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Appendix to Chapter 3 - Animal Emotions

Back to chapter page Body of chapter 3 Conclusions References

1. Should we stipulate consciousness as a requirement for having emotions?
2. Is emotion fundamentally distinct from cognition?
3. Do the basic emotions of fear, anger and desire presuppose a capacity for language?
4. Can emotions be explained as bodily states?
5. Deficient methodologies for distinguishing animal emotions
6. What kinds of emotions do animals have?
7. Which Animals Have Emotions?
8. A general strategy for identifying occurrences of basic emotions in animals


1.Should we stipulate consciousness as a requirement for having emotions?

In this chapter, I refrain from discussing the question of whether emotions in animals are accompanied by phenomenal consciousness.

Scientific reasons for caution on the subject of consciousness include the following:

(i) the lack of an interdisciplinary consensus on the role of consciousness in emotion - among neurologists, the view of LeDoux, that "[t]he brain states and bodily responses are the fundamental facts of an emotion, and the conscious feelings are the frills that have added icing to the emotional cake" (1998, p. 302) is a common one;

(ii) recent research with human subjects showing that subliminal exposure to happy or angry faces - which the subjects were later unable to recall - had a dramatic influence on their subsequent emotions, such as their liking for a fruit beverage, how much they wanted to consume, and how much they would be willing to pay for it if it were sold (Berridge, 2003b);

(iii) research cited by Berridge (2003b), showing that anencephalic infants, whose brains lack cerebral hemispheres and possess only a functioning brainstem, display positive emotional facial reactions (e.g. lip sucking, smiles) to sweet tastes and negative reactions (e.g. gapes, nose wrinkling) to bitter tastes. According to the American Medical Association and American Academy of Neurology, these infants are congenitally incapable of consciousness, although Shewmon (1999) upholds a contrary view;

(iv) the rigorous scientific criteria which Panksepp (1998) has defined for identifying emotions in animals can be applied to animals, regardless of whether or not one endorses Panksepp's own personal view, that there is a "core consciousness" at the heart of every animal emotion which is purely affective and devoid of intrinsic cognitive content. This notion is philosophically controversial, as it seems to imply that feelings evolved in animals prior to cognition, and that the basic animal emotions therefore have no cognitive requirements whatsoever.

In the interests of fairness, I should acknowledge that there is a substantial body of evidence for the occurrence of phenomenal consciousness in mammals and birds, as we shall see in chapter 4.

Finally, I contend that emotions possess a number of well-defined properties (listed below) which make them much more philosophically tractable than the notoriously elusive notion of (phenomenal) consciousness. To stipulate that any adequate definition of animal emotion has to include the notion of consciousness is therefore equivalent to putting the cart before the horse.


2. Is emotion fundamentally distinct from cognition?

Certain influential philosophical theories of emotion characterise emotions using cognitive terminology. For cognitivists, emotions necessarily involve having propositional attitudes towards certain statements. Some cognitivist theories construe emotions as judgements. In appraisal theories, emotions are typically characterised as evaluations.

Regardless of what sort of (conscious or unconscious) cognitions these theories use to characterise emotions, they all collapse in the face of the weighty neurological and behavioural evidence that has been amassed, showing that emotion and cognition are indeed fundamentally distinct.

Neurological arguments for a distinction between emotion and cognition

LeDoux (1998) marshals several lines of argument to the effect that the neural processing for cognitive and emotional responses is quite distinct, which refutes the view that emotions are simply (conscious or unconscious) cognitions. For example:

The fact that emotional processing in the brain seems to occur independently of cognitive processing might seem to suggest that emotion is completely independent of cognition. But in fact, as LeDoux (1998, p. 166) points out, when a hiker encounters a snake while walking in the woods, what happens first is that some low-level "quick and dirty" cognitive processing of sensory data occurs in the thalamus (which identifies "gross" features such as objects that look vaguely like a snake) before the information passes to the amygdala (which mediates the emotional response) and independently, to the visual cortex (which handles the "fine-grained" cognitive task of identifying the stimulus as a snake). The outcome of the cortex's processing is fed back to the amygdala as well.

Behavioural arguments for a distinction between emotion and cognition

The main behavioural argument for a distinction between emotion and cognition is that cognitive processes, in the absence of emotions, are incapable of motivating animals to act. Aristotle seems to have made essentially the same point in his De Anima 3.10, where he argued that of the two things that seem to cause movement in animals - desire and practical thinking - desire is the crucial factor, as thinking cannot move an animal in the absence of an object of desire.

Damasio (1994) has also documented several case studies in which subjects who had a diminished capacity to experience emotion, owing to injuries sustained in the prefrontal and somatosensory cortices of the brain, were severely hampered in their ability to make intelligent practical decisions.

Similarly, Evans (2001) contends that the vital role of emotions in agency can never be replaced by reason alone. He argues that a race of creatures with a capacity for logic but no emotions, like Dr. Spock in Star Trek, would be non-viable:

It should be clear by now that a creature totally devoid of any emotional capacity would not survive for very long. Lacking fear, the creature might sit around and ponder whether the approaching lion really represented a threat or not... Lack of disgust would allow it to consume faeces and rotting food. And without the capacity for joy and distress, it might never bother doing anything at all - not a good recipe for survival (2001, p. 62).

I conclude that animal emotions cannot be reduced to cognitive states such as judgements or evaluations, whether these states be conscious or unconscious. Cognitivist theories and appraisal theories of emotion are therefore inadequate.


3. Do the basic emotions of fear, anger and desire presuppose a capacity for language?

Before we conclude our discussion of the identification of basic emotions in animals, we have to address arguments purporting to show that these emotions presuppose feats of rationality and language that non-human animals are incapable of. I argue that on the contrary, non-human animals can and do satisfy the core cognitive requirements for these emotions, without requiring language.

Cognitive requirements of fear

It has been argued that fear, in the fully-fledged sense of the word, has to be amenable to reason.

Leahy (1994, p. 136) claims that when we ascribe fear to animals and to rational human beings, we are playing two distinct language games: human fear is amenable to reason whereas animal fear is not. People can be argued out of their fears if they can be shown to be groundless, but animals cannot. The object of an animal's fear operates not as a reason for its behaviour, but rather as a cause of its behaviour (1994, p. 135). Indeed, Leahy considers the dissimilarities between animal and human fear to be so profound that one could justifiably use two distinct words to differentiate them. In the end, he decides to use one verb to describe both cases, but only because the similarities in the overt behaviour of frightened people and animals are so profound.

