Image courtesy of Wisconsin Department of Transportation.
This appendix has ten parts:
1.1 Can access consciousness occur in the absence of phenomenal consciousness?
1.3 Other kinds of consciousness in animals: integrative consciousness and object consciousness
1.4 Lurz's criteria for consciousness - attention and object recognition - are found in insects
1.5 Evaluation of Carruthers' arguments against the occurrence of consciousness in non-human animals
1.6 Two kinds of phenomenal consciousness in animals? An evaluation of Panksepp's arguments
1.7.1 An evaluation of Panksepp's criteria for affective consciousness
1.9 The neurological evidence for consciousness in birds, reptiles, amphibia and fish
1.10 How the welfare of animals lacking phenomenal consciousness can be objectively assessed
The case of the distracted driver
Block (1995, 1998) makes some pertinent observations regarding the much-discussed case of the distracted driver, who is supposedly able to navigate his car home despite being oblivious to his visual states. Different philsophers have conflicting intuitions regarding whether the driver is phenomenally conscious while driving home. But according to Block, this is irrelevant: to drive home, what you need is access consciousness, not phenomenal consciousness. Access consciousness, Block suggests, comes in degrees: the inattentive driver has a diminished level of access consciousness, but if he had none at all, the car would crash. An alternative considered by Block (1995) is that the driver's access consciousness is normal, but his poor memory of the trip is due to failure to store the contents of the scene in his memory. (As we shall see, this turns out to be the case.) Likewise, when discussing a case (originally cited from Penfield (1975) and discussed by Searle (1992)) of an epileptic driver who has a petit mal seizure rendering him totally unconscious, but is still able to drive home, the individual "still has sufficient access-consciousness to drive" (1998, p. 5).
Recent research (Wright, 2003) has borne out Block's contention that attention is required for driving. Wright cites three driving studies which show that driving requires a certain minimum amount of attention to the road. As Wright (2003) puts it: "Without sufficient attention being paid to one's visual experience and driving behavior, one will quickly find one's car quite mangled." 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 surprise when he comes to the end of his journey.
In the light of the research cited by Wright, I therefore have to express scepticism about the solitary case of Penfield's (1975) "unconscious driver" cited by Searle (1992) and discussed by Block (1995, 1998). The proposal that a person having a petit mal seizure could drive home appears implausible in the light of the following medical description:
A petit mal seizure is a temporary disturbance of brain function caused by abnormal electrical activity in the brain and characterized by abrupt, short-term lack of conscious activity ("absence") or other abnormal change in behavior.Petit mal seizures occur most commonly in people under age 20, usually in children ages 6 to 12.
Typical petit mal seizures last only a few seconds, with full recovery occurring rapidly and no lingering confusion. Such seizures usually manifest themselves as staring episodes or "absence spells" during which the child's activity or speech ceases.
The child may stop talking in mid-sentence or cease walking. One to several seconds later, speech or activity resume. If standing or walking, a child seldom falls during one of these episodes...
There is usually no memory of the seizure (Campellone, 2002).
There are thus no grounds for believing that there are any real-life cases of drivers who possess access consciousness but have lost their phenomenal consciousness, as Block hypothesises (1998, p. 5). Rather, what happens is that inattentive drivers fail to encode the contents of their phenomenal consciousness in their long-term memory (Wright, 2003).
Conclusion: "Distracted driver" cases cannot be legitimately used to argue against phenomenal consciousness in animals.
Sleepwalking
Even more implausible is the claim, sometimes found in the literature on animal consciousness (Cartmill, 2000) that sleepwalkers can drive. Regrettably, this myth is perpetuated by people who ought to know better. Jiva and Masoodi (2003) repeat this claim in a medical journal of sleep research, but the reference they cite (Cruchet R. 1905. Tics et sommeil. Presse Med. 1905; 13:33-36) is 100 years old. (Incidentally, Jiva did not respond to an email query of mine, requesting evidence for driving by sleepwalkers.)
It is true that sleepwalkers can engage in a range of non-reflex complex behaviours (autonomous automatisms) that are performed without conscious volition, such as dressing, eating, and bathing (Sleepdisorderchannel, 2003). However, two important points need to be made here. First, sleepwalkers do not pay attention to their surroundings, for the simple reason that they cannot. Sleepwalking episodes take place during delta sleep, a slow-wave phase that scientists associate with the absence of primary consciousness. "During sleepwalking, coordination is poor, speech is incoherent, clumsiness is common" (Jiva and Masoodi, 2003). Some sleepwalkers bruise or injure themsleves from collisions with furniture and walls (Sleepdisorderchannel, 2003). We may conclude that access conscious is absent.
