In this section, I address a paradox: the typical behavioural reactions that manifest fear and/or pain in humans and other animals can all take place in the absence of phenomenal consciousness, yet we use these very reactions to identify the occurrence of conscious fear and/or pain in animals. I argue that this identification has a legitimate basis, but only for those animals that are already known to possess the neural wherewithal for phenomenal consciousness. For other animals, I argue that pain-guarding of an injured limb is a necessary but not a sufficient condition for being able to experience pain. As insects (including honeybees) do not pain-guard, we can be reasonably sure that they do not experience pain.
An inferential approach to the identification of conscious feelings in animals
It was argued above (Conclusion 4.xx) that similarity arguments and arguments based on homology were not strong enough to establish the occurrence of conscious feelings in non-mammals, who lack a neocortex and a clear homologue thereof. For birds, I employed a causal argument from analogy to suggest that they were indeed phenomenally conscious. I was unable to apply this argument to reptiles, octopuses and honeybees. For all of these animals, however, there is tentative behavioural evidence of consciousness. In this section, I propose to examine the issue of what kind of behaviours should count as evidence for fear and pain.
The strategy I shall employ in the remainder of chapter 4, part 1, for identifying behaviours that indicate conscious feelings in animals is one of "inference to the best explanation" - that is, attempting to "identify behaviors for which it seems that an explanation in terms of mechanisms involving consciousness might be justified over unconscious mechanisms" (Allen, 2002). If we can make better scientific predictions about a certain kind of phenomenon by using a "first-person" account than by adopting a "third-person" account then we should adopt the former.
Note: in this chapter, when I use the term "pain" I mean a conscious experience. I am adhering here to the usage employed by the International Association for the Study of Pain (1999; see Rose, 2002). The term "fear", as I use it, denotes an emotion which may or may not be conscious.
The identification of fear
Animals possess a variety of neural mechanisms for defending themselves against harm. Prescott (1999) describes the hierarchical organisation of these neural defence mechanisms in rats. At the lowest level, systems in the spinal cord deal with the problem of actual or imminent harm caused by noxious, contact stimuli. The typical response mechanism displayed here is that of reflex withdrawal (e.g. if the rat's paw touches something hot).
At a higher level, hindbrain mechanisms, which are found in all vertebrates, provide rapid responses to distal stimuli that warn of possible harm. For instance, a rat exhibits a startle response to a loud noise. The circuits underlying this response appear to be homologous to escape circuits in fish nervous systems.
Systems in the midbrain and hypothalamus, which are also common to all vertebrates, add a greater degree of sensory and motor refinement, allowing an animal to respond proactively to signs of danger. Sensory systems enable an animal to recognise and locate distant, species-specific threat stimuli, while motor systems co-ordinate a freeze / flight / fight response, depending on the proximity of the threat. A rat will typically freeze in response to a threat which is more than 10 metres away, flee when the threat is 5 to 10 metres away if an escape route is available, switch to defensive vocalisation at distances of less than 0.5 metres and at even closer range, attack with wild jumping and biting behaviour. Mammals whose cortex and limbic systems have been removed display these responses whenever the triggers are presented, irrespective of whether they are appropriate in the wider context.
The limbic system allows an animal to learn arbitrary stimuli that can predict harm, through classical conditioning in the amygdala, which puts an "emotional stamp" on any sensory input that is simultaneous with, or just prior to, a noxious stimulus. For instance, after just a few pairings of a light (neutral stimulus) with a harmful electrical shock will suffice to elicit defensive reactions in a rat. However, the learning is context-specific, as the hippocampus and septum provide the amygdala with contextual knowledge that enables it to distinguish threatening from non-threatening situations. This conditioned emotional response is independent of the cortex. Homologues of the different components of the limbic system, including the amygdala, are present in all vertebrates, with the possible exception of the most ancient vertebrate class (jawless fish).
Lastly, systems in the frontal cortex enable an animal to "unlearn" associations between arbitrary stimuli and harm. These associations are never erased from the animal's amygdala, but the frontal cortex can learn to inhibit the learned response to the stimulus, if the animal is later repeatedly exposed to the neutral stimulus without suffering any harm. According to Prescott (1999), only mammals are known to possess this inhibitory mechanism, but Lissek and Gunturkun (2003) have recently described a similar mechanism in birds.