I have several comments to make in response to Leahy's claims. First, it would be grossly mistaken to view the similarities between human and animal fear as merely behavioural, as Leahy seems to do (1994, pp. 135-136). Animal fear cannot be cashed out in dispositionalist terminology which describes external behaviour. The fact that scientists routinely perform research on animals to discover the causes of and treatments for fear in humans (LeDoux, 1998; Hall, 1999) would make no sense unless the internal neurological and affective states accompanying fear were substantially the same in humans and other animals.

Second, when contrasting human fears with those in other animals, it is essential to compare like cases. Once we do so, we find that fear, properly speaking, is amenable to reasoning in humans only under restricted circumstances. The inability of other animals to reason their way out of their fears then becomes far less anomalous.

There is a growing consensus among psychiatrists (see Catherall, 2003, pp. 76-78) that there is a significant difference between fear and anxiety in both humans and animals: fear is a response to a present danger (e.g. a predator) that is triggered by perceptions (e.g. the sight of a lion), while anxiety (or worrying) is a response to potential threats that involves cognitions rather than perceptions. The point is that because fear, unlike anxiety, is processed within the brain independently of higher-level cognition, fear behaviour is typically involuntary, even in human beings.

Behavioural responses to innate fears, such as the fear of a predator, are involuntary in humans as well as non-human animals. These fears have evolved in response to stimuli that consistently threatened our survival during evolutionary history (Panksepp, 1998, p. 207). These innate fears are tailor-made to circumvent the need for reason and other cognitive inputs, in both humans and animals. In LeDoux's (1998, p. 166) earlier example of a hiker in the woods who abruptly encounters a long thin object in his path and jumps clear, - even before the visual cortex in his brain has had time to ascertain that it is indeed a snake and not a stick, - the ability to respond rapidly may make the difference between life and death.

Conditioned fears in humans and other animals are also largely involuntary, because fear memories are stored in the brain's amygdala, from which they can never be erased (LeDoux, 1998, p. 146; Hall, 1999). There is a good evolutionary reason for this: the brain's ability to recall stimuli associated with danger in the past assisted individuals' survival (LeDoux, 1998, p. 146). According to LeDoux (1998), the only way to eradicate a fear acquired through conditioning) in non-rational animals, is to repeatedly expose the animal to the conditioned stimulus in the absence of the unconditioned stimulus. The same approach is used in the first phase of treatment for humans suffering from post-traumatic stress disorder (Catherall, 2003, pp. 84-87). Eventually, this leads to "extinction" of the fear response. In reality, however, the fear is merely dormant, and may be re-awakened simply by exposure to some stressful or traumatic event (LeDoux, 1998, p. 145). Conditioned fears prove to be equally indelible in people who develop phobias. Phobias show only limited "amenability to reason": psychotherapy allows the fear of the phobic stimulus to be kept under control for several years, but after some stress or trauma, the fear returns in full force, just as it does in animals. Therapy, like extinction, cannot erase the memory (LeDoux, 1998, p. 146). The differences here between humans and other animals hardly deserve to be called a new "language game".

The study of fear disorders in human beings sheds further light on why they are not amenable to reason. Catherall (2003) points out that while anxiety disorders can be treated on a cognitive level (as in insight therapy), fear disorders cannot, because exposure to a traumatic stimulus triggers changes in the brain which prevent reasoning and language processing. PET scans show that in a subject exposed to a traumatic stimulus (e.g. a snake), the speech area of the brain (Broca's area) may be deactivated, making it impossible for the subject to access his explicit or declarative memory and deal with the fearful stimulus by recalling facts ("It's a green tree python, so it can't poison me") that would alleviate his fear. This kind of cognitive processing is only possible while the individual's fear state remains below a certain threshold (Catherall, 2003, pp. 79-80).

Thus Leahy's contention (1994, p. 137) that people (unlike animals) can be argued out of their fears if they can be shown to be groundless, is true of anxiety rather than fear as a whole. Only low-level human fears are "amenable to reasons" (Leahy, 1994, p. 135).

It should not be thought that fear behaviour in non-human animals is totally inflexible. In fact, we find a suite of adaptive behaviours to fear in animals. First, animals can lose their fear of an object through a process of habituation.

Second, animals lose their fear of an object if a change in perception reveals that it was not the danger they thought it to be.

Third, animals living in hierarchical societies are capable of learning from experience, that they need no longer fear formerly dominant conspecifics that lose status.

Fourth, juvenile animals can learn specific skills for avoiding things they fear - such as predators.

Is there, then, any minimum level of adaptability that we should expect in an animal capable of intentional agency, which is undergoing the emotion of fear? Habituation does not seem particularly impressive: as we saw in chapter two, it is not one of the behavioural conditions for intentional agency. By contrast, an animal's ability to use incoming sensory data to self-correct its behaviour is an integral part of the mechanism of intentional agency, be it operant conditioning, spatial navigation, tool use or social learning, and should therefore feature in even a minimal definition of fear as a mental state.

Before it can be credited with fear at its lowest cognitive level, an animal must not only be capable of intentional acts enabling it to avoid some dangerous stimulus, but also be capable of adjusting its behaviour when new sensory data reveal the stimulus to be harmless.

It is certainly true that humans have a unique capacity to control their fears - even innate ones. Most of us have sufficient control over our fear of snakes that we can pick up a green tree python, which we know to be harmless, and a few individuals can even conquer their fears enough to handle poisonous snakes. But what these examples show is the uniqueness of human cognition, rather than human emotion, as we re-define what is and is not dangerous ("That green snake won't hurt you; it's harmless.") Humans, unlike other animals, are capable of modifying their behaviour on the basis of information conveyed through the medium of language: we have been taught that despite appearances, green tree pythons will not hurt us, and even cobras can be handled safely. A non-human animal knows that snakes are dangerous, but because it lacks language, it cannot explain precisely why they are, and thus it is incapable of understanding why its innate fear response to green tree pythons is inappropriate.