Second, sleepwalkers do not acquire new skills; they simply use their existing repertoire of automatisms. Any motor skills that sleepwalkers show are parasitic upon those they acquired during the waking state, while phenomenally conscious. Sleepwalkers do not learn any "new tricks".
By contrast, it has already been shown in chapter two that most phyla of animals are capable of true learning (classical conditioning). A more advanced kind of learning (operant conditioning) was also proposed for insects and cephalopods, as well as vertebrates.
Conclusion: The behaviour of sleepwalkers has no relevance to the question of which animals are conscious.
Blindsight and super-blindsight
Blindsight has sometimes been proposed as an instance of access without phenomenality. However, subjects with blindsight appear to lack the right sort of access to visual information on their blind side:
Their access is curiously indirect, as witnessed by the fact that it is not available for verbal report, and in the deliberate control of behavior. The information ... can be made available to other processes, but only by unusual methods such as prompting and forced choice. So this information does not qualify as directly available for global control (Chalmers, 1996, p. 227).
Block's (1995) hypothetical case of "super-blindsight" makes a testable empirical claim, but there is no evidence for its occurrence in human or non-human animals.
Reverse Anton's Syndrome
Block (1998, p. 4) also discusses one possible case of "Reverse Anton's Syndrome", but its interpretation is by no means certain. Because the condition was caused by brain injury, it cannot be invoked as evidence that access consciousness could have evolved in animals independently of phenomenal consciousness.
Libet's experiments
Rosenthal (2002) cites experimental results by Libet et al. (1983), in which a rational human agent's (access-conscious) decision to act occurs some time before she is consciously aware of it, as evidence that "global access" can occur independently of phenomenal consciousness. But an alternative interpretation is possible: the subject forms a conscious intention at the beginning of the experiment, when receiving instructions. The subsequent decision to move reported by the subject is not a voluntary action in the conventional sense, but a perceived effective urge to move, induced by specific experimental instructions (Zhu, 2003).
The mammalian visual system
Among the cases discussed in the philosophical literature, the strongest evidence that access consciousness can exist in the absence of phenomenal consciousness comes from recent studies of the mammalian visual system:
According to Milner and Goodale (1995), the human mind / brain contains two visual systems that are functionally and anatomically distinct; and indeed, there is now a wealth of evidence that this is so (Jacob and Jeannerod, 2003). The dorsal system is located in the parietal lobes and is concerned with the on-line detailed guidance of movement. The ventral system is located in the temporal lobes and serves to underpin conceptual thought and planning in relation to the perceived environment. Each receives its primary input from area V1 at the posterior of the cortex, although the dorsal system also receives significant projections from other sites. The dorsal system operates with a set of body-centered or limb-centered spatial co-ordinates, it is fast, and it has a memory window of just two seconds. The ventral system uses allocentric or object-centered spatial co-ordinates, it is slower, and it gives rise to both medium and long-term memories. Importantly for our purposes, the outputs of the dorsal system are unconscious, while those of the ventral system are phenomenally conscious (in humans). Finally, homologous systems are widespread in the animal kingdom, being common to all mammals, at least. On this account, the phenomenally conscious experiences that I enjoy when acting are not the percepts that guide the details of my movements on-line. Rather, the phenomenally conscious percepts produced by the ventral system are the ones that give rise to my beliefs about my immediate environment, that ground my desires for perceived items ("I want that one") and that figure in my plans in respect of my environment ("I'll go that way and pick up that one"). But my planning only guides my actions indirectly, by selecting from amongst a data-base of action schemata. The latter then directly cause my movements, with the detailed execution of those movements being guided by the percepts generated by the dorsal system (Carruthers, 2004b).
The research by Milner and Goodale (1995) suggests that each human brain has two visual systems: a phenomenally conscious system that allows the subject to select a course of action but which she cannot attend to when actually executing her movements, and an access-conscious system that guides her detailed movements but is not phenomenally aware. Care should be taken not to exaggerate the significance of these findings, as they relate to just one sensory modality (sight) and only apply to a limited class of animals (mammals). Nevertheless, they are significant insofar as they reveal a distinction at the physical level between access-consciousness and phenomenal consciousness.
