–148

Boredom? Fear and play

• A single exposure to a small 20 mg sample of cat hair on the 5th day of testing inhibited rat rough and tumble play completely

• this contextual fear response continued for up to 5 subsequent test days

– at higher levels with the measure of pinning (bottom)

– less with the dorsal contact measure of play solicitation (top).

Panksepp 2005

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Weaning: breaking the mother-young bond

• locomotion

• vocalisation

• increase of visible eye white in cows (decreases when reunited with calves or treated with diazepam)

• altered feeding and sleep patterns

• suspension of play

• elevated corticosteroid levels

• changes in heart rate and core body temperature

Ways to ease the effect of weaning

• allow periods away before weaning (pigs)

• gradual weaning (anti-suck devices plus fence-line weaning)

• maybe human contact (depends on human)

• social environment (siblings, friends)

• remove mother, not offspring

Newberry & Swanson 2008

• A three-month-old baby died in its mother’s arms earlier this month. For hours the mother, Gana, gently shook and stroked her son Claudio, apparently trying to restore movement to his lolling head and limp arms. People who watched were moved to tears — unfazed by the fact that Gana and Claudio were “only” gorillas in Münster zoo, northern Germany.

The Sunday Times, 24 Aug 2008

• Is what you feel your emotion or the animal’s emotion?

Mendl, Burman, Parker and Paul, 2009. Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying

mechanisms. Applied Animal Behaviour Science 118: 161-181

• the emotion of fear includes

– the subjective experience of fear, but also

– the expression of freezing or fleeing behaviour,

– alterations in physiology such as

• changes in heart rate, blood pressure, and circulating glucocorticoids

• We can ask other humans, but can we ‘ask’ animals how they feel?

Common indicators of animal emotional states

• behaviour:

– approach/avoidance behaviour

– vocalizations

– play behaviour

• behavioural tests such as

– open field

– elevated plus maze (EPM)

– light–dark box test

• indicators of hypothalamic–pituitary adrenal (HPA) and sympathetic–adrenomedullary (SAM) activity (stress)

Neural correlates of emotional responses

• in humans:

– primarily functional magnetic resonance imaging

• in animals: range of techniques including

– single-cell recording, lesioning studies, microdialysis

• many brain areas, including:

– amygdala, prefrontal and orbitofrontal cortex (OFC), anterior cingulate, insula, nucleus accumbens (NAc), ventral tegmental area, and periaqueductal grey

• brain systems such as:

– the dopamine, noradrenaline, opioid and serotonin systems

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Cognitive component of emotion

• cognitive processes influence and are influenced by an individual's emotional state

• ‘cognitive’ refers to: – information processing including attention

– learning

– memory

– decision-making

• examples

Judgement bias

• people in a negative state are more likely to make negative judgements about future events or ambiguous stimuli (‘pessimism’) than people in positive states who show more optimistic judgements and interpretations

Cognitive bias

• the influence of affect on a range of cognitive processes including attention, memory and judgement

Judgement in animals?

• the Crespi effect (1942)

• rats run for a high or low reward

• then they get the other level

• emotion?

low > high high -> low

Judgement Bias

• bad mood negative judgement (‘pessimism’)

• good mood positive judgement (‘optimism’)

Cognitive Bias

good bad ? ‘optimist’ will go there ‘pessimist’ will not or slowly approach

‘optimist’ good welfare

‘pessimist’ bad welfare

Judgement bias

Experimental paradigm for the original cognitive (judgement) bias task (Harding et al., 2004).

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• two housing conditions:

– predictable: ‘good’

– unpredictable: inducing mild stress/depression like state

Mendl, Burman, Parker and Paul, 2009. Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying

mechanisms. Applied Animal Behaviour Science 118: 161-181

Proportion of cues responded to with a lever press (a), and latency to lever press (b) during test sessions in which rats were presented with either training cues (‘food tone’ = tone predicting positive event (food); ‘noise tone’ = tone predicting negative event (white noise)) or ambiguous probe cues. During this phase of the study, subjects were kept either in unpredictable (filled circles) or predictable (open circles) housing conditions (see text for details). Harding et al. (2004) Nature 427, 312

Emotions – Can we measure them?

• “Not everything that counts can be counted, and not everything that can be counted, counts.” Einstein

• The scientific experience of the world must seem a bit like watching a football match at night, with a single spotlight instead of floodlights.

• ‘you don’t read poetry with a microscope’

• many scientists: we cannot get access to internal states of other individuals, human or animal, only about our own

• Calm down! - I AM CALM!!!!!!!

• Darwin said there was continuity in evolution, so the differences between species are differences in degree rather than differences in kind. They’re shades of grey. (Marc Bekoff)

Summary

• scientists will keep arguing about emotions

• others use animals as models to work on medication for the treatment of human emotions

• there are many parallels, physiological and behavioural, between humans and animals

• “Occam’s razor Lex parsimoniae: among competing theories, the one that makes the fewest assumptions should be selected

• there are ways of making the daily lives of animals better that don’t need too many theories