Chapter 3 - Animal Emotions and Subjective States

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4. Emotions and the First Person Intentional Stance: Which Animals are Conscious, and When?

In what follows, I review the major arguments for and against phenomenal consciousness in non-human animals, and briefly discuss the significance of animal consciousness in everyday human life.

The point I wish to make at the outset is that the fundamental divide is not between organisms for which the first-person intentional stance is appropriate and those for which a third-person intentional stance is warranted, but between cases where the third-person singular and the third-person plural stances are warranted - i.e. between organisms, which behave as co-ordinated wholes, and artefacts, which lack intrinsic unity and behave as assemblages.

In my discussion of methodology in chapter two, I proposed that we should adopt a mind-neutral intentional stance except where the adoption of a mentalistic stance enables us to make better scientific predictions than we otherwise would. The implications for our search for conscious emotions are that we do not need to look for events that can only be understood from a first-person standpoint; rather, we need to identify events that are easier to understand and predict scientifically from this standpoint.

The key points I wish to make here, after reviewing the literature on animal emotions, are as follows:

Non-Inferential Arguments

Searle (1998) rejects attempts to infer the existence of conscious states in animals as vestiges of a dualistic mindset, according to which we must infer hidden mental causes from an individual's outward behaviour. Our belief in animal consciousness is a properly basic belief:

[I]t doesn't matter really how I know whether my dog is conscious, or even whether or not I do know that he is conscious. The fact is, he is conscious and epistemology in this area has to start with this fact (Searle, 1998, p. 50).
Allen (2003) criticises this position on the grounds that it fails to settle in practical terms the question of which non-human animals possess consciousness and which ones lack it (the Distribution Question). Where does one draw the line? As a biological naturalist, Searle is confident that science will one day tell us how lower level neural phenomena cause consciousness, and that when we know the "electrochemical" formula for the necessary and sufficient conditions for consciousness, we shall be able to apply it to difficult cases like snails (1998, pp. 45-47). Allen (2003, pp. 7-8) thinks it unlikely that such a formula will yield clearcut answers, and in the meantime, we have to make practical moral decisions as to what kind of legal protection we should accord different kinds of animals. Searle's non-inferential approach is incapable of telling us how to proceed here.

Nevertheless, I would argue that for a small number of companion animals, Searle is right. What I am proposing here is a transcendental argument, which takes as its starting point a fact of everyday life: the fact that we can befriend cats and dogs. To affirm this is to affirm the conditions that make it possible - including the fact that they are phenomenally conscious. (There can be no friendship without the possibility of sharing mutually enjoyed experiences.) But it does not follow from this that most other animals (e.g. hippopotamuses) are conscious.

Conclusion E.20 While the belief that selected animals (e.g. cats and dogs) are conscious is a psychological "given", the same does not apply to most other animals.

Inferential arguments

If we do not, after all, "just know" that most animals possess phenomenal consciousness, then it seems we must infer its presence or absence. Similarity arguments invoke some human or mechanical analogue to explain the behaviour of non-human animals, and use the similarities between the analogue's features and those of non-human animals to justify their conclusions about animal awareness, while dissimilarity arguments do the opposite and argue from disanalogies.

Similarity arguments for animal awareness in non-human animals use human beings as the analogue, and trade on the numerous resemblances between our anatomy, behaviour, neurobiology and pharmacology and theirs. Similarity arguments against animal consciousness point to similarities between animal behaviour and that of machines or human individuals that lack awareness. Dissimilarity arguments are usually cited to prove that other animals do not possess awareness as we do. These arguments may be based on disanalogies between the behaviour of conscious human beings and that of certain animals, who are then said to lack awareness; or on the absence of some mental attribute in non-human animals, which is then alleged to be a pre-requisite for consciousness.

Both kinds of arguments have been brought to bear on the subject of animal minds for at least the past 2,500 years, so it may help if we first examine the limitations of these arguments. Similarity arguments that make use of some human or mechanical analogue certainly work if all of the similarities between animals and the analogue are relevant to the capacity for consciousness, and none of the dissimilarities are relevant. In reality, life is not that simple, and we find both relevant similarities and relevant dissimilarities. In that case, one can attempt to "weigh up" the similarities and dissimilarities, to see which predominates.

A problem arises when the similarities and dissimilarities are incommensurable, as they relate to different sets of features. This is what I found in my search of the literature relating to other animals' capacity to experience pleasure and pain: on the one hand, there are strong behavioural similarities between human beings and other animals (especially mammals, birds and reptiles), suggesting that consciousness may be widely distributed in the animal kingdom; and on the other hand, massive neurological dissimilarities between the brains of mammals and other animals, which seem to preclude these other animals from having conscious experiences of any kind.

A review of the behavioural evidence relating to conscious pleasure and pain

When our chosen indicators for animal consciousness conflict, we have no choice but to reject one set of attributes as an unreliable indicator of animal awareness, and make the other set of features a definitive yardstick for consciousness. In so doing, we have to reject some of our basic intuitions about consciousness.

The question then arises: which set of features do we select as our yardstick? The fact that arguments have raged on this matter for centuries suggests that conflicting intuitions are at work here, so it may help if we ask why. The problem, I suggest, is that there is no generally agreed answer to the question of what consciousness is for. If we knew that consciousness is for X-ing, we could resolve the Distribution Question simply by determining which animals can and cannot X, but there is still no agreed answer as to what X might be.

Since consciousness is said to be a first-person phenomenon, we might try to find X by looking for a kind of behaviour that could only be explained on a first-person account. In practice, however, what we find is that an alternative, third-person account is possible for all of the various kinds of behaviour that are usually cited as evidence of animal awareness. It is difficult, perhaps impossible, to envisage a genre of behaviour that requires subjectivity.

At this point, we can react in one of two ways: (a) decide that we have set the bar too high and plump for some more modest criterion, or (b) decide that non-human animals are not conscious after all. Both choices appear unpalatable: the former is an intellectually soft option, while the latter appears too sceptical.

I suggest that philosophers should swallow their pride and admit that their conceptual tools have failed to resolve the deadlock. A new tack is needed. The most promising course of action, I would argue, is to find out where consciousness is located in the human brain, and why those regions are so special. This might help us understand what consciousness is for. After that, we can decide which animals possess it by ascertaining whether they can perform the requisite feats.

Indicators of Pleasure and Pain

Simple behaviour patterns

Stress responses

All cellular organisms exhibit some form of stress response. For instance, the bacterium Bacillus subtilis exhibits a stress response to heat shock, salt stress, ethanol, starvation for oxygen or nutrients, and so on, which is mediated by the same set of general stress proteins, as well as specific stress proteins (Hecker, Schumann and Volker, 1996). Plants respond to stress by releasing ethylene all over their surfaces, which promotes cell growth and other restorative responses. However, these responses can be described in third-person terminology, and there appears to be no scientific advantage in re-describing all of these stress responses as episodes of conscious pain.

Conclusion E.21 A stress response is not a sufficient criterion for the occurrence of conscious pain.


A variety of animals exhibit a trait called nociception. Nociception includes the sensory detection of potentially injurious stimuli by specific receptors known as nociceptors, the transmission of information within the nervous system, and the resulting response. (The protozoan Paramecia exhibits an avoidance response when poked with a needle, but because it is triggered by changes in electrical activity at the cell surface membrane rather than a nervous system, this response is not considered to be nociceptive.) Among invertebrate animals, only sponges are thought to lack nociception; even Cnidaria such as sea anemones (which lack a brain) respond to aversive mechanical, electrical and chemical stimuli. The roundworm C. elegans exhibits a nociceptive heat response to an acute heat stimulus (Wittenburg and Baumeister, 1999), as do earthworms, leeches, insects, snalils and octopuses (Smith, 1991). Surprisingly, one group of vertebrates, the elasmobranchs (sharks and rays) "lack the neural structures for processing nociceptive information, much less sensing pain" (Rose, 2002, p. 22). It is thought that sensitivity would be a disadvantage for these fish, as they often feed on prey with embedded barbs, such as stingrays.