This leads me to formulate the following tentative conclusion:
Conclusion: The occurrence of access consciousness is physically distinguishable from the occurrence of phenomenally conscious states in a human being.
Behavioural wakefulness can certainly exist in the absence of phenomenal consciousness. As an extreme example, Rose (2002, p. 14) discusses six human patients (first described in Jouvet, 1969), who had suffered the complete loss of their cerebral cortex. Some of these decorticate patients still displayed intermittent wakefulness, manifested by the presence of behavioural sleep-wake cycles, and even exhibited behaviours such as grimacing and cries evoked by noxious stimuli, and pushing at the hands of the examiner. The condition of persistent vegetative state, in which "persons with overwhelming damage to the cerebral hemispheres commonly pass into a chronic state of unconsciousness" (JAMA, 1990), has been defined as "chronic wakefulness without awareness" (JAMA, 1990). Patients exhibit behavioural sleep-wake cycles - in contrast with coma, during which patients are never awake. PVS patients may exhibit behaviours such as grinding their teeth, swallowing, smiling, shedding tears, grunting, moaning, or screaming without any apparent external stimulus. The point that needs to be made here is that all of the wakeful behaviours displayed by these patients are generated by their brain stems and spinal cords. Studies have shown that activity occurring at this level of the brain is not accessible to conscious awareness in human beings (Rose, 2002, pp. 13-15; Roth, 2003, p. 36). (For a more complete discussion of PVS, see JAMA, 1990; Multi-Society Task Force on PVS, 1994; Laureys, 2002; Baars, 2003; National Health and Medical Research Council, 2003. Borthwick, 1996, critiques the medical criteria used to define PVS, and argues that misdiagnoses are common and that the condition should not be viewed as irreversible.)
Conclusion: If we define wakefulness according to behavioural criteria, then its occurrence in an animal is an insufficient reason for ascribing phenomenally conscious states to it.
The point I am making here is a purely negative one. Let me state clearly that I am not proposing that the behaviour of PVS patients, who require assisted feeding in order to stay alive, is a model for that of behaviourally wakeful animals lacking a cortex. On the contrary: whereas humans and other mammals are very much dependent on their cerebral hemispheres for functionally effective behaviour, other animals exhibit much less dependence or none at all (Rose, 2002, pp. 9, 10, 13).
A snake presumably uses transitive consciousness to hunt its prey. However, Grandin (1998) cites research by Sjolander (1993), sugesting that a snake does not have a centralised internal representation of its prey:
It seems to live in a world where a mouse [its prey] is many different things... [S]triking the mouse is controlled by vision; following the mouse after striking is controlled by smell; and swallowing the mouse is controlled strictly by touch. There is no integration of information from all the senses. Each sensory channel operates independently of the others. When a snake has a mouse held in its coils, it may still search for the mouse as if the information from its body which is holding the prey did not exist. It appears that the snake has no ability to transfer information between sensory channels (Grandin, 1998).
I propose to use the term integrative consciousness to designate the kind of consciousness which gives an animal access to multiple sensory channels and enables it to integrate information from all of them.
Grandin (1998) also observes that a snake, unlike a predatory mammal, has no ability to anticipate that a mouse running behind a rock will reappear (Grandin, 1998). Thus it may be said to lack what I would call object consciousness.The relationship between these concepts of consciousness and phenomenal consciousness remains to be determined.
According to Lurz's (2003) same-order (SO) account of consciousness, a creature's experiences are conscious if it is conscious of what its experiences represent. by of what Lurz means their intentional object, or what they are about. Lurz evidently regards consciousness as a common animal phenomenon:
[M]any animals seem to attend to certain features of what they are perceiving ... which suggests that they are, to some degree, conscious of what they are perceiving in perceiving those features (italics mine).
Elsewhere in the same article, Lurz writes:
A cat who sees movement in the bushes, for instance, but who is not conscious of what she is perceiving - perhaps, as a result of being momentarily distracted by a loud noise - is less likely to catch the mouse in the bushes than the cat who sees the movement and is conscious of what she is perceiving (Lurz, 2003).