The question of which system corresponds to the first emergence of the emotion of fear can be answered by looking for evidence of intentional agency. The freeze / flight / fight response behaviour generated by the midbrain seems too inflexible to qualify as intentional. However, the amygdala's ability for context-specific learning (which allows it to distinguish threatening from non-threatening stimuli) is a more sophisticated reponse which is amenable to self-correction (which, as we saw in chapter two, is one of the pre-requisites of agency). In chapter three, it was shown that the limbic system regulates several distinctive patterns of response to primal challenges, each of which corresponds to a genuine emotion in animals.
Conclusion 4.xx All vertebrates undergo fearful stress (at a non-conscious level) when they encounter a harmful stimulus.
Should the limbic system's pattern of behavioural response count as evidence for phenomenally conscious fear? I would argue that it should not, for two reasons. First, it can be adequately described and modelled without the use of first-person terminology. Second, from a neurological standpoint, only the highest level of response, mediated by the frontal cortex, engages all of the levels of the brain (including the cortex) that are known to be required for consciousness (see Conclusion 4.33).
Conclusion 4.xx No fearful reaction per se can establish that an animal is undergoing phenomenally conscious fear.
This is a paradoxical conclusion, as it is precisely these reactions which we customarily use to infer the presence of fear in other individuals. The resolution of the paradox, I suggest, is that we already have good grounds for believing that these individuals are similar enough to us to be capable of phenomenally conscious experiences. The only animals we have identified so far are mammals and birds.
Conclusion 4.xx It is legitimate to infer the occurrence of conscious fear in an individual animal on the basis of his/her reactions, provided that we have prior grounds for believing that the animal has the neurological wherewithal for phenomenal consciousness.
Conclusion 4.xx It is likely that only mammals and birds experience phenomenally conscious fear.
Preliminary remarks about pain
The identification of conscious pain in animals is complicated by the fact that its biological function remains poorly understood. The popular notion that pain serves as an "alarm bell", which alerts the animal to an injurious stimulus and which may be temporarily shut down during a "fight-or-flight" situation, is too simplistic to be correct. Such a notion fails to explain what selective advantage an animal with a capacity for conscious pain would have over an animal that lacked consciousness but possessed the ability to detect and respond appropriately to noxious stimuli (i.e. nociception, which does not require conscious awareness). Oft-cited cases of individuals who are disadvantaged by their congenital insensitivity to pain are irrelevant, as these individuals lack nociception as well (Allen, 2003). Recently, it has been suggested that pain may serve a useful function in enabling animals to learn better ways of dealing with actual or possible tissue damage, and that phenomenal experience may be the best explanation for some forms of learning involved (Allen, 2003). However, it has been argued in the previous chapter that none of the varieties of associative learning seem to require phenomenal consciousness.
A complete explanation of pain, which incorporates the "why" as well as the "what", thus continues to elude us. However, it would be excessively pessimistic to conclude, as Allen does, that "the existing arguments for and against the existence of animal pain remain weak" (2003, p. 19) and that the question of which animals feel pain cannot be resolved until we understand its biological function (2003, pp. 17-20). Scientists are already in possession of a large body of neurological evidence regarding how pain originates in the nervous system and brain, as well as a vast amount of experimental evidence from animal studies sponsored by the pharmaceutical industry, which is continually endeavouring to find new and better treatments for pain in human beings. These studies would be of little value unless scientists were able to reliably identify pain in experimental animals.
Are there any clear behavioural indicators of pain in animals?
Rose (2002) emphasises the following points in his survey of the scientific literature relating to pain:
(1) Pain is a well-understood phenomenon: "pain and its neurological basis have been under intense and productive investigation for decades" (Rose, 2002, p. 29).