However, the biological function of nociception can be explained using third-person terminology, without recourse to conscious states such as pain.

Confirming evidence from human studies indicates that nociception is processed at a subconscious level which can be described using to third-person terminology. In human beings, spinal cord neurons send axons to a cluster of neurons in the brainstem, known as the reticular formation. This network processes the nociceptive information, sends it to various subcortical brain structures, and also generates the suite of complex but innate behavioural responses to nociceptive stimuli (Rose, 2002, p. 17). It is important to understand that none of this occurs at the conscious level, as human beings are never aware of the neural activity taking place below the level of the cortex - whether it be in the spinal cord, brainstem or cerebral regions beneath the neocortex (Rose, 2002, p. 6). Brain monitoring techniques have shown researchers that human beings consciously perceive only information that is processed in special regions of the cerebral cortex, known as the associative regions, and that activities processed outside the cortex cannot be accessed by consciousness (Roth, 2003, p. 36).

Conclusion E.22 Nociception per se is not a sufficient criterion for consciousness.

Complex nociceptive responses in human beings lacking consciousness

Studies of brain-damaged human beings show that complex nociceptive responses to stimuli, which are mediated by the spinal cord and brain stem, can occur in the absence of consciousness. People in a persistent vegetative state can make organised responses to nociceptive stimuli and appear to be wakeful. People born without cerebral hemispheres still exhibit nociceptive behavioral responses: when a limb is stimulated, they will withdraw the limb, vocalise, exhibit facial grimaces, and release hormones and neurotransmitters associated with pain. In other words, they exhibit wakefulness without consciousness (Rose, 2002, pp. 14, 17).

Conclusion E.27 Being awake is not a sufficient criterion for consciousness.

Conclusion E.28 A complex nociceptive response to noxious stimuli is not a sufficient condition for the occurrence of conscious pain in animals.

Presence of Opiate Receptors

Many animals, including earthworms, molluscs and insects, manufacture opioid substances such as enkephalins and beta-endorphins - which are known to deaden pain in humans - in their bodies. These creatures also have nerve receptors that respond to opiates. However, the mere presence of opiates in an animal's body is insufficient to establish that it can suffer pain: the substances in question serve other biological functions as well as pain relief, and it is believed that in evolutionary terms, opioids originated in order to attack bacteria and send signals to the immune system (Stefano, Salzet and Fricchione, 1998).

Pharmacological criteria cannot yield decisive evidence of pleasure or pain, because it is possible that the molecules which modify our responses to pleasure and pain originally evolved for another purpose. In fact, this appears to be the case. Stefano, Salzet and Fricchione (1998) note that the association between pain-killing opioids and anti-bacterial compounds goes back at least 500 million years, as both are found in invertebrates as well as vertebrates. In addition, there are chemical affinities between opioids and bacteriocides: pro-enkephalin, a naturally occurring analgesic molecule, contains an anti-bacterial peptide named enkelytin. The authors remark:

In the process of immune defense or neural activation, a bacteriocidal compound, enkelytin, may be released along with the opioid peptides (1998, p. 267).

As it turns out, opioid peptides do more than alleviate pain: they also serve to stimulate immunocytes, which stage an immune reponse in the body.

Stefano, Salzet and Fricchione (1998) argue that bacteria and viruses are and always have been persistent threats to animals, which had to develop means of combating these threats. The authors hypothesise that the association of enkelytin and opioids is part of such a strategy, and that the function of enkelytin is a dual one: to attack bacteria and allow time for other substances (opioid peptides) to stimulate the immune system, while an animal is orienting itself to an invasion by bacteria. Pain may have evolved later, as a means of alerting the animal to the presence of a noxious stimulus such as bacteria. They conclude:

The reason for the evolving relationship between opioid neural and immune processes now appears quite simple, that is analgesic priority-setting activities associated with an anti-infectious / anti-inflammatory process. This combination would provide a high degree of survival benefit to any organism since it would ensure appropriate behavior to meet not only these non-cognitive challenges but also cognitive ones (1998, p. 267).

Additionally, the administration of man-made opioid substances such as morphine or nalaxone produces analgesic effects in these animals and can reduce or abolish their responses to noxious stimuli (Smith, 1991). But here again, we need to ask: is the animal's response a true pain response, or should it be described in more neutral terms? It is easy to envision how opiates might serve a useful role in modulating animal behaviour, even in the absence of consciousness. For example, an animal with an injured leg benefits from nociceptive reflexes that encourage keeping weight off the leg, but the animal is best served by suppressing this reflex with opiate-like neurotransmitters when being chased by a predator.

Conclusion E.23 The presence of opiate receptors in animals' brainstems is an insufficient criterion for the occurrence of conscious pain.


The phenomenon of pain-guarding, in which an animal shows protective behaviour towards an injured part, has been cited as evidence that animals feel pain (Grandin and Deesing, 2002).

I would argue that the complete absence of pain-guarding in certain animals can reasonably be taken as evidence that they lack the capacity for pain. It is hard to see how we can still meaningfully speak of a creature as being in pain if it shows no inclination to protect an injured body part.

Conclusion E.24 Absence of pain-guarding in certain kinds of animals is strong evidence that they are incapable of feeling conscious pain.

Smith (1991) cites a review of the biological evidence concerning pain in insects:

No example is known to us of an insect showing protective behavior towards injured parts, such as by limping after leg injury or declining to feed or mate because of general abdominal injuries. On the contrary, our experience has been that insects will continue with normal activities even after severe injury or removal of body parts.

Conclusion E.25 Insects (and by extension, worms, whose nervous systems are simpler) are incapable of feeling conscious pain.

The phenomenon of pain-guarding is well-documented among mammals and birds, and there is tentative but conflicting evidence of its occurrence in reptiles (Grandin and Deesing, 2002). A recent, well-publicised report by Sneddon, Braithwaite and Gentle (2003), claiming to have identified pain-gaurding in fish, has been subjected to a devastating critique by Rose (2003a) (see Appendix). I have not been able to locate any reliable accounts of pain-guarding in amphibians, fish or cephalopods, although Grandin and Deesing (2002) discuss a few cases of pain-guarding in fish that may alternatively be due to physical illness or fear. It would be unwise, given our present lack of knowledge, to be dogmatic regarding these animals, as "absence of evidence is not evidence of absence".

Pain-guarding would seem to constitute strong prima facie evidence of pain in animals. On the other hand, the biological function of pain-guarding can be explained without recourse to a first-person account, let alone conscious states. For example, an animal with an injured leg benefits from nociceptive reflexes that encourage keeping its weight off the leg.

Conclusion E.26 Pain-guarding per se is not a sufficient condition for the occurrence of conscious pain.


A recent well-publicised report by Sneddon, Braithwaite and Gentle (2003) claims to have identified evidence of pain guarding in fish. Administration of bee venom to the lips of trout affected both their physiology and behaviour. Fish injected with venom exhibited significantly increased respiration, rubbed their lips against gravel and performed a characteristic sideways "rocking" behaviour. In response, Rose (2003a) has written a devastating critique of the report's findings. Briefly, Rose:

(a) acknowledges the occurrence of nociception in bony fish;
(b) argues forcefully that the behaviour exhibited by the trout injected with bee venom is inconsistent with pain guarding, and if anything indicates oral insensitivity on their part;
(c) argues that Sneddon et al. (2003) used a faulty definition of pain of pain in their article - instead of relying on the definition used by the International Association for the Study of Pain ("pain is a conscious experience, with a sensory component and a component of emotional feeling (suffering)"), they considered any form of nociception which is more complex than a reflex to be evidence of pain. Rose argues that this way of distinguishing pain from nociception is invalid because there are clearly complex, non-reflexive behaviors (exhibited by decorticate human beings) that can be purely nociceptive and unconscious.