Language also allows human beings to rationalise stimuli that might otherwise frighten them. According to Grandin (1997), prey animals (including horses and cattle) have an innate tendency to acquire fears of things that look out of place (even a piece of paper blowing in the wind), sudden movements (which resemble the movements of predators) and high-pitched noises. But even though these animals cannot tell themselves that there's nothing to be afraid of, there is no reason to doubt the reality of their fear.

Cognitive requirements of anger

The difficulty in ascribing anger to animals arises from the advanced mental states that anger appears to require. Thus Aristotle defined anger as "a longing, accompanied by pain, for a real or apparent revenge for a real or apparent slight... when such a slight is undeserved" (1959, The Art of Rhetoric, 1378a, J. H. Freese (tr.), London: William Heinemann). Leahy (1994, p. 80) argues that these cognitive requirements are beyond the competence of non-human animals, and that it is only their enraged behaviour that resembles that of angry human beings.

Two comments are pertinent here. First, instead of saying that only undeserved slights can elicit anger, it would be better to say that the knowledge that a slight is deserved can reduce (and perhaps obviate) anger. Of course, most animals, like very young human infants, lack the concept of "just deserts", so their feelings of rage cannot be assuaged in this way.

Second, Aristotle's definition of anger is too narrow: he focuses on "slights", or insults, but in human life, one may feel anger at another individual for a variety of reasons: a slight, an action that gave offence without being intended to do so, some sensory irritation ("He has terrible body odour") or a physical obstruction ("I wish he'd get out of my way").

Third, we can speak of various "cognitive grades" of anger. A human longing for revenge against a mortal enemy is obviously of a much higher grade than the momentary surge of anger an infant may feel towards an "offending" individual who is thwarting her wishes (e.g. by denying her something she wants), but I would argue that if the infant attempts to strike back at the individual, acting on certain strategic beliefs about appropriate ways of doing so (e.g. "Pushing didn't work? OK, try punching or kicking"), then her behaviour qualifies as intentional agency and hence bona fide anger of a low-level variety: rage. I propose the following tentative conclusion:

In order to be capable of anger at its lowest cognitive level, an animal must be capable of intentional acts directed against some offending object, individual or bodily irritation, which are accompanied by certain strategic beliefs about an appropriate way to strike at the offending stimulus.

This ability is likely to be found in all vertebrates, as well as many insects and cephalopods.

We could define a higher grade of anger as the desire to strike out at an offending individual. The cognitive requirements of anger are likely to be satisfied by many species of vertebrates and possibly even insects. The desire to strike out at an offending individual requires nothing more than (a) an ability to recognise other individuals and (b) an ability for "book-keeping", or keeping track of other individuals' behaviour during past interactions. The former ability has been documented even in wasps (Tibbetts, 2001) and is widespread across fish families (Bshary, Wickler and Fricke, 2001). The latter ability has been identified in at least two kinds of fish - sticklebacks and guppies are capable of "book-keeping" with several partners simultaneously, and there is tentative evidence that they tend to adopt a "tit-for-tat" strategy in their dealings with one another: a player starts co-operatively and does in all further rounds what his/her partner did in the previous round (Bshary, Wickler and Fricke, 2001). Non-human primates are renowned for their ability to keep track of their own and others' misdeeds over a longer period, as described by van der Waal in his book "Good Natured" (1996).

Cognitive requirements of desire

Frey (1980) offers an ingenious argument against the occurrence of desires in animals. He considers the straightforward case of a dog that desires a bone. "Suppose", he argues, "my dog simply desires the bone: is it aware that it has this simple desire? It is either not so aware or it is" (1980, p. 104). He then argues against both possibilities. If the dog is unaware of its simple desires, then it has unconscious desires. While it might make sense to say that some of a creature's desires are unconscious, it makes no sense to say that all of them are, for then the creature's conduct would be no different from that of a creature with no desires at all.

If one the other hand, the dog is aware of its desires, then we have to answer the epistemological question: how do we know that it is aware of them? Nothing in the dog's behaviour could tell us this.

However, Frey's argument hinges on the questionable assumption that to have a conscious desire, one must be aware of one's desire. An alternative position (Lurz, 2003) is that to have a conscious desire, one must simply be aware of its object.

Additionally, there may be ways of ascertaining whether a dog is aware of its desires. The phenomenon of hedonic behaviour (e.g. preference rankings) suggests that the animal might be aware of its internal affective states.

I conclude that the basic emotions of fear, anger and desire do not presuppose the use of language.


4. Can emotions be explained as bodily states?

One popular scientific theory of the emotions, known as the James-Lange theory because it was developed independently by Williams James and Carl Lange in 1884, holds that emotions are internal feelings that are generated by the body's internal physiological reactions to events. These reactions centre on the body's autonomic and motor functions:

[W]hen we see [a] ... bear, we run away. During this act of escape, the body goes through a physiological upheaval: blood pressure rises, heart rate increases, pupils dilate, palms sweat, muscles contract in certain ways... Fear feels different from anger and love because it has a different physiological signature. The mental aspect of emotion, the feeling, is a slave to its physiology, not vice versa: we do not tremble because we are afraid or cry because we are sad; we are afraid because we tremble and sad because we cry (LeDoux, 1998, pp. 44-45).

LeDoux (1998, pp. 292-295) has recently proposed a more sophisticated version of the James-Lange theory, which he calls a "feedback theory" of the emotions. LeDoux holds that emotions are generated in the brain's amygdala, but acquire their distinctive feeling as a result of bodily feedback.

Theories which construe emotion in terms of bodily feedback do a good job of accounting for the second of the five features of animal emotions identified above - their bodily manifestation - as well as part of the third feature - their distinct kinds. Contrary to criticisms voiced by Cannon in 1929, we now know that the body's somatic feedback system has the requisite speed and specificity to account for the rapidity and diversity of our emotional responses (LeDoux, 1998, pp. 292-295). If we confine ourselves to emotions that do not presuppose language, each kind of emotion can be characterised in terms of its distinctive pattern of bodily response. For instance, fear can be characterised by an increase in heart rate and blood pressure, decreased salivation and increased perspiration, respiratory changes, scanning and vigilance, an increased startle reflex, defecation and either freezing (at low intensity) or flight (at high intensity) (LeDoux, 1998, pp. 144, 172; Panksepp, 1998, pp. 208, 213).