(2) Nociception is not the same thing as pain. Pain, as defined by the International Association for the Study of Pain, is essentially a conscious experience. In particular: (i) pain is an unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage; (ii) pain is always subjective; (iii) pain is sometimes reported in the absence of tissue damage and the definition of pain should avoid tying pain to an external eliciting stimulus (Rose, 2002, p. 15). Nociception, defined as "the activity induced in ...nociceptive pathways by a noxious stimulus" (2002, p. 15), "does not result in pain unless the neural activity associated with it reaches consciousness" (Rose, 2002, p. 16).
(3) In all vertebrates, the fundamental behavioural reactions to injurious stimuli are generated by neural systems in the spinal cord and brainstem. These reactions include withdrawal of the stimulated body part, leg locomotion, struggling, facial grimacing, and in some animals vocalisation (Rose, 2002, pp. 16-17).
(4) These behavioural reactions occur in people who are unconscious - for example, people with extensive cortical damage and children born without cerebral hemispheres (Rose, 2002, pp. 13-14, 17), as well as in animals .
(5) Activity in the cortex is responsible for both the cognitive-evaluative components of pain (attention to the pain, perceived threat to the individual, and conscious generation of strategies for dealing with the pain), as well as the emotional unpleasantness (suffering) aspect of pain. The cognitive-evaluative component of pain depends on the anterior cingulate gyrus, prefrontal cortex, and supplementary motor area, while the emotional unpleasantness of pain depends on the anterior cingulate gyrus and the prefrontal cortex (Rose, 2002, pp. 19-21).
In an Appendix, I discuss in detail the behavioural response patterns that have been proposed as measures of pain in animals, and conclude that since these responses are regulated at levels of the brain below the level of consciousness, none of them can be regarded as an unambiguous indicator of animal pain.
In particular:
Conclusion 4.xx A stress response in an organism does not constitute a sufficient warrant for ascribing conscious feelings to it.
Conclusion 4.xx Nociception per se does not constitute a sufficient warrant for ascribing conscious feelings to an animal.
Conclusion 4.xx The presence of opiate receptors in an animal's brainstem does not constitute a sufficient warrant for ascribing conscious pain to it.
Conclusion 4.xx An animal's ability to undergo flavour aversion learning does not constitute a sufficient warrant for ascribing conscious feelings to it.
Conclusion 4.xx An animal's ability to undergo associative learning (classical or instrumental conditioning) does not constitute a sufficient warrant for ascribing conscious feelings to it.
Conclusion 4.xx An animal's ability to undergo operant conditioning does not constitute a sufficient warrant for ascribing conscious feelings to it.
Conclusion 4.xx A complex nociceptive response to noxious stimuli is not a sufficient warrant for ascribing conscious pain to animals.
Conclusion 4.xx Absence of pain-guarding in certain kinds of animals is strong evidence that they are incapable of feeling conscious pain.
Conclusion 4.xx Pain-guarding of a structurally sound limb is good prima facie evidence of conscious pain.
Conclusion 4.xx An injured animal's preference for a bitter solution containing analgesics over a sweet solution constitutes suggestive of but not conclusive evidence that it is consciously experiencing pain.
Models of animal pain
Animal models for various kinds of pain (see Eaton, (2003), Schwei et al. (1999) and Honore et al. (2000))are described in an Appendix. The criteria for two kinds of animal pain are shown below.
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Kind of pain: Acute phasic pain.
Cause: a high-intensity stimulus.
How it is measured: a rapid response which is specific to the kind of nociceptors activated.
Kinds of tests used: Three tests are commonly used to measure acute pain in animals (mostly rats and mice).
The tail-flick test uses a radiant heat-source and an automated timer to determine the withdrawal time of the tail. This test is reliably used to reveal the potency of opioid analgesics and to predict their efficacy in humans.
The hot-plate test involves placing a mouse or rat in an open space on a metallic floor capable of being precisely heated, and measuring the time it takes for the animals to react by licking their paws and jumping in the air. This test yields inconsistent results in rats because their movements are chaotic and difficult to identify and observe.
The paw-pressure test involves placing the animal's hind-paw between a plane surface and a blunt point mounted on cogwheels, and mechanically applying increasing pressure until the animal removes its tail. The force applied corresponds to the threshold of the animal's response. However, because the threshold intensity is difficult to reproduce, the test is more often used to compare response thresholds for a paw injured beforehand by inflammation or nerve injury, with that of a non-injured paw.