Pain-guarding revisited

The fact that mammals may exhibit pain guarding of a limb even when it is structurally sound and capable of bearing weight (Grandin and Deesing, 2002) is not readily explicable in biological terms. A first-person account seems more appropriate here: we could say that the behaviour is indicative of pain.

Conclusion E.29 Pain-guarding of a structurally sound limb is prima facie evidence of conscious pain.

Satiety in animals

Mammals also exhibit the phenomenon of satiety: both rats and humans find sweet liquids less appealing just after a meal than when hungry, and make the same appetitive judgements as humans do, depending on how much sugared water they have drunk: their pattern of changing preferences is indistinguishable from that of people (Vines, 1994). However, satiety in rats and humans is likely to be explicable in terms of underlying chemical processes.

Conclusion E.33 The phenomenon of satiety need not indicate conscious pleasure in animals.

(ii) Actions said to be indicative of pleasure and pain

Self-administration of analgesics

Cases where injured animals will actively seek out analgesic drugs would seem to suggest that they are in pain. Grandin and Deesing (2002) describe such a case in rats:

Colpaert et al. (1980, 1982) performed a series of very important experiments which showed that rats with chronic inflammation of the joints will drink water containing an analgesic instead of a sweet solution that control rats preferred. The rats' intake of fentanyl analgesic followed the time course of arthritis that was induced with an inoculation with Mycobacterium butycium (Colpaert et al. 2001). This study clearly shows that rats drank the medication to reduce pain and not for its rewarding effects. Because the rats choose water containing an analgesic which possibly tasted bad compared to the highly palatable sweet solution shows that self-administration of pain relief may be taken as evidence that rats experience pain and suffer in a way similar to humans.

However, a more minimalistic interpretation is also possible: the rats' preference for opiates and willingness to tolerate a bitter taste in exchange for pharmacological relief is the result of some chemical "weighing-up" process in their bodies, rather than a mental evaluation of the pros and cons of imbibing bitter medicine. Before we adopt a first-person stance to explain these phenomena, we should ask whether it makes any useful prediction that a third-person stance would not.

Weighing-up processes are also known to occur in bacteria: if E. coli's sensors detect an attractant (e.g. galactose), and later sense another compound (e.g. glucose) that is more attractive than the first one, a "weighing" of the relative quality of the nutrients occurs, and the chain of reactions resulting in directed motion is amplified. The co-presence of attractants and repellents in solution generates an integration of the "run" and "tumble" responses, at the chemical level (so-called "conflict resolution"). However, as Kilian and Muller (2001, p. 3) point out, the way in which bacteria react to a chemical is utterly inflexible, at the molecular level, and the apparently complex behaviour of bacteria in response to multiple simultaneous stimuli (positive and/or negative) is merely the resultant of two or more inflexible existing action patterns (built-in preferences). The behaviour of the bacteria can be perfectly well described using a third-person intentional stance.

There is no good philosophical reason to adopt a first-person stance to account for injured animals' willingness to self-administer analgesics, unless we find evidence of behavioural flexibility in animals weighing up their options.

Conclusion E.30 An injured animal's preference for a bitter solution containing analgesics over a sweet solution does not constitute conclusive evidence that it is consciously experiencing pain.

Animals can learn to avoid noxious stimuli

Bermudez (2000) has argued that the ability of many animals to undergo conditioning can only be explained by the fact that the unconditioned stimuli (primary reinforcers) with which new behaviour patterns are associated feel pleasant or unpleasant:

[L]earning through conditioning works because primary reinforcers have qualitative aspects. It is impossible to divorce pain's being a negative reinforcer from its feeling the way it does (Bermudez, 2000, p. 194).

But as we saw in chapter two, associative learning does not require a mind, let alone consciousness. We could explain the behaviour of conditioned animals using third-person terminology: reinforcers work because animals have innate drives to seek or avoid them.

For this reason, I cannot agree with Cabanc (2003) when he claims that the ability of animals (including mammals and lizards but not frogs and toads) to learn after a single exposure to avoid foods whose taste they associate with subsequent illness, constitutes evidence that they consciously remember a painful experience. Nor does the inability of frogs and toads to form such associations prove they lack consciousness: other factors, such as physiology or a shorter memory span, may be responsible.

Conclusion E.31 An animal's ability to undergo associative learning is not a sufficient criterion for the occurrence of conscious pleasure or pain.

Tendency of animals to engage in self-stimulation

The tendency of animals to engage in self-stimulation has been cited as evidence that they feel pleasure, as it seems to require an animal to pay attention to its own internal states, rather than external objects. The animal may have to perform a complicated action (press a lever) in order to prolong the arousal of its brain's SEEKING system - hence it needs to "pay attention" to both its arousal state and its current course of action (which it needs to modulate to prolong the arousal state).

Self-stimulation has been identified in a wide variety of animals, including fish, crustaceans, and even snails (Panksepp, peronal communication, 30 May 2004). (In these cases, however, no complex motor behaviour, such as pressing a lever, was required on the animal's part.) We could say that the animals are seeking to prolong their arousal, but non-mentalistic explanations are possible: the animal is now in some automated "do loop", or the instinctual arousal of seeking and the consequent affect keeps the animal magnetised in a repetition compulsion (Panksepp, personal communication, 30 May 2004).

Conclusion E.32 An animal's tendency to engage in self-stimulation is an insufficient criterion for the occurrence of conscious pleasure.

Trade-offs and Relative Rankings of Goods by Animals

More suggestive is the willingness of animals to make trade-offs whereby they expose themselves for a short time to an aversive stimulus in order to procure some attractive stimulus. It has been shown that lizards are willing to leave a warm refuge, where they were supplied with standard food, and venture out into a cold environment, in order to acquire a more palatable food (lettuce). The lizards sought out the lettuce, even though they did not need the food. Additionally, they appeared to weigh up the relative costs and benefits of their choices: when it got too cold, the lizards stayed in their warm enclosure and ate the nearby food, but as experimenters improved the quality of the food in the cold corner, the lizards proved willing to tolerate lower temperatures (Cabanac, 2003). The researchers concluded that the lizards were making decisions based on palatability, a form of pleasure.

Cabanac (2003) reports that "all aspects of palatability reported by humans can be found in rats as well, including decision making in conflicts of motivation, palatability vs. cost".

Researchers such as Marian Dawkins (1994) have also found ways of ranking animals' desires for different "goods", by measuring how much they are willing to work (e.g. peck a key) to obtain each good, or alternatively, how much discomfort they are willing to put themselves through in order to obtain various goods. For instance, hens are averse to squeezing through narrow gaps, and even a hungry hen will not squeeze through a 9 centimetre gap to get food, but will readily do so to obtain access to a floor that is suitable for scratching or dust bathing (Vines, 1994).

From an economist's perspective, the behaviour described above probably meets the requirements for wanting, as the strength of animals' desires for different goods allows economists to construct utility curves. All that would be needed to complete the picture would be evidence to animals' willingness to exchange one combination of goods for an equally desirable combination.

McKee, M. 2004. "Material Girls." In California Wild, the magazine of the California Academy of Sciences, spring 2004 edition. Web address: stories/materialgirls.html.
(Maggie McKee is a science writer from Washington DC.)

Since animals' short-term appetitive behaviour is so similar to our own, it would seem churlish to deny the overwhelming behavioural evidence that these animals experience conscious likes and dislikes. However, it has not been shown that a first-person account yields better scientific predictions than a third-person account that employs more neutral terminology. Cabanc himself employs such terminology: the lizards face "conflict between two motivations: a thermoregulatory drive (to avoid cold) and an attraction to palatable bait" (2003).

Rational and irrational pursuit in animals

Berridge (2001) suggests ways of distinguishing between rational and irrational choice in humans and animals:

Let's grant at the outset that the rationality or irrationality of your choice has nothing to do with why you like it, or with whether anyone else likes it too. The question of rationality hinges only on whether your choice consistently follows your expectations of hedonic likes.