However, I would argue that no theory of emotions which describes them in terms of bodily feedback can explain why emotions are mental states and why they have intentional objects - the first and third of our five essential features of animal emotions.

Even though a "bodily feedback" theory allows us to construe emotions as unconscious mental states which are experienced bodily before being felt consciously by human beings (and possibly some other animals), the problem is that bodily reactions per se give us absolutely no warrant for regarding animal emotions as mental states of any kind, whether conscious or unconscious. It has been argued above that there is nothing about a bodily reaction as such that requires explanation in terms of mental states. A mind-neutral intentional stance can account for the behaviour observed. If we characterised emotions in terms of their bodily reactions, we could ascribe them to any organism capable of responding to an environmental stimulus, but at the cost of robbing them of their mental status.

Additionally, de Sousa (2003) argues that "feeling theories, by assimilating emotions to sensations, fail to take account of the fact that emotions are typically directed at intentional objects". Of course, bodily feelings have a cause, but that does not mean they have an intentional object. In any case, the cause of an emotion and its object may be quite different: if A, while drunk, gets annoyed at B over some trifling matter, drunkenness is the cause of A's annoyance, yet its object may be some innocent remark of B's, which merely occasioned (not caused) the annoyance (de Sousa, 2003).

In particular, bodily feelings, which are states of the body, cannot account for the fact that the intentional objects of emotions are generally states of affairs outside the body:

Suppose I am delighted that my son has become a doctor. I may have various sensations in my body that express this emotion - say, lightness in my limbs and a warm feeling in my viscera. But the object of my delight is not my body; it is my son's success. My bodily sensations are directed to my body and my emotion is directed to my son. Therefore my emotion cannot be identical to my bodily sensations - for the two have different objects (McGinn, 2003).

The James-Lange theory can be faulted on other philosophical grounds. First, the undeniable fact that bodily states can induce emotions does not show that they always or even typically do so. McGinn (2003) argues that "[t]here is causal interplay between feelings and their bodily expression, rather than a one-way dependence".

Second, the language we use to describe emotions does not translate into descriptions of bodily states. McGinn (2003) cites Wittgenstein's observation that the horribleness of my grief when someone I love dies cannot be explained as the horribleness of the sensations I feel in my body. The neurophysiological account of emotions defended above fares better here: on a generic level, grief is about the environmental challenge it arose to cope with - separation from a socially significant other (Panksepp, 1998, p. 50) - and in this particular case, it is about the death of the person I loved.

Panksepp (1998) also criticises theories of emotion that are based on bodily reactions for their implicit cognitivism: emotions are supposed to arise from "our cognitive appraisal of the commotion that occurs in our inner organs during certain vigorous behaviors" (1998, p. 56). Thus Damasio (1994) differentiates emotions according to the entire pattern of somatic and visceral feedback from the body, arguing that feelings are "mental sensors of the organism's interior" (2002).

However, this characterisation overlooks the motivational aspect of emotions. There is an impressive body of evidence (Panksepp, 1998) that animals possess several basic motivational systems, which Panksepp refers to as emotional "operating systems". Each emotional system has its own neural circuitry and evolved to meet a special kind of environmental challenge, which motivates emotional behaviour in animals. These emotional systems in animals are thus defined by their brains, rather than their bodies. I will discuss these systems below.

I conclude that internal bodily feedback cannot account for all of the essential features of animal emotions.


5. Deficient methodologies for distinguishing animal emotions

Before discussing how we should differentiate animal emotions, I would like to explain why certain popular methods of distinguishing human emotions are unsuitable when applied to animals.

Linguistic analysis supports the existence of a short list of basic emotions. Most people, when asked to name the emotions they feel, mention love, anger, fear, sorrow and joy. Other emotions figure in less than 20% of responses (Panksepp, 1998, p. 46). The chief problem with a linguistic approach is that it cannot be applied to non-human animals. Another reason why language may be an unreliable guide to animal emotions is that some of the emotions that have been proposed for animals by scientists (e.g. eagerness, play and nurturance) are not generally described as emotions.

Taxonomies of emotions based on facial analysis, starting with the work of Paul Ekman, have shown that six emotions - surprise, happiness (or joy), anger, fear, disgust and sadness (or distress) - have facial expressions that are universal across all cultures and can be clearly recognised in photos (Le Doux, 1998, p. 113; Evans, 2001, p. 7). However, most people would not consider surprise or disgust to be "proper" emotions. Additionally, Ekman's research focuses on only one species of animal: Homo sapiens. Panksepp (1998) argues that facial expression is a poor indicator of emotion in other animals:

Although in humans and some related primates the face is an exquisitely flexible communicative device, this is not the case for most other mammals, which exhibit clear emotional behaviors but less impressive facial dynamics. Although most animals exhibit open-mouthed, hissing-growling expressions of rage, and some show an openmouthed play/laughter display, they tend to show little else on their faces (1998, pp. 46-47).

Bodily indicators might seem to be a good general criterion for distinguishing animal emotions, as they could be reliably measured by sensors attached to an animal's body. However, as we saw above, this method of differentiating emotions fails to take account of their intentional objects.


6. What kinds of emotions do animals have?

The brain of every species of mammal contains various basic emotional systems. Panksepp (1998, pp. 48-49) defines these emotion systems in terms of the following features:

The first, second and fifth features are particularly relevant to my proposed method for classifying emotions according to their kinds. A suite of sensory stimuli that trigger identical unconditional responses in one of the emotion systems in an animal's brain all instantiate the same kind of environmental challenge that the animal has to deal with - i.e. its generic intentional object. The instinctive motor outputs triggered by the inputs are the animal's first line of defence. The fact that they can be subsequently modulated by cognitive inputs, means that provided the system satisfies the cognitive requirements for intentional agency (specified in chapter two), the system's response can be described as genuinely emotional and not merely reflexive.

Panksepp (1998) summarises the research to date on these systems:

There is good biological evidence for at least seven innate emotional systems ingrained within the mammalian brain (1998, p. 47).