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Kind of pain: Chronic cancer pain
Cause: cancer-induced bone destruction induces an ongoing pain that is referred to the bone and is initially experienced as contsant and dull. Over time, its intensifies and can become incapacitating.
How it is measured: Pain-guarding of the affected limb is considered to indicate ongoing pain. This behaviour correlates with the extent of bone destruction. Once significant bone destruction has occurred, mice exhibit hypersensitivity to touch (palpation). This behaviour correlates with the extent of bone destruction and is considered to indicate pain when the limb is handled. A protective (nocifensive) behavioural response to touch that causes no pain in normal animals is positively and significantly correlated with the progression of the bone cancer. Finally, morphine, which reduces bone cancer pain in humans, reduces pain-related behaviours in rats (Honore et al., 2000; Schwei et al., 1999).
Kinds of tests used: In the model of bone cancer pain developed by Schwei et al. (1999), animals were observed 21 days after bone cancer was induced by injection of a sarcoma. They were subjected to mechanical stimulation (palpation) of the femur which would normally not be noxious. Their behaviours were ranked on a scale of 0 to 5: no reaction during palpation (0); pain-guarding of the hindlimb (1); guarding and strong withdrawal of the hindlimb (2); guarding, strong withdrawal and fighting (3); guarding, strong withdrawal, fighting and audible vocalization (4); guarding, strong withdrawal, fighting, audible vocalization and intense biting (5). In the model developed by Honore et al. (2000), mechanical allodynia (abnormal tactile sensitivity to stimuli that are not usually harmful or painful) is determined by measuring the paw withdrawal threshold in response to probing with fine hairs. Both the number and duration of occurrences of pain guarding (holding the paw aloft while not ambulatory) are measured over a 5-minute interval, as an index of ongoing pain. Morphine has been shown to increase the mechanical threshold to paw pressure and to reduce pain guarding.
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Although the criteria used to identify pain vary according to the kind of pain being investigated, certain recurring themes are readily apparent:
Conclusion 4.xx When determining criteria for conscious states in animals, we should use behaviours that: (i) can be measured on a scale; (ii) correlate well with other measures of the state and also with descriptions of the state in human beings; (iii) are highly specific; (iv) have a causal structure that parallels that in human beings; and (v) can be used to define the state. We should avoid criteria that: (i) give inconsistent results; (ii) are difficult to reproduce; (iii) are non-specific; (iv) can be interpreted in other ways (are ambiguous).
The paradox of pain
Although some of the behaviours used to identify chronic pain (allodynia and pain-guarding) are more suggestive of phenomenal consciousness, most of the criteria used to identify pain in animals are purely nociceptive and none of them need be phenomenally conscious. Once again, we are confronted with a paradox. What justifies using nociceptive behaviour and vocalizations to identify pain in animals, if they are controlled by systems in the brain that operate below the level of consciousness? The answer, I suggest, is the same as for fear: we already have good grounds for believing that these individuals are similar enough to us to be capable of phenomenally conscious experiences.
Conclusion 4.xx It is legitimate to infer the occurrence of pain in an individual animal on the basis of its reactions, provided that we have prior grounds for believing that the animal has the neurological wherewithal for phenomenal consciousness.
Conclusion 4.xx It is likely that only mammals and birds experience pain.
CASE STUDY: Pain in Fish
The fact that we can identify homologues between brain parts in mammals and vertebrate non-mammals at the gross level can yield useful negative as well as positive results.
First, because their brain parts are homologous to those of mammals, we can rule out alternative mechanisms for generating consciousness in those vertebrates whose brains lack the quantitative and qualitative features required to support consciousness in mammals.
The question of whether fish feel pain has recently attracted attention in the media (BBC, 2003). Rose (2002) has written an exhaustive critique of arguments for that fish feel pain, concluding that consciousness of any kind in fish is "a neurological impossibility" (2002, p. 2). First, fish lack the quantitative and qualitative features that support consciousness in mammals, which Rose summarises as "exceptionally high interconnectivity within the cortex and between the cortex and thalamus, and enough nonsensory cortical mass and local functional diversification to permit regionally specialized, differentiated activity patterns" (2002, p. 21). In fish, for example, we find the cerebral hemispheres are much smaller and less organised than those of mammals.