Thus an animal is choosing rationally when it chooses what it expects to like, even if its expectations happen to be wrong. Rational pursuit may be manifested when animals are trained to work for real rewards, which come only sporadically, so the animals learn to persist in working for a reward. Under extinction conditions, when the rewards no longer come at all, the animals will keep working for quite some time because they still expect the reward: they have learned that perseverance pays off.

Irrational pursuit, on the other hand, occurs when an animal desires something it neither likes nor expects to like:

The notion of irrational choice may seem to be self-contradictory when viewed from the perspective that people always choose what has the most value or decision utility to them... However, as documented by a number of authors..., people may sometimes choose an outcome whose eventual hedonic value does not justify their choice...

Irrational pursuit can be identified when an animal, under the influence of some drug (e.g. dopamine), is suddenly presented with the rewarding stimulus, which cues hyperactive pursuit of the stimulus.

Conclusion E.29 Only mammals and birds feel pain.

Affective distortions

By affective distortions I mean extreme behaviours - such as addiction, phobias, intense rage and grief - which make no sense except in the light of animal feelings.

A scientific test for subjectivity

Consider the nineteenth century scenario of two healthy young bachelors who engage in a pistol duel in order to win the hand of a woman they both ardently wish to marry. From a purely biological standpoint, a fight to the death is absurdly irrational: each man faces a high probability of dying without leaving any children behind him if he fights, but is still likely to leave a large number of descendants behind if he refrains from duelling and marries someone else. Only if marrying the woman would double each suitor's expected number of descendants would it be biologically "rational" for him to expose himself to a 50% risk of sudden death. In reality, of course, the suitors do not weigh the risks in this way, because they have feelings. Each man mistakenly believes that he will be heartbroken forever if he does not marry the woman, and each confidently believes (buoyed by a false sense of optimism) that his prospect of victory is much greater than 50%.

The foregoing example suggests one way of identifying kinds of behaviour which manifests feelings in animals:

(1) The kind of behaviour in question should not be "hard-wired". In particular, it should satisfy the requirements for one of the four varieties of intentional agency, described in chapter two (see DF. 1 to DF. 4). Roughly speaking, the behaviour is voluntary in the sense that Aristotle would have allowed for animals.

(2) The behaviour should be undertaken in pursuit of some goal that the animal might find rewarding (e.g. a dainty morsel of food, or a desirable mate).

(3) The behaviour should be risky to the animal's biological prospects (of leaving descendants).

(4) The biological risks should "outweigh" the biological benefits: the animal can expect to be biologically worse off (as measured by its long-term number of descendants) for engaging in the behaviour.

(5) The behaviour should be systematic - i.e. typical of a species and not just an individual. An individual may behave erratically, but if a species which has evolved for millions of years engages in biologically illogical behaviour, then we have to ask why the behaviour has persisted over time.

If the above conditions are satisfied, then the only sensible explanation for the behaviour is that it is feeling-driven. The reason why the behaviour has not been eradicated would then be that feelings confer benefits on their possessors.

Condition (4) is elaborated in an Appendix, where I explain why I have chosen the long-term number of descendants as a measure of biological rationality of an organism's choice, and set forth the mathematical conditions for a biologically irrational choice.


Let us consider a class of risky behaviour B, which is found in some species of organism, and which may adversely affect the organism's reproductive prospects. Suppose also that B satisfies the requirements for some form of intentional agency (see Conclusions DF. 1 to DF. 4). Let r be the probability of an adverse effect on the organism's reproductive success. Let E(not-B) be the organism's expected number of progeny if it abstains from behaviour B, E(fail) be the organism's expected number of progeny if it engages in behaviour B and its reproductive prospects are harmed, and E(success) be the organism's expected number of progeny if it engages in behaviour B and its reproductive prospects are enhanced. Then I propose that B manifests phenomenal consciousness if:

E(not-B) > r.E(fail) + (1 - r).E(success).

We can be more precise if we stipulate the number of descendants after N generations. (Allows for considerations of fitness - not all progeny are equal from an evolutionary viewpoint.)

Which animals are CONSCIOUS?


Silby, B. 1998. E-paper. "On A Distinction Between Access and Phenomenal Consciousness." Web address:

Robert Lurz, "Neither HOT nor COLD: An Alternative Account of Consciousness", Psyche, 2003, Volume 9, No. 1, at

Fox, D. 2004. "Do fruit flies dream of electric bananas?" In New Scientist, vol. 181, issue 2434, 14 February 2004, page 32. Web address:

Carruthers, P. 2000. Phenomenal Consciousness. Cambridge University Press.

Block, N. 1997. "On a Confusion about a Function of Consciousness". In The Nature of Consciousness, edited by Block. N., Flanagan. O., and Guzeldere. G. MIT Press.

Rosenthal, D. 1986. "Two concepts of consciousness." In Philosophical Studies 49: 329-359.

Gallup, G. 1998. "Animal Self-Awareness: A Debate - Can Animals Empathize? - Yes." In Scientific American, 1998.

Different kinds of consciousness

The term "consciousness" has various usages: it can be ascribed to both animals and their mental states. We may impute consciousness to a creature (e.g. a bird), or we might argue about whether its mental states (e.g. its perceptions of a worm) are conscious. Accordingly, philosophers, following Rosenthal (1986), draw a distinction between creature consciousness and state consciousness.

Creature consciousness comes in two varieties: intransitive and transitive. We can say that a bird is conscious simpliciter if it is awake and not asleep or comatose, and we can also say that it is conscious of something - e.g. a wriggling worm that looks good to eat. Furthermore, an animal with transitive creature consciousness might be conscious of an object outside its mind (e.g. a worm) or of an experience inside its mind (e.g. an unpleasant sensation). In the former case, the creature is said to be outwardly conscious of the object; in the latter case, it is said to be inwardly conscious of its experience.

State consciousness, by contrast, can only be intransitive. As Dretske (1995) puts it:

States ... aren't conscious of anything. They are just conscious (or unconscious) full stop.

Ned Block (1997) criticises the concept of state consciousness as a mongrel concept, and has proposed a distinction between two different types of state consciousness: access consciousness and phenomenal consciousness. A mental state is access-conscious if it is poised to be used for the direct (i.e. ready-to-go) rational control of thought and action. Phenomenally conscious states are states with a subjective feel or phenomenology, which, according to Block, we cannot define but we can immediately recognise in ourselves. However, some philosophers have queried the explanatory relevance of this distinction (e.g. Silby, 1998).

Finally, certain scientists distinguish between primary consciousness (also called "core consciousness" or "feeling consciousness") - a moment-to-moment awareness of sensory experiences and some internal states - and higher-order consciousness, also known as "extended consciousness" or "self-awareness" (Rose, 2002).

The debate about animal consciousness is not a debate about creature consciousness: wakeful and dormant states are known to occur in various phyla of animals, and all cellular organisms (including bacteria) are capable of responding to events occurring in their surroundings. Rather, what is at stake is state consciousness, and in particular, phenomenal consciousness, which roughly corresponds to what Rose calls primary consciousness. In the discussion that follows, I shall use the term "conscious" to mean "phenomenally conscious".

The contemporary philosophical debate is split into several camps, with conflicting intuitions regarding the following four inconsistent propositions (Lurz, 2003):

1. Conscious mental states are mental states of which one is conscious.
2. To be conscious of one's mental states is to be conscious that one has them.
3. Animals have conscious mental states.
4. Animals are not conscious that they have mental states.

Proponents of so-called higher order representational (HOR) theories of consciousness accept propositions 1 and 2. HOR theorists argue that a mental state (such as a perception) only becomes conscious by virtue of its being an object of creature consciousness. Perceptions, on this account, are not intrinsically conscious; they require higher-order states to make them so. These higher-order states are variously conceived as thoughts (by HOT theorists) or as inner perceptions (by HOP theorists) (Wright, 2003).