"In the vernacular", writes Panksepp, the seven emotional systems include "fear, anger, sorrow, anticipatory eagerness, play, sexual lust, and maternal nurturance" (1998, p. 47). The first four systems are "evident in all mammals soon after birth" (1998, p. 54, italics mine), because the relevant neural circuits lie below the cortex, at a deeper level where the similarities between mammals are most profound. The neural circuits for our emotional systems are actually very ancient, since they arose in response to persistent external environmental challenges. The three special purpose systems - sexual LUST, maternal CARE and PLAY - are engaged only at certain times in mammals' life-cycles, and are not as clearly understood.

The classification of eagerness, play and nurturance as emotional states will strike many readers as odd. However, it makes good sense to do so if they motivate us to act as other emotions do. Panksepp also acknowledges the existence of many more affective feelings (e.g. pain, hunger), but argues that they do not qualify as basic emotional systems because they do not meet all the above criteria (1998, p. 47).

The seven emotion systems are summarised in the table below. (The capitals are Panksepp's.)


Table - Emotion Systems identified to date in Mammals (based on Panksepp, 1998)
(See also College of Integrated Science and Technology, James Madison University.)

Emotion System #1: FEAR system.

Animal Emotions corresponding to this system: Fear, anxiety, alarm and foreboding

Corresponding Environmental Challenge (generic intentional object): Pain and the threat of destruction

Motivation: Avoiding the threat of bodily harm

Characteristic behaviour: Freezing (mild intensity); flight (high intensity); scanning and vigilance

Associated bodily states: Increases in heart rate, blood pressure, the startle response, elimination and perspiration; respiratory changes

Key sites in the brain: Hierarchical. Amygdala regulates anterior & medial hypothalamus, which regulates periventricular gray substance in lower brain stem, which regulates autonomic indices of fear through spinal cord. Lower components can operate without higher ones.

Key brain chemicals: NMDA glutamate plus various neuropeptides (CRF, alpha-MSH, ACTH, CCK and DBI)

Notes:

  • Contrary to earlier ideas that fear was a learned, conditioned response to cues that predict pain., FEAR is now known to be affectively distinct from pain: electrical stimulation of the brain's pain systems does not produce fear in humans, and electrical activation of the FEAR system in the brain does not appear to evoke the sensation of pain in either humans or animals (Panksepp, 1998, p. 215). Although animals fear painful stimuli, fear and pain are neurologically distinct.
  • FEAR is also distinct from PANIC. PANIC is thought to be linked with an animal's distress when separated from a socially significant other (e.g. its mother).

Emotion System #2: RAGE system

Animal Emotions corresponding to this system: Rage, anger

Corresponding Environmental Challenge (generic intentional object): Events that restrict the animal's freedom (physical restraint or irritation of the animal's body surface) or access to resources (e.g. an invasion of the animal's territory)

Motivation: The need to compete effectively for environmental resources.

Characteristic behaviour: Tendency to strike out at, attack, bite or fight the offending agent (a living creature).

Associated bodily states: Invigoration of musculature; increase in heart rate, muscular blood flow and temperature

Key sites in the brain: Hierarchical system. Medial amygdaloid area regulates ventrolateral and medial hypothalamus, which regulates periaqueductal gray in the mid-brain. Aggressive signals from top levels depend on functioning of lower levels, but not vice versa.

Key brain chemicals: Substance P, glutamate and acetylcholine

Notes:

  • Not all aggressive behaviour can be classified as RAGE. Of the three kinds of aggression circuits identified in the brain - corresponding to predatory aggression, intermale aggression and affective attack - only the last has the distinctive pattern of the RAGE system described above.
  • The SEEKING system mediates wanting as opposed to liking. It is not a pleasure system but an appetitive system.
Emotion System #3: PANIC system

Animal Emotions corresponding to this system: Loneliness, panic, grief

Corresponding Environmental Challenge (generic intentional object): Social loss

Motivation: The urge to be reunited with companions after separation, which helps to create social bonding

Characteristic behaviour: Cries of distress when separated from caregiver

Associated bodily states: Decreases in body temperature, sleep and growth hormone secretion. Increases in brain arousal, behavioural reactivity, sucking tendencies and corticosterone secretion.

Key sites in the brain: Cingulate cortex, septal area, ventral bed nucleus of the stria terminalis, preoptic area, dorsomedial thalamus and periaqueductal gray

Key brain chemicals: Glutamate and CRF

Notes: PANIC is distinct from FEAR. PANIC is thought to be linked with an animal's distress when separated from a socially significant other (e.g. its mother).

Emotion System #4: Exploratory, appetitive SEEKING system

Animal Emotions corresponding to this system: Anticipatory eagerness

Corresponding Environmental Challenge (generic intentional object): Positive environmental incentives such as food, water, sex and warmth.

Motivation: The need for food, water, sex and warmth.

Characteristic behaviour: Stimulus-bound appetitive behaviour: forward locomotion, sniffing, and investigating, mouthing and manipulating objects in the animal's environment. Also self-stimulation - a tendency to engage in events that increase the animal's arousal.

Associated bodily states: Energisation and a feeling of invigoration. Excitation of the lateral hypothalamus. Sustained nural firing in the brain's dopamine system.

Key sites in the brain: Lateral hypothalamus continuum, which runs from the ventrotegmental area at the back of the hypothalamus to the nucleus accumbens. Also the medial septal area, amygdala and frontal cortex.

Key brain chemicals:Dopamine, norepinephrine and epinephrine, serotonin, (site-specific effect), glutamate and acetylcholine.

Notes:

  • Predatory aggression belongs to the mammalian brain's SEEKING system, not the RAGE system.
  • The SEEKING system mediates wanting as opposed to liking. It is not a pleasure system but an appetitive system.
  • The SEEKING system is a single emotion system, despite the diversity of targets (e.g. food, sex). Guided by regulatory imbalances in the animal's body, the SEEKING system triggers non-specific search behaviour that helps the animal obtain what it wants.

Emotion System #5: PLAY (special purpose system)

Animal Emotions corresponding to this system: Play

Corresponding Environmental Challenge (generic intentional object): Opportunity for rough-and-tumble play with conspecifics

Motivation: The need for social interaction

Characteristic behaviour: Rough-and-tumble (RAT) play between juveniles or between parent (usually the mother) and offspring. RAT play includes pinning and dorsal contacts, but varies widely among mammals. Solitary running, jumping, prancing and rolling in herbivores may also represent a form of play. Also laughter (humans) or very high-frequency chirping (rats).