Lurz's wording here suggests that any animal that is capable of paying attention to occurrences in its surroundings and recognising objects would qualify as conscious. This implies that Lurz would regard some insects as conscious.
Attention
Scientists have recently identified attentional mechanisms in insects. Van Swinderen and Greenspan (2003) have reported the discovery of "a physiological signature of object salience" by measuring local field potentials in the brain of the fruit fly Drosophila melanogaster. Although the authors prefer to avoid the word "attention" because of its controversial associations with consciousness (2003, p. 585), they describe some impressive correlations with the brain mechanisms of attention in monkeys and humans: "amplitude increases with salience, salience can be increased either by an unconditioned stimulus or by novelty, selection suppresses the response to simultaneous unattended stimuli, and coherence increases with selective attention" (2003, p. 585, italics mine).
Object recognition
Tests by Gould and Gould (1988) showed that bees could learn to recognise and distinguish human letters, regardless of size, colour, position or font. Giurfa, Eichmann and Menzel (1996) trained foragers to associate symmetrical shapes with food. Asymmetrical shapes were not rewarded. (In another test, asymmetrical shapes were rewarded while symmetrical ones were not.) By the seventh visit, the bees could choose a correct novel stimulus over an incorrect one.
As well as being able to recognise objects, one species of insect - the paper wasp Polistes fuscatus - can recognise other individuals. Paper wasps use chemical cues to distinguish between friends and intruders. However, they also have distinctive yellow markings on their faces and abdomens. The wasps live within a rigid hierarchy where every individual has a pecking order, suggesting that colony members can tell one wasp from another. Elizabeth Tibbetts, a doctoral candidate and behavioral ecologist at Cornell University, speculated that wasps used visual cues to identify an individual's rank, because of the variety of markings on their faces and bodies. But after studying the variations in color and marking patterns, such as stripe positions and stripe thickness, she could find no apparent correlations between the wasps' markings and their health or social rank (Indiana University, 2003).
Tibbetts explored her hypothesis by inducing changes in wasps' behaviour towards their nestmates by painting the faces and abdomens of some individuals, so as to alter their markings. The altered individuals were the target of hostile attacks for up to two hours, but were eventually accepted on the basis of their chemical cues which identified them as kin (Friedlander, 2002; Abrams, 2003). Had they been taken for outsiders, they would have been attacked much more aggressively. Tibbetts proposes that wasps have two separate identification systems: a chemical system which determines whether a wasp belongs or not, and visual cues to decide the individual identity and rank of wasps whose smell marks them as kin.
"Basically the wasp sees a painted wasp with altered markings and thinks, 'She smells right, so she must be a nest mate, but if I don't recognize her, is she a threat to my rank?' So the wasp is aggressive," said Tibbetts. "Whenever the nest mate then sees the altered wasp, she will know who it is and think, 'No need to worry, it is just Susie over there laying an egg.' Hence individual recognition" (quoted in Friedlander, 2002).
The methodology proposed here would not impress Carruthers, who has consistently upheld the view that phenomenal consciousness is the peculiar preserve of human beings - though he allows that chimpanzees may also have it. Carruthers rejects the ability to give "accurate report" as a way to identify phenomenal consciousness in animals. I propose to discuss his views under two headings: first, do his arguments against animal phenomenality work, and second, is it possible to prove his views wrong?
Carruthers' argument against the possibility of phenomenal consciousness in animals
The essence of Carruthers' case against phenomenal consciousness in non-human animals can be summarised as follows:
(i) phenomenal consciousness requires the ability of to think about one's own thoughts;
(ii) the ability to conceptualise one's thoughts requires one to possess a theory of mind and attribute mental states to other individuals;
(iii) there is little evidence that non-human animals (except possibly chimpanzees) possess this ability; so
(iv) there is no reason to ascribe phenomenal consciousness to most other animals.
The first premise expresses the HOT theory of phenomenal consciousness which both Carruthers and Rosenthal endorse. There is some evidence for a rudimentary theory of mind in chimpanzees, dogs and elephants (Horowitz, 2002; Nissani, 2004), but let us grant Carruthers' third premise for argument's sake. The critical step in his argument is the second, which has been critiqued by Allen (2003).