Exclusive HOR theorists like Carruthers also accept 4 but reject 3 - that is, they allow that human infants and non-human animals have beliefs, desires and perceptions, but insist (Carruthers, 2000, p. 199) that we can explain their behaviour perfectly well without attributing conscious beliefs, desires and perceptions to them.

Inclusive HOR theorists, such as Rosenthal, accept 3 but reject 4. Rosenthal (1986) argues that animals can have very crude thoughts about their mental states - e.g. the thought that one is having a particular sensation.

Defenders of first-order representational (FOR)accounts of consciousness, such as Dretske, accept 2, 3 and 4 but reject 1. Thus Dretske argues that a mental state becomes conscious simply by being an act of creature consciousness. An animal need not be aware of its states for them to be conscious. On this account, consciousness has a very practical function: to alert an animal to salient objects in its environment - e.g. potential mates, predators or prey. On the other hand, such an account is vulnerable to Chalmers' (1996) zombie argument, as one could conceive of an unconscious zombie with the same discriminatory abilities as a conscious animal.

Lurz (2003) rejects Dretske's position, on the grounds that it seems counter-intuitive to say that an animal could have a conscious experience of which it was not conscious. According to Lurz's (2003) same-order (SO) account, it is the assumption (shared by HOR and FOR theorists) that to be conscious of one's mental states is to be conscious that one has them, that needs to be queried. Lurz suggests that a creature's experiences are conscious if it is conscious of what (not that) its experiences represent.

I believe that if we are to resolve the current argumentative deadlock about animal consciousness, we might do well to set aside both our philosophical thought experiments (such as Chalmers' zombie) and our grammatical intuitions about the proper usage of the word "conscious", and focus instead on the empirical cases that underlie the arguments. In particular, recent research on attention mechanisms (discussed in Wright, 2003) sheds valuable light on animal consciousness.

Wright (2003) considers the much-discussed case of the distracted driver, who is supposedly able to navigate his car for miles despite being oblivious to his visual states. FOR theorists happily grant that the distracted driver has conscious visual states of which he is not aware; HOR theorists deny this. Wright faults both camps for being too gullible, citing three driving studies which show that driving requires a certain minimum amount of attention to the road. What really happens in "distracted driving" is that the driver pays attention to the road for some of the time, but the other matter that he is thinking about demands a much greater share of his cognitive resources, with the result that the information about the visual scene is quickly bumped from working memory and never encoded in long-term memory. Hence the driver's shock when he comes to the end of his journey.

Additionally, studies of inattentional blindness (IB) and change blindness (CB) refute the claim made by FOR theorists that subjects can have visual experiences that they are not attending to. Wright (2003) cites research on IB, showing that when subjects are engaged in visual tasks demanding a high degree of attention, they fail to notice unexpected objects in their field of vision, even when they occupy the same point on their visual scene as the objects they are attending to. During CB, subjects fail to notice large-scale changes in a scene directly before their eyes, because their attention is diverted to other features of the scene. The upshot is that "there seems to be no conscious perception without attention" (Wright, 2003). Dretske's (1995) assertion that "You may not pay much attention to what you see, smell, or hear, but if you see, smell or hear it, you are conscious of it" is therefore empirically wrong.

The relevance of the above research to animals should be obvious:

Conclusion E.20 Attending to an object is an necessary condition for being conscious of it.

Conclusion E.21 Only those animals that are capable of attending to objects in their surroundings can be described as having phenomenally conscious states.
Wright does not define exactly what he means by "attention". Scientific models of attention often include aspects of selectivity, selecting one item in favor of another. Either the selected one is enhanced, or the other one is suppressed. Other models discuss the assignment of resources to items. Due to the resulting reduction of data to be processed, models of computer vision sometimes use mechanisms of visual attention. Another aspect of attention is that it allows to select relevant items and suppress distractors for task specification.

Which criteria should we use to identify phenomenal consciousness in animals?

Use Carruthers' article to distinguish different kinds of consciousness.

Suggest the following theses:

Talk about: representationalism (presupposed here).

(1) What we call phenomenal consciousness consists simply in paying attention to our experiences (esp. our internal bodily representations). Paying attention to external objects is creature consciousness, but need not be phenomenal. Third person account will do. (Aside: paying attention to internal states is not the same as looking inside your body. Seeing your body from the inside is not the same as seeing inside your body from outside.) Paying attention to internal states requires a first-person account.

(2) Intentional activity, manifest as controlled behaviour, indicates paying attention.

(3) Any creature capable of controlling its behaviour in order to stabilise or prolong its internal states (in the absence of any external object that mirrors or tracks those states) is conscious.

Alternate argument: (2) Are there purely neural criteria for attention? See report on fruit flies in New Scientist 14/2/2004.

Is Drosophila at the flight simulator conscious? Recall the case where it was flying blind without any cues. Was it exercising control here? Maybe not (see earlier remarks about whether intentional agency was required in this case). However if it had to perform complicated manoeuvres we might say yes. Certainly recent research shows that flies are capable of paying attention to external objects (see report in - New Scientist 14/2/2004).

Rats engaged in self-stimulation. See Panksepp 1998.

See Wright, W. 2003. "Attention and Phenomenal Consciousness." Washington University PNP Medical School Seminar Program (December 2003). Web address: Criticises Tye's theory in favour of HOR theory, but one which does not require thought-like or perception-like higher-order states, just higher-order attention states.

Criticism of Wright. What exactly is attention? Wright spoils his definition by including consciousness in the definition, of a term which was supposed to elucidate the nature of consciousness. "The attentional resources I have in mind - and which seem to be at work in the earlier cited studies of the cognitive demands of driving - operate at a conscious level and have to do with access to and control over information by the perceiving subject." Later he complicates his case by suggesting that there are also "subconscious attentional mechanisms".

However, his notion of control over information by the subject seems a promising one.

Elsewhere he writes: "Attention marks certain elements of the scene as salient and the rest are lost to consciousness. Those elements of the before view that have been indexed are loaded into visual short-term memory (VSTM), persist through the distractor event, and are available for comparison to the after view." This is more detailed, but what about the other senses?

Also refer to New Scientist report (14/2/2004) about attention in fruit flies.

See Allen, C. 2003. Animal Pain. In Nous 2 April 2003.

DON'T argue here: behaviour X can occur without any subjective feelings, so it can't indicate the presence of an emotion or pain. This ASSUMES that emotions and pain are always SUBJECTIVE, which has yet to be proven. Most of what goes on when we feel is SUB-CONSCIOUS (LeDoux, 1998). Maybe in some cases, ALL of what goes on is sub-conscious. (Sub-conscious fears? dislikes? desires? Maybe even pains?)

Pain - aversive behaviour not a sufficient criterion; learned avoidance behaviour not a sufficient criterion; analogous neurophysiology not a sufficient criterion; presence of nociceptors not a sufficient criterion; insensitivity arising from a distributed nervous system not sufficient to rule out pain; pain guarding a sufficient criterion?
Useful quotes:

"Noiception is the physiological response to painful stimuli and it does not involve the highest parts of the brain and pain proper" (Grandin and Deesing, 2003).

"In humans, the prefrontal cortex must be intact in order to experience the emotional sensation associated with pain (Freeman and Watts, 1950). However, neurobiologists long believed that the PFC is a recent evolutionary acquisition and is unusually large in the human brain. Recent advances in the study of prefrontal cortex find no justification for these beliefs. Jerison (1997) conducted a formal analysis of similarities and differences between species and provides evidence that the PFC is an ancient part of the mammalian brain, is put together in all mammals pretty much the same way, and its functions are basically similar. The percentages of frontal cortex in relation to the rest of the brain are 29% in humans, 17% in chimps, 7% in the dog, and 3% in the cat (Broadman, 1912, Fuster, 1980). Although cats have less PFC compared to dogs, we would argue against any suggestion that cats suffer less from pain than dogs, or that rats suffer less than cats. It is likely that the cat has sufficient frontal cortex circuitry to have the minimum required amount to fully suffer" (Grandin and Deesing, 2003).