Associated bodily states: Changes in skin sensitivity (skin becomes ticklish).

Key sites in the brain: Involves non-specific reticular nuclei - parafascicular complex and posterior thalamic nuclei. More research needs to be done.

Key brain chemicals: Acetylcholine, glutamate and opioids (all non-specific). No specific chemical is known to regulate play.

Notes:

  • The mammalian brain also contains one or more pleasure systems that correspond to the alleviation of bodily imbalances and a return to an optimal level of functioning. The location and number of the brain's pleasure systems remains unknown.
  • PLAY is quite distinct from aggression as well as SEEKING. It roughly corresponds to "joy". It may not represent a single system.

Emotion System #6: LUST (special purpose system)

Animal Emotions corresponding to this system: Sexual desire

Corresponding Environmental Challenge (generic intentional object): Opportunity to procreate

Motivation: The need to procreate

Characteristic behaviour: Males: courting, territorial marking and mounting.
Females: decrease in aggression towards aroused males. Active tendency to solicit male attention. Receptive posture indicating readiness to be mounted (lordosis reflex).

Associated bodily states: Genital arousal, culminating in ejaculation in males.

Key sites in the brain: Medial preoptic area is predominant in males, vwentromedial hypothalamus in females. Also periaqueductal gray in the midbrain. There are inputs from amygdaloid and higher frontal areas too.

Key brain chemicals: Arginine-vasopressin (AVP) - especially in males. Oxytocin - especially in females. Also Luteinizing hormone releasing hormone (LHRH).

Emotion System #7: Maternal CARE (special purpose system)

Animal Emotions corresponding to this system: Nurturance

Corresponding Environmental Challenge (generic intentional object): Offspring requiring maternal care

Motivation: The need to care for one's offspring

Characteristic behaviour: Responsiveness to distress signals by offspring. Nursing offspring and providing them with warmth and shelter (e.g. a nest). Gathering offspring together.

Associated bodily states: Lactation. Build-up of mood-altering neuropeptides which promote bonding between mother and infant.

Key sites in the brain: "Brain circuits extend far and wide in the subcortical regions of the brain. Part of the circuitry descends from the preoptic area along a dorsal route through the habenula to the brain stem, and part through a hypothalamic route to ventral tegmental (VTA) dopamine systems and beyond" (Panksepp, 1998, p. 253).

Key brain chemicals: Oxytocin (vasotocin in birds), opioids, prolactin and estrogen.

Glossary

The vertebrate brain can be subdivided as follows:

Forebrain, midbrain and hindbrain: The three main divisions of the brain. Also known as the prosencephalon, mesencephalon and rhombencephalon. The forebrain includes the cerebral hemispheres of the telencephalon, as well as two main subcortical zones of the upper brain stem, the thalamus and hypothalamus, jointly known as the diencephalon. The midbrain is relatively undifferentiated. The hindbrain divides into the pontine-cerebellar area, or metencephalon, and the medulla oblongata, or myelencephalon.

Scientists also divide the brain on a functional basis, into the basal ganglia, the limbic system and neocortex, which are said to specialise in motor performance, emotional behaviour and cognition respectively. The boundaries of these regions are not universally agreed upon; different authors list different structures.

The deepest area in the brain is a group of nerve cells known as the basal ganglia (the so-called reptilian brain). It regulates motor performance and controls essential bodily functions such as elimination, seeking shelter, periods of hunting, basking in the sun, aggressive challenges and submissive displays. It also mediates the emotional behaviour asociated with fear and anger. According to Panksepp, this region includes structures such as the caudate nucleus, globus pallidus, nucleus accumbens, entopeducular nucleus, ventrotegmental area and the substantia nigra.

Surrounding this core is an intermediate layer loosely referred to as the limbic system (also misleadingly known as the old-mammalian brain) which increases the sophistication of the basal ganglia's fear and anger responses and elaborates the social emotions. The limbic system interacts with the visceral organs. According to Panksepp, it includes the amygdala, hippocampus, septal area, preoptic area, hypothalamus, and central gray of the mesencephalon as well as other regions. These zones of the brain mediate emotional processes in all mammals and also regulate the emotional behaviour of the "reptile brain".

Finally, the neocortex (popularly known as the neomammalian brain, although it is found in all vertebrates) surrounds the limbic system and is linked with cognition. The size of the neocortex varies a great deal between species. It is found in all vertebrates but is most pronounced in mammals. The cortex of most mammals has six distinct layers (five in dolphins and whales). The cortex in birds lacks these layers.


The mammalian brain also contains one or more pleasure systems that correspond to the alleviation of bodily imbalances and a return to an optimal level of functioning. However, the location and number of the brain's pleasure systems remains unknown (Panksepp, 1998, pp. 181-185). Because the list of basic emotions described above is not exhaustive, the supposition that only these emotions correspond to natural kinds is unwarranted.

It should also be stressed that neurological criteria alone cannot establish the presence of mental states such as emotions. To show this, it has to be demonstrated that each of the emotion systems described above can motivate intentional agency. However, since mammals are certainly capable of intentional agency (as argued in chapter two) we can provisionally assume that they possess the seven-plus kinds of emotions described by Panksepp. Arguments that some of these emotions presuppose "higher" mental states unique to human beings are addressed below.

While Panksepp's approach to the emotions avoids anthropocentrism, it remains very focused on the most studied animals: mammals. I propose to use it as a starting point, bearing in mind the dangers of generalising to other animals.


7. Which Animals Have Emotions?

Some of the brain's emotional architecture appears to be very old. A neurophysiological approach to emotions suggests that some are common to all vertebrates (and possibly other animals), while others may be unique to mammals and birds.

Panksepp (1998, pp. 42-43, 48-51, 70-79) uses a refined version of Maclean's model of the triune brain for illustrative purposes, describing it as an "informative perspective" (1998, p. 43) which "provides a useful overview" (1998, p. 70), while conceding that it is a "didactic simplification from a neuroanatomical point of view" (1998, p. 43). The deepest layer of the forebrain, known as the basal ganglia, is where behavioural responses related to seeking, fear, anger and sexual lust originate. This region is well-defined in all vertebrates. Thus it is likely that all vertebrates share the emotions of fear, anger and sexual desire - whether they be phenomenally conscious or not.