The interesting thing about Carruthers' theory of the origin of phenomenal consciousness is that it is a by-product that was not directly selected for: it arose as a consequence of animals acquiring a "mind-reading faculty" that enabled them to interpret other animals' behaviour and attribute mental states to them. According to Carruthers (2000), this mind-reading faculty may have arisen in response to the need to interpret early hominid attempts at speech. Since the human senses of touch, taste, smell, hearing and sight all have a phenomenal feel to them, Carruthers needs to explain why his mind-reading faculty needed to have access to the full range of perceptual representations:
It would have needed to have access to auditory input in order to play a role in generating interpretations of heard speech, and it would have needed to have access to visual input in order to represent and interpret people's movements and gestures, as well as to generate representations of the form, "A sees that P" or "A sees that [demonstrated object/event]" (Carruthers, 2000, p. 231).
Allen (2003, p. 12) finds this argument unconvincing, as it only explains sight and hearing:
The way others look to us, sound to us, and the sensations they produce when they touch us are all possible targets of interpretation. In contrast, there seems little to innterpret regarding others' mental states in the way they smell and taste to us, nor in the way our stomachs feel when they have not eaten for a while. I conclude that the mind-reading faculty has no need for access to smell and taste, nor to many somatosensory sensations, for interpretative purposes.
In any case, Carruthers' claim that our "mind-reading faculty" has access to the full range of perceptual systems is a mistaken one: the vomeronasal system, which responds to pheromones and affects human behaviour, is devoid of phenomenality (Allen, 2003, p. 13).
Conclusion: Carruthers' argument fails to explain the range of our phenomenal consciousness and is unsuccessful in undermining the case for phenomenal consciousness in non-human animals.
Can there be a proof of phenomenal consciousness in animals?
According to Carruthers, most human behaviour can be explained in terms of first-order states which we share with animals. Only those behaviours which require explanation in terms of higher-order states can be described as phenomenally conscious. In particular, "phenomenal consciousness is implicated whenever we draw a distinction between the way things are and the way they seem or appear" (Carruthers, 2004).
Recent experiments with binocular rivalry have demonstrated that the humans and other animals make identical reports about what they see when conflicting data is presented to their left and right two visual fields:
If two different stimuli - e.g. horizontal and vertical stripes - are presented to each of one's eyes, one does not see a blend, but rather first horizontal stripes that fill the whole visual field and then vertical stripes, that fill the whole field. Logothetis and his colleagues... trained monkeys to pull different levers for different patterns. They then presented different patterns to the monkeys' two eyes, and observed that with monkeys as with people, the monkeys switched back and forth between the two levers even though the sensory input remained the same (Block, 2003, italics mine).
The most obvious way to explain these results is to say that human and monkey brains handle the conflict of data in the same way, and that humans and monkeys experience the same inconstancy in their conscious perceptions. Carruthers could, however, reply that there is no need to postulate higher-order states here: the monkeys simply have fluctuating first-order perceptions, which they have been conditioned to respond to by pulling a lever.
This suggests one way of testing for phenomenal consciousness in animals: any animals that can learn to correct their perceptual errors are phenomenally conscious (Allen, 2002). On this point, the only findings that I have been able to uncover are negative:
The possibility of differentiating between the phenomenal field and objective, "meaningful" images evidently is a property only of human consciousness; owing to it, man is liberated from the slavery of sensory impressions when they are distorted by incidental conditions of perception. In this connection experiments with monkeys fitted with glasses inverting the retinal image are interesting; it developed that as distinct from man, in the monkeys this completely disrupted their behavior, and they entered a long period of inactivity (Leontev, 1978).
Why were the monkeys unable to adjust to their new view of the world? I would suggest that Carruthers' (2004) distinction between the way things are and the way they seem can only be drawn by those able to formulate the concepts of appearance verus reality. These concepts require abstract language, which monkeys (and some human beings) lack. Since positive proof of consciousness requires this distinction, we are forced to the following pessimistic conclusion:
Conclusion: Carruthers' claim that non-human animals are not phenomenally conscious remains, for the time being, consistent with the experimental evidence.
Panksepp (1998, 2001, 2003f) and Liotti and Panksepp (2003) have proposed that we possess two distinct kinds of consciousness: cognitive consciousness, which includes perceptions, thoughts and higher-level thoughts about thoughts and requires a cortex, and affective consciousness, which relates to our feelings and arises within the brain's limbic system.
Is there a more primitive form of consciousness in the brainstem, independent of the cerebral cortex?