"On the question of size, the PFC in humans is very large, but not disproportionately large. In other words, as a brain becomes larger and more complex it requires more circuits which can associate and merge inputs from many different parts of the brain. A small brain requires a less complex 'control room' than a bigger brain" (Grandin and Deesing, 2003).

There has been some controversy in the scientific literature on the evolution of the prefrontal cortex. Some of the controversy may be caused by differences in how the prefrontal cortex is defined. Wood and Grafman (2003) contains an excellent map of prefrontal cortex and its connections to other parts of the brain. The ventromedial prefrontal cortex is old from an evolutionary standpoint. It has direct connections to the amygdala (emotion center). The dorsal lateral frontal cortex developed later and it integrates inputs from many parts of the brain and it makes it possible for an animal to engage in more abstract behaviors. It receives emotional information via the more primitive ventromedial prefrontal cortex (Wood and Grafman 2003). Some scientists consider the dorsal lateral prefontal cortex to be the 'true' prefontal cortex" (Grandin and Deesing, 2003).

"Although some fundamental uncertainty exists when it comes to assessing subjective experiences such as pain and suffering in mammals, certain criteria can provide insight. For example, when an animal shows protective behavior towards an injured part, such as limping after an injury to a leg, going off feed because of abdominal injury, or actively seeking relief from pain by ingesting both opiate and non-opiate analgesics, such responses can indicate that something more complex than a simple reflex is taking place. All mammals pain guard after an injury... Poultry also engage in pain guarding after beak trimming and will peck less (Duncan, et al 1989, Gentle, et al 1991). Pain guarding occurs even when a limb is structurally sound and capable of bearing weight... Research on de-beaked chickens shows they pain guard after the procedure and will reduce food intake. De-beaked chickens are reluctant to use their beaks. Sometimes a neuroma forms on the end of the beak after it heals. Neuromas can cause pain in man (Gentle, et al 1990). Chickens with neuromas reduce the number of pecks at feeding (Gentle, et al 1990; Duncan et al 1989).... Grandin (1997) and Bateson (1991) stress the importance of separating fear stress from physical stress such exertion from running or overheating. Fear has a powerful ability to override pain in the chicken. The work by Gentle and Corr (1995) shows that a chicken that was pain guarding by holding its leg up will stop pain guarding when it is placed in a scary novel place... However, it is likely that birds may experience pain differently. Recent work by Gentle (1997) show that decerebrate chickens will still pain guard legs injected with a substance that causes pain. The results suggest that in chickens, pain from chronic arthritis is organized in the brainstem. However, if the chicken's beak is trimmed and the frontal area of the brain is removed, pain guarding and other pain related behaviors are absent. But, if the beak is trimmed six days after the frontal area of the brain is removed, the chicken continues to pain guard (Gentle, et al 1997). It appears that chickens are unable to process two emotions simultaneously. Chickens may suffer from chronic pain when they are undisturbed, but when disturbed or frightened, the pain ceases and the chicken can only attend to the fear (Gentle and Corr, 1995). Prelaying behavior and feeding motivation can completely suppress pain coping behaviors in arthritic chickens (Gentle and Corr, 1995; Wylie and Gentle, 1998). Turkeys with degenerative hip disorders reduce spontaneous activity and sexual activity (Duncan et al 1991). The authors conclude that the different systems in a bird's brain may be less integrated than in higher mammals. A bird may be more mono channel and operate only one system at a time. The bird would probably be suffering if the pain or fear channel is operating" (Grandin & Deesing, 2003).

Do reptiles or amphibians suffer from pain? Research shows that the nervous system of amphibians responds to analgesic drugs. Amphibians will respond to a painful stimulus applied to the skin. Many different types of analgesic drugs will reduce the response (Stevens et al., 1994; Stevens et al., 2001). Is this true suffering from pain or is it just a reflex like touching a hot stove? Do reptiles and amphibians pain guard or seek analgesics? Both these areas need to be researched. The antedotes below may provide some insights for guiding future research. Discussions with reptile specialists indicate that reptiles may or may not pain guard. Friend (1998 personal communication) indicates that iguanas will walk on a severely damaged leg and make no attempt to reduce weight on the damaged limb. Iguanas are physically capable of lifting a leg to favor it, but they do not. Lizards react to noxious stimuli which may cause acute pain, but may have little reaction to injuries that would cause long term pain... A tortoise with a sore mouth will not eat and if it has a sore toe it will not walk. This is likely to be true pain guarding. Snakes with a damaged mouth may refuse to eat or lie on their backs to avoid pain. A tortoise with an abscess in its head will refuse to eat. Eating resumes shortly after the abscess is drained" (Grandin & Deesing, 2003).

"Research by Lynne Sneddon at the Roslin Institute indicates that fish engage in true pain related behavior. Fish that had acetic acid injected into their lips engaged in more pain related behaviors such as rubbing their lips on the gravel and rocking compared to saline injected controls. There were no differences in swimming activity. Administering morphine reduced the pain related behaviors... Fish injected with acetic acid took significantly longer to start feeding compared to saline injected controls. These studies indicate that to insure a reasonable level of welfare providing pain relief should be considered for fish. This excellent research study separated the variables of pain from fear by having a saline injected control" (Grandin & Deesing, 2003).

Steve Kaufman's review (Vegan Outreach, of Rose's article, "The neurobehavioral nature of fishes and the question of awareness and pain", in Fisheries Science, Vol. 10, 2002, pp. 1-38:

Many of us would claim that fishes' behavior clearly demonstrates that they can suffer. Yet, James D. Rose argues that scientific evidence strongly favors the conclusion that fishes do not feel pain. If valid, this has implications for animal advocacy.

Rose's argument rests heavily on the observation that human consciousness depends on the neocortex, which is absent in fishes. While humans, fishes, and other vertebrates share more primitive spinal cord and brainstem structures, neuroanatomic studies show that the fishes' cortex is far less developed than that of humans and does not include a neocortex. Decorticate humans, who have no input from the brainstem to the cortex due to trauma, stroke, or other damage, can still exhibit behavioral responses to stimulating nociceptors (nerve receptors that are stimulated by injury). Such humans will withdraw a stimulated limb, vocalize, exhibit a facial grimace, and release hormones and neurotransmitters associated with pain, even though there is no evidence that they are conscious. Even people under general anesthesia receive analgesics to block the hormonal responses that unconsciously accompany nociception.

The spinal cord and brainstem, which are much older structures than the cortex in terms of evolution, mediate the primitive withdrawal responses to nociception in all vertebrates. Spinal cord and brainstem activity occurs unconsciously in humans and, presumably, other animals. When you step on a tack, high velocity neurons to and from the spinal cord mediate rapid withdrawal of the foot, and slower impulses go the brain where, about a second later, you experience a decidedly unpleasant sensation.

Humans and fishes have evolved independently for 400 million years. In humans, consciousness, including conscious perception of pain, requires multiple inputs from frontal and parietal neocortex structures that fishes lack. Further, frontal cortical structures that are absent in fish mediate the unpleasant aspect of pain perception in humans. People lacking input from the frontal cortex (due to disease, trauma, surgery, etc.) relate that they can feel painful stimuli, but it doesn't bother them.

Fishes do have a cortex, which is anatomically far less complicated and much smaller in proportion to the brainstem than that of humans. The cortex in fishes is involved in sensory reception (particularly smell) and modulates responses to nociception, but fishes' cortex is not essential for their normal responses to noxious stimuli.

Rose addresses several possible objections to his thesis:

Fishes react to injurious or threatening stimuli. The ability to response to such stimuli is also seen in unicellular organisms and multicellular organisms without brains, and we do not attribute consciousness to them. And, humans have unconscious brainstem- and spinal cord-mediated responses to such stimuli.