The next, loosely defined layer is commonly called the limbic system - a term attacked as outdated by LeDoux (1998, pp. 98-103) but defended as a useful heuristic concept by Panksepp (1998, pp. 57, 71, 353). (However, both authors agree that certain specific structures in the limbic system serve important functions relating to the emotions.) This region of the brain contains neural programs relating to social emotions such as maternal care, social bonding (companionship), separation distress, and playfulness (Panksepp, 1998, p. 71). The limbic system is of similar relative size across all mammals, but is much smaller in reptiles. The social emotions, such as parental care, social bonding (companionship), separation distress, and playfulness, are likely to be absent in most or all fish and amphibians.

Surrounding the limbic system is the neocortex, which Panksepp describes as the "storehouse of our cognitive skills". This region is most developed in human beings, but is not where feelings originate: "We cannot precipitate emotional feelings by artificially activating the neocortex either electrically or neurochemically" (1998, p. 43), whereas subcortical stimulation of specific areas can induce anger, fear, curiosity, hunger and nausea in mammals (1998, p. 79). There are no basic kinds of emotions that are unique to human beings. The only emotions that are specific to human beings are those whose cognitive requirements are beyond the capacities of other animals.

It is hard to draw conclusions for invertebrates, as their brains have a very different layout. For instance, the amygdala, which is thought to be responsible for the emotional evaluation of stimuli (Moren and Balkenius, 2000), is confined to vertebrates (Panksepp, personal communication, 11 April 2004). However, LeDoux claims that invertebrates "do the same thing with other circuits" (personal communication, 13 April 2004). It should therefore not occasion surprise that recent research (J C Anderson, R J Baddeley, D Osorio, N Shashar, C W Tyler, V S Ramachandran, A C Crook and R T Hanlon. 2003. "Modular organization of adaptive colouration in flounder and cuttlefish revealed by independent component analysis." In Network: Computation in Neural Systems, Vol. 14:321-333) using independent component analysis (ICA) has shown that cuttlefish (cephalopods which are distantly related to octopuses) can signal each other by manipulating the intricate display of coloured patterns on their skin. This display is sensitive to the emotional state of the animals - e.g. it changes when they feel threatened.

Below, I propose criteria for identifying each kind of emotion, which are applicable to all animals.


8. A general strategy for identifying occurrences of basic emotions in animals

Earlier, we suggested that any positive or negative internal state that is capable of motivating animals acting intentionally was an eligible candidate for being a genuine emotion. This suggests that any animal which can be motivated to undergo operant conditioning, spatial learning, tool-manipulation or social learning (subject to the conditions defined in chapter two, part C) in pursuit or avoidance of one of the motivators described in Table 3.1 is experiencing a mental state: the basic emotion corresponding to that motivator.

However, in order to conclusively establish that an animal is indeed undergoing a basic emotion, an emotion system in the animal's brain and/or nervous system has to be identified, which responds specifically to the relevant motivator.

For example, a fruit fly's ability to undergo operant conditioning in order to avoid a noxious or dangerous stimulus (a heat beam), strongly suggests that it is being motivated by fear. However, the discovery of a circuit in the animal's brain or nervous system that responds specifically to danger would be required to confirm this.

Likewise, an animal that learns by its own efforts how to navigate its way around a dangerous location, or how to use a tool in order to repel something dangerous, or how to manipulate the behaviour of other individuals in its group, in order to reduce the risk of danger, can properly be said to be motivated by fear. (Of course, many of our fears are learned. From an epistemological perspective, however, we can only identify unlearned fears as mental states in animals that are capable of learning to avoid bodily harm by their intentional acts.)

Similar considerations apply to the other basic emotions, as shown in the table below.


Table - Behavioural criteria for identifying intentional agency associated with each of the basic animal emotions
Kind of Emotion How manifested in Intentional Agency (general description) How manifested in Operant conditioning How manifested in Spatial Navigation How manifested in Tool Use How manifested in Social learning
FEAR Controlling and fine-tuning one's behaviour in order to avoid danger Ability to fine-tune one's bodily movements in order to avoid danger Ability to modify one's route in order to avoid danger Ability to manipulate objects in order to avoid danger Ability to model one's behaviour on others in order to avoid danger
General experimental strategy for identifying the occurrence of FEAR.

Would the experiment be ethical? No.

- Place an animal in a situation where it has to fine-tune its bodily movements in order to avoid a predator or a noxious stimulus Place an animal in a situation where it has to modify its route in order to avoid a predator or a noxious stimulus Place an animal in a situation where it has to manipulate some object in order to avoid a predator or a noxious stimulus Place an animal in a situation where it has to model its behaviour on another animal in order to avoid a predator or a noxious stimulus
RAGE or anger Controlling and modifying one's behaviour in order to get an opportunity to attack an offending agent/object Ability to fine-tune one's bodily movements in order to get an opportunity to attack an offending agent/object Ability to modify one's route in order to get an opportunity to attack an offending agent/object Ability to manipulate objects in order to get an opportunity to attack an offending agent/object Ability to model one's behaviour on others in order to get an opportunity to attack an offending agent/object
General experimental strategy for identifying the occurrence of RAGE.

Would the experiment be ethical? No.

- Place an animal in a situation where it has to fine-tune its bodily movements in order to get the opportunity to attack an offending agent/object Place an animal in a situation where it has to modify its route in order to get the opportunity to attack an offending agent/object Place an animal in a situation where it has to manipulate some object in order to get the opportunity to attack an offending agent/object Place an animal in a situation where it has to model its behaviour on another animal in order to get the opportunity to attack an offending agent/object
Anticipatory Eagerness (SEEKING) Controlling and modifying one's behaviour in order to attain an attractive object Ability to fine-tune one's bodily movements in order to attain an attractive object Ability to modify one's route in order to attain an attractive object Ability to manipulate objects in order to attain an attractive object Ability to model one's behaviour on others in order to attain an attractive object
General experimental strategy for identifying the occurrence of SEEKING.

Would the experiment be ethical? Yes.