Panksepp (1998, 2001, 2003f) has proposed that we possess two distinct kinds of consciousness: cognitive consciousness, which includes perceptions, thoughts and higher-level thoughts about thoughts and requires a cortex, and affective consciousness, which relates to our feelings and arises within the brain's limbic system. Of course, these two kinds of awareness interact continually, but according to Panksepp, the latter is the more ancient, and it is controlled below the level of the cortex, in the brainstem. Panksepp has suggested (1998, p. 314) that this affective consciousness first arose in a region of the mid-brain, known as the peri-acqueductal gray (PAG).
If this alternative view is correct, even animals with a primitive cerebral cortex - or none at all - may have primitive feelings which are consciously experienced (Panksepp 1998, 2001, 2003f; Denton et al. 1999; Parsons et al., 2000; Parsons et al., 2001; Liotti et al. 2001; Cabanac, 2002, 2004; Liotti and Panksepp, 2003). According to this account, affective consciousness is phylogenetically very ancient: it is certainly shared by all mammals and possibly reptiles and birds as well. Panksepp proposes that some human beings in a permanent vegetative state, as well as some anencephalic infants, may also possess it (personal email, 15 June 2004).
The following table summarises the main arguments adduced by Panksepp (2003) for a real distinction between two forms of consciousness in the brain:
Table: Contrasts between Affective and Cognitive Consciousness
| Affective awareness | Cognitive consciousness |
| Intrinsically valenced - characterised by positive or negative feelings. | Not valenced. |
| Largely subcortical. Emotional responses and many basic affective tendencies survive many forms of cortical brain damage that severely impair cognitions. | Cognitions are largely cortical and are impaired by cortical brain damage. |
| Affects are more powerful and easier to induce in the young. Children are very "emotionally alive". | Sophisticated cognitive activities prevail among adults. |
| Feelings are easily activated by direct brain stimulation. Affects may be generated more by analog types of neurohumoral processes. | Conscious cognitions are difficult to activate by direct brain stimulation. Cognitions may be generated more by digital-type computations. |
| Emotions generate spontaneous, trans-cultural, facial and bodily expressions as well as prosodic vocal changes. | Cognitions do not generate this kind of behaviour. |
| In general, our right cerebral hemisphere tends to be more emotionally deep and perhaps negativistic (or realistic). When the more emotionally introspective right hemisphere is damaged, the linguistically proficient left hemisphere commonly carries on as if nothing very serious has transpired and chooses to repress negative emotions. At its most extreme, right hemisphere damaged patients often deny that their left side is even paralysed when it clearly is, from an objective standpoint. | The left hemisphere tends to be more cognitively skilled and positively valenced in comparison. Thus left hemisphere-damaged individuals are very much aware of their post-stroke plight. |
Of the contrasts listed here between emotion and cognition, those of special significance are the fact that the two forms of consciousness are controlled by separate regions of the brain and the fact that one can be badly damaged without having much effect on the other. These facts indicate that the distinction between the two forms of consciousness is real rather than merely conceptual.
However, the distinction between these two forms of consciousness should not be exaggerated: in normal individuals, they are highly integrated. Recent studies (Allman et al., 2001) suggesting that the anterior cingulate cortex of the brain has an important role both in regulating the emotions and in rational problem-solving, illustrate this point.
I would also like to observe that the terminology used is philosophically misleading, as it suggests that affective consciousness is completely independent of cognition. It was argued in chapter three that emotions could only be attributed to organisms that were capable of having beliefs. If this is the case, then affective consciousness must also contain a cognitive element - even if the sensory processing involved is very low-level.
The distinction between cognitive and emotional processes within the brain is generally accepted by neuroscientists (see LeDoux, 1998, p. 161). However, the notion that there are two forms of consciousness - in the brain is much more contentious. The key point at issue is the role of affect (phenomenally conscious feeling) in emotions. LeDoux, a notable adversary of the "affective neuroscience" perspective approach championed by Panksepp, questions its relevance on the grounds that conscious feeling is not an essential feature of emotion - the icing on the cake is how he describes it (1998, p. 302) - and is likely to have emerged only recently in evolutionary history.
There are two ways in which Panksepp and his colleagues could buttress their claim that animal consciousness originally arose in the brainstem. First, brain imaging studies of human patients experiencing powerful emotions should reveal an activiation of regions in the brain stem. Second, affective consciousness should remain intact in human beings or animals lacking a cerebral cortex.