Fishes have nerve receptors that respond to opiates, which deaden pain in humans. Like humans, fishes have opiate receptors in their brainstems. Their presence in human brainstems demonstrates that opiate receptors have functions besides modulating conscious awareness of pain. It is easy to envision their use in modulating behavior without requiring consciousness. For example, an animal with an injured leg benefits from nociceptive reflexes that encourage keeping weight off the leg, but the animal is best served by suppressing this reflex (with opiate-like neurotransmitters) when being chased by a predator.

Noxious stimuli alter fish behavior. While learning would appear to be compelling evidence for consciousness, it appears that humans gain considerable learning without conscious awareness. Perhaps humans require consciousness in order to learn about and make subtle discriminative choices in much more complex situations than fishes experience. Just as a computer can be programmed to unconsciously learn from experience, fishes may exhibit analogous abilities. Fishes can exhibit simple associative learning, and humans seem to have this capacity at an unconscious level as well. Furthermore, fish behavior is largely preserved after their cortex has been removed, with the principle deficit being loss of responses to smell, because their sense of smell is mediated by their cortex.

While inconclusive, it appears that fishes have analogous structures to the human limbic system, which is involved in emotions and in life-sustaining behaviors in mammals, including reproduction, aggression, defense, feeding, and drinking. In humans, consciousness of emotions requires the neocortex that, again, is absent in fishes. Furthermore, a component of the limbic system known as the cingulate gyrus appears to be essential for the human emotional response to pain. This structure has been identified only in mammals, and researchers have done extensive neuroanatomic research on fish.

Rose argues that, if fishes were conscious, their experiences would differ so fundamentally from those of humans that any attempts at empathetic understanding would be futile. Neuroanatomy research, including studies on injured humans and invasive experiments on animals, has shown that specific functions require specific neuroanatomic structures. Lacking the human structures involved in consciousness and emotional perception, Rose asserts that it is unreasonable to believe that fishes experience noxious stimuli in analogous ways to humans. Similarly, we can't prove that plants are insensate, but we strongly doubt that they experience damaging events as we do, because they lack the anatomic components we regard as essential to conscious experience.

I think that the burden of proof is on those who would harm fishes, particularly if the damage to fishes' well-being were unnecessary. It seems most reasonable to avoid harming fishes because there is no way to know for certain whether or not they can have some kind of unpleasant sensation. Just as we can't empathize with a bat's echolocation, we may be unable to empathize with what a fish feels when hooked, but the possibility that fish find the experience subjectively unpleasant is good reason to refrain.

-Steve Kaufman

Different senses of "conscious" (Allen, 2002) - awake (not asleep); able to respond to stimuli; phenomenally conscious in a "subjective" sense; self-conscious (not relevant in this chapter).
Distinguish different senses of "conscious":

"Although consciousness has multiple dimensions and diverse definitions, use ofthe term here refers to two principal manifestations of consciousness that exist inhumans (Damasio, 1999; Edelman and Tononi, 2000; Macphail, 1998): (1) "primary consciousness" (also known as "core consciousness" or "feeling consciousness") and (2) "higher-order consciousness" (also called "extended consciousness" or "self-awareness"). Primary consciousness refers to the moment-to-moment awareness ofsensory experiences and some internal states, such as emotions. Higher-order con-sciousness includes awareness of one's self as an entity that exists separately fromother entities; it has an autobiographical dimension, including a memory of past life events; an awareness of facts, such as one's language vocabulary; and a capacity for planning and anticipation of the future. Most discussions about the possible existence of conscious awareness in non-human mammals have been concerned with primary consciousness, although strongly divided opinions and debate exist regarding thepresence of self-awareness in great apes (Macphail, 1998). The evidence that the neocortex is critical for conscious awareness applies to both types of consciousness. Evidence showing that neocortex is the foundation for consciousness also has led to an equally important conclusion: that we are unaware of the perpetual neural activity that is confined to subcortical regions of the central nervous system, including cerebral regions beneath the neocortex as well as the brainstem and spinal cord (Dolan, 2000; Guzeldere et al., 2000; Jouvet, 1969; Kihlstrom et al., 1999; Treede et al., 1999). Although consciousness has been notoriously difficult to define, it is quite possible to identify its presence or absence by objective indicators. This is particularly true for the indicators of consciousness assessed in clinical neurology, a point of special importance because clinical neurology has been a major source of information concerning the neural bases of consciousness. From the clinical perspective, primary consciousness is defined by: (1) sustained awareness of the environment in a way that is appropriate and meaningful, (2) ability to immediately follow commands to perform novel actions, and (3) exhibiting verbal or nonverbal communication indicating awareness of the ongoing interaction (Collins, 1997; Young et al., 1998). Thus, reflexive or other stereotyped responses to sensory stimuli are excluded by this definition. Primary consciousness appears to depend greatly on the functional integrity of several cortical regions of the cerebral hemispheres especially the 'association areas' of the frontal, temporal, and parietal lobes (Laureys et al., 1999, 2000a-c)... Wakefulness is not evidence of consciousness because it can exist in situationswhere consciousness is absent (Laureys et al., 2000a-c)" (Rose, 2002, p. 6).

The reasons why neocortex is critical for consciousness have not been resolved fully, but the matter is under active investigation. It is becoming clear that the existence of consciousness requires widely distributed brain activity that is simulta-neously diverse, temporally coordinated, and of high informational complexity (Edelman and Tononi, 1999; Iacoboni, 2000; Koch and Crick, 1999; 2000; Libet,1999). Human neocortex satisfies these functional criteria because of its unique structural features: (1) exceptionally high interconnectivity within the neocortex and between the cortex and thalamus and (2) enough mass and local functional diversification to permit regionally specialized, differentiated activity patterns (Edelman and Tononi, 1999). These structural and functional features are not present in subcortical regions of the brain, which is probably the main reason that activity confined to subcortical brain systems can't support consciousness (Rose, 2002, p. 7).

Our fundamental behavioral reactions to noxious stimuli, including vocalization, facial grimacing, and withdrawal, are mediated by subcortical brain and spinalsystems (Jouvet, 1969; Kandel et al., 2000; Laureys et al., 1999, 2000a,b; Young et al.,1998). Activation of these responses by noxious stimuli can occur without consciousness in people with extensive cortical damage (Figure 3) and in humans born without cerebral hemispheres (Kolb and Whishaw, 1996; Steiner, 1987). Thus, the behavioral displays related to noxious stimuli or emotion in humans, as in other animals, are stereotyped, automatic behavioral programs controlled by lower levels of the central nervous system, and these responses can be evoked without any corresponding awareness of noxious stimuli. Limb withdrawal and leg locomotor responses, of course, are produced directly at the spinal cord level (Rose, 2002, p. 17).

Comments on Rose's definition: none of the criteria Rose lists for primary consciousness are necessarily confined to mammals. Other vertebrates, and even some invertebrates (e.g. bees and octopuses), are surely "aware of their environment". Many animals can follow commands to perform novel actions (birds? fish?). Nonverbal communication exhibiting awareness of the ongoing interaction is surely not excluded for non-mammals. Where is the evidence that these abilities require a neocortex?

The indispensability of subjectivity (or: Which intentional stance is appropriate for discussing emotions and pain?)

Is our knowledge of animals' mental states an inference to the best explanation? No, argues Allen (2003).

Look at arguments AGAINST animal subjectivity (see Allen's article):
(1) Dissimilarity argument: Animals lack key brain structures (especially a neocortex - see Rose's article on fish). Animals lack language (Descartes, Frey?).
(2) Similarity argument: Animals behave like human beings on autopilot, or blindsight subjects.
(3) Phenomenal consciousness requires ability to think about one's thoughts & distinguish appearance from reality (see Allen 2002, 2003).
(4) Experimental arguments. It is experimentally possible to make human and animal subjects want things they are not conscious of (subliminal processing), and even to want things that they do not expect to make them feel better (irrational pursuit - addiction) (Berridge, 2003a, 2003b). Conclusion: wanting need not be conscious.