- Place an animal in a situation where it has to fine-tune its bodily movements in order to attain an attractive object Place an animal in a situation where it has to modify its route in order to attain an attractive object Place an animal in a situation where it has to manipulate some object in order to attain an attractive object Place an animal in a situation where it has to model its behaviour on another animal in order to attain an attractive object
PANIC Controlling and modifying one's behaviour in order to obtain comforting social contact Ability to fine-tune one's bodily movements in order to obtain comforting social contact Ability to modify one's route in order to obtain comforting social contact Ability to manipulate objects in order to obtain comforting social contact Ability to model one's behaviour on others in order to obtain comforting social contact
General experimental strategy for identifying the occurrence of PANIC.

Would the experiment be ethical? No.

- Place an animal in a situation where it has to fine-tune its bodily movements in order to obtain comforting social contact Place an animal in a situation where it has to modify its route in order to obtain comforting social contact Place an animal in a situation where it has to manipulate some object in order to obtain comforting social contact Place an animal in a situation where it has to model its behaviour on another animal in order to obtain comforting social contact
LUST Controlling and modifying one's behaviour in order to get an opportunity to satisfy sexual urges Ability to fine-tune one's bodily movements in order to get an opportunity to satisfy sexual urges Ability to modify one's route in order to get an opportunity to satisfy sexual urges Ability to manipulate objects in order to get an opportunity to satisfy sexual urges Ability to model one's behaviour on others in order to get an opportunity to satisfy sexual urges
General experimental strategy for identifying the occurrence of LUST.
Would the experiment be ethical? Yes.
Would the experiment be ethical? Yes. Place an animal in a situation where it has to fine-tune its bodily movements in order to gain access to a receptive sexual partner Place an animal in a situation where it has to modify its route in order to gain access to a receptive sexual partner Place an animal in a situation where it has to manipulate some object in order to gain access to a receptive sexual partner Place an animal in a situation where it has to model its behaviour on another animal in order to gain access to a receptive sexual partner
Maternal CARE Controlling and modifying one's behaviour in order to get an opportunity to nurture offspring Ability to fine-tune one's bodily movements in order to get an opportunity to nurture offspring Ability to modify one's route in order to get an opportunity to nurture offspring Ability to manipulate objects in order to get an opportunity to nurture offspring Ability to model one's behaviour on others in order to get an opportunity to nurture offspring
General experimental strategy for identifying the occurrence of CARE.

Would the experiment be ethical? No.

- Place an animal in a situation where it has to fine-tune its bodily movements in order to get an opportunity to nurture its offspring Place an animal in a situation where it has to modify its route in order to get an opportunity to nurture its offspring Place an animal in a situation where it has to manipulate some object in order to get an opportunity to nurture its offspring Place an animal in a situation where it has to model its behaviour on another animal in order to get an opportunity to nurture its offspring
PLAY Controlling and modifying one's behaviour in order to engage in rough-and-tumble play Ability to fine-tune one's bodily movements in order to get an opportunity to engage in rough-and-tumble play Ability to modify one's route in order to get an opportunity to engage in rough-and-tumble play Ability to manipulate objects in order to get an opportunity to engage in rough-and-tumble play Ability to model one's behaviour on others in order to get an opportunity to engage in rough-and-tumble play
General experimental strategy for identifying the occurrence of PLAY.

Would the experiment be ethical? Yes.

- Place an animal in a situation where it has to fine-tune its bodily movements in order to get an opportunity to engage in rough-and-tumble play Place an animal in a situation where it has to modify its route in order to get an opportunity to engage in rough-and-tumble play Place an animal in a situation where it has to manipulate some object in order to get an opportunity to engage in rough-and-tumble play Place an animal in a situation where it has to model its behaviour on another animal in order to get an opportunity to engage in rough-and-tumble play


It should be stressed that all of the above experimental identifications of basic emotions are tentative, and subject to the identification of a dedicated neurological system in the animal's brain.

Experiments designed to verify the occurrence of emotions and/or feelings in animals run the risk of being unethical. As Allen (2003) remarks in his discussion of nociception (roughly, the sensory detection of injurious stimuli by an animal's nervous system), "[t]here is a need for serious comparative work in this area, but there are, of course, questions about the ethical propriety of doing more of this kind of work, precisely because it might cause morally objectionabale pain" (2003, p. 19).

The reader will have noticed that I have described four of my seven proposed strategies for experimentally identifying basic emotions in animals as unethical, if carried out. It is not often that a researcher counsels against an experiment he/she has proposed, but it is a fact that animals will try to avoid being made to feel afraid, angry, lonely or worried about their offspring. This suggests that to induce these states in animals is to do them emotional harm. According to Panksepp, most animals "readily learn to turn off" electrical stimulation of the brain which artificially induces affective attack, or RAGE, so and concludes that "most animals do have unpleasant affective experiences during such stimulation" (1998, p. 194). However, even if it turns out that the animal is incapable of feeling pain at a conscious level, I believe such conduct to be wrong, for reasons I shall elaborate in chapter five.

It would of course be easy to limit the harm done to experimental animals. For instance, one could design non-invasive experimental techniques to identify anger, such as the following:

Put the animal in a box. Place another animal (actually a lifelike toy) inside its territory and give the animal a chance to attack the toy, but only as long as it moves in a specific way (e.g. run at a certain speed in a specific direction). If it fails to do so, a clear plastic partition comes down and separates the animal from the intruder, which it can still see occupying its territory.

It might be argued that because the above experiment involves no physical cruelty, it is morally justifiable. But in fact, the experimental animal would still be subjected to the physical and emotional stress of having its territory invaded. For this reason, I suggest that research would be better directed at identifying the three emotion systems in animals (seeking, lust and play) where ethical research can be performed.

In play experiments, the animal would have to learn a strategy for obtaining access to its playmates. For instance, the animal could be placed on the other side of a clear plastic partition, giving it a full view of them while they were engaged in play. In order to access its playmates, the animal might have to learn to perform some complicated manoeuvre such as pressing a lever in a particular way (operant conditioning), or successfully navigating a maze (navigational agency), or using some object as a tool to open the partition (tool use), or letting itself be guided to the other side by a video featuring another animal (social learning).

In experiments for identifying sexual desire, the animal would have to perform similar learning feats in order to gain the opportunity to mate with a suitable partner.

Finally, in experiments for identifying seeking (anticipatory eagerness), the animal would have to perform learning tasks in order to maintain a neural state of expectant arousal.