APPENDIX ONE: Criteria for Animal Pain
Below, after briefly reviewing what I consider to be poor and ambiguous behavioural indicators of pain that have been rejected by scientists, I shall discuss other behavioural indicators that are treated by pain researchers as indices of pain in animals.
Behaviours that do not define pain
The occurrence of stress responses in all cellular organisms and of nociceptive responses to noxious stimuli in nearly all animals, as well as the presence of pain-killing opiates within the brainstems of various kinds of vertebrate and invertebrate animals, may seem to suggest that the ability to experience pain is widespread in the animal kingdom. The results of my investigation are unambiguous: these phenomena cannot be taken as constitutive of pain, because the behaviour observed is capable of being comprehensively modelled by a third-person account, and because no first-person model of the behaviour exists, even though selected features of the behaviour are evocative of conscious behaviour in human beings. My comments on each of these phenomena are summarised in the table below.
Table 4.4 Behaviours which constitute poor evidence for the existence of conscious feelings in animals
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Kind of behaviour: Stress response
Description: A response to any disturbance of the organism's equilibrium.
Examples: The bacterium Bacillus subtilis exhibits stress responses to heat shock, salt stress, ethanol, and starvation for oxygen or nutrients, which are all 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.
Found in which organisms? All cellular organisms
Alternative, "third-person" explanation: The organism is harnessing its internal resources to respond to stressful events which which disturb its equilibrium with its environment.
Grounds for preferring a third-person explanation: Many of our own bodily responses to stressful events take place below the level of consciousness (e.g. the immune system's response to disease). |
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Kind of Behaviour: Nociception
Description: 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.
Examples: 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, snails and octopuses (Smith, 1991).
Found in which organisms? All vertebrate and invertebrate animals except sponges, sharks and rays (Smith, 1991; Rose, 2002).
Sponges lack nociception as they do not have a nervous system (Smith, 1991).
Sharks and rays "lack the neural structures for processing nociceptive information, much less sensing pain" (Rose, 2002, p. 22), possibly because it would be maladaptive for these fish, as they often feed on prey with embedded barbs.
N.B. 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.
Alternative, "third-person" explanation: The organism detects a potentially injurious stimulus with its sensors, transmits information about it, and responds appropriately to it.
Grounds for preferring a third-person explanation:
2. Nociception is known to be mediated by the brainstem. Direct stimulation of the brainstem is not consciously perceived in human beings.
3. Nociception occurs in simple animals (cnidaria) that cannot plausibly be credited with conscious feelings. |
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Kind of Behaviour: Presence of opiate receptors and manufacture of opioid substances within the organism's body
Description: Many animals 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.
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).
Found in which organisms? Opioids are found not only in vertebrates but also in invertebrates (Stefano, Salzet and Fricchione, 1998), including earthworms, insects and molluscs (Smith, 1991).
Alternative, "third-person" explanation: 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). Opioid peptides not only alleviate pain, but also serve to stimulate immunocytes, which stage an immune reponse in the body. Both pain-killing opioids and anti-bacterial compounds are found in invertebrates as well as vertebrates (Stefano, Salzet and Fricchione, 1998). In addition, there are chemical affinities between opioids and bacteriocides: pro-enkephalin, a naturally occurring analgesic molecule, contains an anti-bacterial peptide named enkelytin, which may be released along with the opioid peptides during immune defence (Stefano, Salzet and Fricchione, 1998, p. 267). Bacteria and viruses are and always have been persistent threats to animals, which had to develop means of combating these threats. Enkelytin may have a dual function: 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. This combination of analgesic priority-setting activities with an anti-infectious / anti-inflammatory process 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 (Stefano, Salzet and Fricchione, 1998, p. 267).
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.
Grounds for preferring a third-person explanation: A complete "third-person" model has been developed, but no general "first person" account appears has been formulated. In any case, a "first-person" account does no extra explanatory work.
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Kind of behaviour: Flavor aversion learning.
Description: The ability of animals to learn after a single exposure to avoid foods whose taste they associate with subsequent digestive illness.
Found in which organisms? Flavour aversion learning is well-studied in mammals and birds. Recent experiments (Cabanac, 2003; Paradis and Cabanac, 2004) have shown that reptiles (specifically, basilisks and skinks) show this learning effect too. Frogs and toads show no such learning effect, despite every effort being made to induce strong aversion in the amphibians. Invertebrates, while capable of changing their food preferences as a result of conditioning, cannot acquire aversion to new foods (Paradis and Cabanac, 2004). Paradis and Cabanac suggest that this constitutes evidence that reptiles, birds and mammals, but not other animals, are capable of developing dislikes for foods that make them ill.