Look at arguments FOR animal phenomenal consciousness (see Allen's 2002 and 2003 articles)

(1) Similarity arguments - neurophysiological & behavioural
(2) Evolutionary arguments. Pain and other feelings evolved because of their survival value.
(3) Inference to the best exlanation
(4) Non-inferential awareness (Searle). I "just know" my dog is conscious. It doesn't matter how I know. Problem: which animals are conscious? Where do you draw the line?
(5) Argument from illusion - animals are susceptible to the same perceptual illusions as we are. Extension: some of them can be trained to make corrections for their illusions.
(6) Argument from efficacy of conditioning (Bermudez, 2000). It is impossible to divorce something's being a positive (negative) reinforcer from its feeling good (bad).
(7) "Affective distortions" - extreme behaviours such as phobias, intense rage, grief, addiction - which make no sense except in the light of animal feelings.

(8) Attention in fruit flies - Report in New Scientist, 14/2/2004. Web site: Fruit flies have conscious experiences

Scientists in California have discovered that fruit flies seem to respond to stimuli in a similar way to a mammal or human ?Eexhibiting traits of attention and interest.

Insects in general have been assumed to be little more than hard-wired automatons, even though there is considerable proof that many insects do exhibit conscious traits (see the example of the honey bee dance as an excellent example of this). The fruit fly in particular has a brain which consists of only 250,000 neurons. Compare this to the honeybee?s 1 million neurons and the human brain which consists of 100 billion neurons.

However, recent behavioural studies have shown insects doing things that hint at more complex brain functions. Studies have shown that fruit flies sleep every night and also possess short, medium and long term memory.

These new studies are interesting since they demonstrate the fruit fly also has an attention span. The flies have been shown to exhibit greater brain activity when following external stimuli such as light beams. While this might not sound too impressive, there is more to it. The brainwaves that were found looked uncannily like the ones you see in a human brain when it is paying attention.

The EEG from the flies were recorded from three different regions of the brain. Normally, the electrical chatterings of these regions vary wildly. But show the fly a stripe and they suddenly fall into sync at 20 to 30 hertz, rising and falling in unison like a crowd doing a Mexican wave. This is called synchrony and it is exactly what you see in a mouse or human brain when it pays attention to something. Synchrony is attention defined: all eyes focused on one stimulus, one stripe, one wave - and everything else is ignored.

The first time a fly sees a stripe, the brain signal increases, but with each new pass the increase shrinks slightly as the fly gradually loses interest - until a new stripe appears. What's more, the signal increases when you enhance the importance of that stripe for the fly - by simultaneously puffing the fly with banana odour, which it likes, or heating it with a lamp, which it doesn't. And if you show the fly the stripe alone, having previously shown it at the same time as heating the fly, the signal is still elevated: the fly associates that stripe with something bad, so watches it even more intently. It all suggests that the 20 to 30 hertz signal encompasses not just vision, but other senses too - that it reflects some overall assessment of whether something is worth keeping an eye on or can be safely ignored. What is most interesting is that when the fly watches the stripe, it ignores everything else.

These are exciting discoveries. To neuroscientists, attention is an important phenomenon. Exactly how the brain filters out external stimuli to allow it to focus on specific things is one of neuroscience's biggest questions. The reason for this? Attention is intimately associated with consciousness. What you pay attention to defines how you experience the world from moment to moment.

Many neuroscientists believe that if they can discover how the brain decides what to pay attention to, they will have taken the first step towards teasing out the neuronal basis of consciousness. And that's why finding human-like attention in a fly is so promising. Flies are much easier to work with than people - could studying their brains open a new window on the human mind?

The scientists are planning to extend their trials by showing the fly two visual cues and seeing which it pays more attention to. Then showing it two variations of the one it has chosen. Repeat this many times and you might discover to what degree those decision criteria are hard-wired in all flies, as opposed to being shaped by each fly's experiences.

These discoveries also provoke more debate in the perennial question ?which animals are conscious??E If an insect with a brain size which is four hundred thousand times smaller than ours can demonstrate conscious activity, can we not suggest that everything in between does as well?

Source: New Scientist 14/2/2004

Which animals have feelings?

Are humans and animals emotionally symbiotic? (Mary Midgley)

The relevance of emotions to animals' interests (Having an interest vs. taking an interest. Addiction. Binged-out beetles.)


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Grandin, T. & Deesing M. 2003. "Distress in Animals: Is it Fear, Pain or Physical Stress?" Paper given at American Board of Veterinary Practitioners - Symposium 2002, May 17, 2002, Manhattan Beach, California. Special Session: Pain, Stress, Distress and Fear. Updated in September 2003. Web address:

Hartwell, S. 1994/95, 2003. "Why Feral Eradication Won't Work." Web address: Sarah Hartwell works for the UK's Cats Protection (CP) and writes articles related to the welfare, care and behaviour of cats.

Hartwell, S. 1999, 2003. "The Great Australian Cat Predicament." Web address:

Hartwell, S. "Do Cats Have Emotions?" Web address:

Midgley, M. 1993. '"The Four-Leggeds, the Two-Leggeds, and the Wingeds": An Overview of Society and Animals.' In PSYETA, Vol. 1, No. 1. Web address:

Ball, J. 1998. "The Question of Non-Human Intelligence." Web address:

Moren J. & Balkenius C. 2000. "A Computational Model of Emotional Learning in the Amygdala." From animals to animats 6: Proceedings of the 6th International conference on the simulation of adaptive behavior. Cambridge, MA. MIT Press, 2000. Web address:

Jordan, A. 2002. "Pain without 'Pain'." Web address: Serendip has information on an wide array of different topics in the area of brain and behavior, including papers with web references written by students in Biology 202, a course at Bryn Mawr College. Like other things on Serendip, these are not intended to be the final word on any subject, but rather represent the sense that individuals have been able to make for themselves about particular questions and windows through which others can begin their own explorations of them.

LeDoux, J. "The Emotional Brain, Fear and the Amygdala." In Cellular and Molecular Neurobiology, Vol. 23, Nos. 4/5, October 2003. Web address:

Rifkin, S. 1995. "The Evolution of Primate Intelligence." In The Harvard BRAIN (Harvard's Undergraduate Neuroscience Magazine), Volume II, Issue I, Spring 1995. Web address: Talks about different ways of measuring the brain, as well as different hypotheses regarding the importance of brain size and the evolution of primate intelligence. More comprehensive than Kinser.

Kinser on the relation of the brain to animal intelligence. (Role of neocortex in animal intelligence.) (Relationship between brain size and body size.) (Different ways of measuring intelligence in relation to brain.) (Changes over evolutionary time.) (Brain Size and Evolution - summary of key findings) (Role of neurons.) (Brain size and body size.) (Cortical folding)

McGinn, C. 2003. Review of Antonio Damasio's "Looking for Spinoza: Joy, Sorrow, and the Feeling Brain". In The New York Times, February 23, 2003. Web address: Good Web site: Do fish feel pain? Plus: Fish behaviour relevant to pain Article on scientific meaning of attention Scientific models of attention often include aspects of selectivity, selecting one item in favor of another. Either the selected one is enhanced, or the other one is suppressed. Other models discuss the assignment of resources to items. Due to the resulting reduction of data to be processed, models of computer vision sometimes use mechanisms of visual attention. Another aspect of attention is that it allows to select relevant items and suppress distractors for task specification.

Cotterill, R. 1997. "Navigation, Consciousness and the Body/Mind 'Problem'." In Psyke and Logos, 1997, vol. 18, pp. 337-341. Web address: (Professor Cotterill is a physicist who lectures at Danish Technical University. He has written numerous papers and a best-seller, "Enchanted Looms", on the physiological basisi of consciousness and intelligence.)

Cotterill, R. 2001. "Co-operation of the basal ganglia, cerebellum, sensory cerebrum and hippocampus: possible implications for cognition, consciousness, intelligence and creativity." In Progress in Neurobiology, 64, (2001), 1-33. Web address:

Cotterill, R. 2002. "Mind - A Moving Story." In Science and Consciousness Review 2002, August No. 2. Web address:

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