Second, the entire range of behaviour in fish, including learning abilities, is controlled not by their cerebral hemispheres but by motor mechanisms that are located in the brainstems of mammals and non-mammalian vertebrates alike:
In fishes, the degree to which most aspects of neurobehavioral function are controlled by the brainstem and spinal cord is extreme, as shown by experiments in which the cerebral hemispheres have been removed from diverse species of fishes, leaving only the brainstem and spinal cord intact ... The behavior of these fishes is strikingly preserved. They still find and consume food, show basic capabilities for sensory discrimination (except for the loss of the sense of smell, which is processed entirely in the forebrain) and many aspects of social behavior, including schooling, spawning, and intraspecies aggression. Although there are some species differences, courtship, nest building, and parental care often persist after forebrain removal. Most of the forms of learning of which fishes are capable are intact in the absence of the forebrain, although avoidance learning seems to be much more difficult for fish with the cerebral hemispheres removed ... This difficulty with avoidance learning is not due to reduced responsiveness to noxious stimuli because the reflexive and locomotor, including escape, responses to such stimuli by fish without cerebral hemispheres appear to be quite normal. The general conclusion that emerges from many studies is that the basic patterns of fish behavior are controlled by lower brain structures, mainly the brainstem and spinal cord. The cerebral hemispheres serve mainly to "modulate" behavior, that is, to regulate its intensity or frequency and to refine its expression (Rose, 2002, p. 8).
Third, the mechanisms that cause behaviour in fish are shared with human beings, in whom they are known to be non-conscious. The brainstems of fish are built on the same structural principles as our own - indeed, their design is simpler than our own (Russell, 1999). In humans, activity confined to the brainstem is inaccessible to consciousness (Roth, 2003, pp. 36, 38).
Rose concludes:
[F]ish brains are understood well enough to make it highly implausible that there are alternate, functionally uncommitted systems that could meet the requirements for generation of consciousness (Rose, 2002, p. 21).
Rose (2002), who has comprehensively reviewed the current literature on the neural basis of pain and other forms of primary consciousness, argues that even complex nociceptive behaviour in human beings and other animals need not imply the occurrence of conscious pain. The nub of his case is that the brain's response to noxious stimuli occurs at levels of the brain that are inaccessible to consciousness - the brain stem and spinal cord:
A critical point in this analysis is the fact that a large part of the activity occurring in our brain is unavailable to our conscious awareness (Dolan, 2000; Edelman and Tononi, 2000; Koch and Crick, 2000; Libet, 1999; Merikel and Daneman, 2000). This is true of some types of cortical activity and is true for all brainstem and spinal cord activity (Rose, 2002, p. 15, italics mine).
Citing numerous authorities, Rose then argues that since nociceptive behavioural reactions, "including vocalization, facial grimacing, and withdrawal, are mediated by subcortical brain and spinal systems" we may conclude that "the behavioural displays related to noxious stimuli or emotion in humans ... can be evoked without any corresponding awareness of noxious stimuli" (2002, p. 17).
Rose then concludes that the complex nociceptive responses exhibited by animals such as fish do not necessarily indicate that they are consciously experiencing pain. Rose acknowledges that fish display "robust, nonconscious, neuroendocrine, and physiological stress responses to noxious stimuli" (2002, p. 1), but insists that "[c]onscious experience of fear... [and] pain, is a neurological impossibility for fishes" (2002, p. 2), because they lack a true neocortex, which only mammals have.
It needs to be kept in mind that Rose's negative conclusions regarding the occurrence of pain and primary consciousness in fishes presuppose what Panksepp would describe as a "cognitive" account of consciousness. For instance, one of Rose's key arguments is that complex nociceptive responses cannot establish the occurrence of pain, as they are also found in decorticate human beings and patients in a permanent vegetative state. The assumption here (which reflects the views of most but not all neurologists) is that these human beings are not conscious.
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 behavioural wakefulness without consciousness (Rose, 2002, pp. 14, 17).