Alternative third-person explanation: Flavour-aversion learning can be explained as a purely automatic process that can occur without any attention on our part (Utah State University, 1995). Grounds for preferring a third-person explanation: According to Paradis and Cabanac (2004), flavour aversion learning may occur even while an animal is asleep. It is hard to see how such learning can be used to establish the occurrence of conscious feelings. For this reason, I cannot agree with Cabanac (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: at most, it shows that they do not enjoy the taste of food. |
Ambiguous evidence
The evidence which I have placed in this category includes: classical and instrumental conditioning; and operant conditioning. Because these kinds of behaviour are emotional, they more suggestive of conscious feelings than the behaviours described above, but their status as evidence for phenomenally conscious feelings in animals remains problematic. My reasons for rejecting these kinds of evidence are summarised in the table below.
Table 4.5 Behaviours which constitute evidence for the existence of feelings in animals, but not conscious feelings
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Kind of Behaviour: Classical and instrumental conditioning Description: An animal undergoing conditioning learns to seek or avoid a conditioned stimulus depending on the qualities of the primary reinforcer (unconditioned stimulus) it is associated with. See chapter two for further discussion. Bermudez (2000) argues conditioning works because primary reinforcers 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). Examples: The roundworm C. elegans is routinely used in studies of classical and instrumental conditioning.
Found in which organisms? All animals except sponges, cnidaria and possibly flatworms.
Alternative, "third-person" explanation: Conditioning can be described using a goal-centred intentional stance, as we saw in chapter two. We can also explain the behaviour of conditioned animals using third-person terminology: reinforcers work because animals have innate drives to seek or avoid them.
Grounds for preferring a third-person explanation: Conditioning has been observed in the severed spinal cords of rats, the legs of cockroaches and the human autonomic nervous system - none of which are likely to be conscious (see chapter two).
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). |
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Kind of Behaviour: Operant conditioning.
Description: An animal undergoing operant conditioning learns to reach an attractive stimulus or avoid a potentially injurious stimulus by fine-tuning its motor movements.
Examples: Fruit flies are capable of fine-tuning their flight behaviour to avoid a heat beam (Brembs, 2000). See discussion in chapter two.
Found in which organisms? Insects, some molluscs and vertebrates.
Alternative, "third-person" explanation: Operant conditioning does not require phenomenal consciousness. Access consciousness is what is required.
Grounds for preferring a third-person explanation: Scientific evidence (see section 4.1.2) that access consciousness can take place in the absence of phenomenal consciousness. |
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Kind of Behaviour: Self-administration of analgesics.
Description: Cases where injured animals will actively seek out analgesic drugs. Examples: Grandin and Deesing (2002) describe 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.
Found in which organisms? Mammals, at least.
Alternative, "third-person" explanation: Grounds for preferring a third-person explanation: It might be useful to contrast the rats' preference for opiates and willingness to tolerate a bitter taste in exchange for pharmacological relief can be compared with chemical "weighing-up" processes that are known to occur in bacteria. 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. By comparison, the rats' behaviour is far less rigid than that of the bacteria. While the rats' behaviour is far less rigid than that of the bacteria, 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 true behavioural flexibility (as defined in chapter two) in animals weighing up their options. |
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Kind of Behaviour: Pain-guarding
Description + Examples of Third-person phenomema: The animal shows protective behaviour towards an injured part of its body. 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).
N.B. A recent, well-publicised report by Sneddon, Braithwaite and Gentle (2003), claiming to have identified pain-guarding 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.
Explanation in Third-Person Terminology: Some instances of pain-guarding may be nociceptive responses to injury. For instance, an animal with an injured leg benefits from nociceptive reflexes that encourage keeping its weight off the leg.
Description + Examples Better Construed as First-person Phenomema
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. Grounds for preferring a First-person Interpretation: An animal's pain-guarding of a structurally sound limb is difficult to explain unless it is still in conscious pain. |
Pain-guarding
Although the phenomenon of pain-guarding is too evidentially ambiguous to establish the presence of pain in an animal, 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.
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.xx Insects (and by extension, worms, whose nervous systems are simpler) are incapable of feeling conscious pain.
In particular, pain-guarding of a structurally sound limb appears to serve no biological function that would warrant a third-person description. Incidentally, a recent, well-publicised report by Sneddon, Braithwaite and Gentle (2003), claiming to have identified pain-guarding in fish, has been subjected to a devastating critique by Rose (2003a), who argues convincingly that the report's authors engaged in sloppy methodology and mis-interpreted their own findings.
APPENDIX:
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 behaviours (exhibited by decorticate human beings) that can be purely nociceptive and unconscious.
Rose also criticises the philosophically naive assumption of some people who argue that fish are capable of undergoing pain, that any behaviour which is not reflexive must be conscious.
END APPENDIX