It is generally agreed that human beings and animals that lack a cerebral cortex cannot report their feelings - in other words, they do not possess primary consciousness. Neuroscientists choosing to use the second method of validating affective consciousness are therefore bound to propose alternative diagnostic criteria for conscious. I will discuss these issues below.
Conclusion: There is good prima facie evidence for the existence of two forms of consciousness in humans and other mammals. One form of consciousness is more "affective" and is associated with feelings and crude, low-level processing of sensory inputs; the other is more "cognitive", and is linked with more detailed, fine-grained processing of sensory inputs.
If it were possible to nominate certain kinds of behaviour other than accurate reporting that reliably indicated the presence of phenomenal consciousness, then primary consciousness would no longer be required to justify the ascription of phenomenal consciousness to animals. Here, I examine three classes of indicators that have been proposed as alternatives: Panksepp's criteria for affective consciousness; behavioural indicators of pain; and hedonic behaviour in animals.
Can affective consciousness occur in individuals lacking a cerebral cortex?
Brain imaging studies have failed to establish that consciousness can occur in the absence of a cerebral cortex. However, the identification of consciousness in individuals lacking a cerebral cortex would certainly clinch the case. I propose to examine the evidence for consciousness in human children suffering from anencephaly and from animals.
Evidence from anencephalic children
Merker (2003) defines the condition of hydranencephaly as follows:
Basically hydranencephaly indicates that a child is missing much or most of their cerebral hemispheres, that is, the two masses of folded brain tissue (cortex) that surround the brain stem. Literally "anencephaly" means "without brain", but this is technically incorrect as a term for the cases to which it is applied, which almost invariably have a brain stem (Merker, 2003).
Most neurologists would agree that "[i]nfants with anencephaly, lacking functioning cerebral cortex, are permanently unconscious" (Medical Task Force on Anencephaly, 1990). However, Panksepp and "quite a few other neurologists" consider that the behaviours exhibited by anencephalic infants and decorticate human beings "have a high probability of reflecting affective experience" (personal email, 15 June 2004).
As evidence, Panksepp cites an article by Shewmon (1999) describing three cases of children born with hydranencephaly (a rare condition in which the brain's cerebral hemispheres are absent and replaced by sacs filled with cerebrospinal fluid) and another child born with a similar condition. "Each of these children defied a prognosis of permanent vegetative state, rendered with absolute certainty by multiple physicians, including pediatric neurologists and neurosurgeons" (Shewmon, 1999, p. 370). Despite the total or near-total absence of a cerebral cortex in these children, they proved to be capable of a variety of forms of discriminative awareness, including "distinguishing familiar from unfamiliar people and environments, social interaction, functional vision, orienting, musical preferences, appropriate affective responses, and associative learning" (Shewmon, 1999, p. 364). The two children with rudimentary limbic structures were more affective and sociable, and possessed more motor function (Shewmon, 1999, p. 371).
The following account by Barb Aleman (2003) on behalf of the International Hydranencephaly Support Group, of her hydrancephalic deceased daughter Kayda's behaviour gives examples of some prima facie conscious affective behaviours where more research needs to be done:
During her last couple of years she would only sleep if she had her husky dog under her left arm and her bunny under her right. If either was missing or not in the "right" arm she would not sleep. I tested this many times, always with the same result.She would only sleep listening to a story not music. Again, we tested it numerous times.
If you put on a book that had more than one tape she would stay awake to listen to the whole book.
If she didn't want a particular toy or stuffed animal you'd given her she'd push or toss it onto the floor (http://hydranencephaly.com/communication.htm).
A recent survey of 81 parents of children with hydranencephaly provides further reason to query the prevailing view among neurologists that these children are not conscious. Although the survey was not scientifically conducted and has not been published in any medical journal, it was consistent with earlier research findings. The following table lists selected results relating to movement, awareness and affective consciousness:
Table: Selected behaviours in a survey of 81 children with hydranencephaly, which constitute prima facie evidence of consciousness
| Survey Question | Response by percentage (absolute figures in brackets) |
| Can your child move his/her arms? | Yes: 60.49% (49) No: 2.46% (2) A little: 32.1% (26) Used to: 0 |
| Can your child move his/her legs? | Yes: 61.72% (50) No: 3.7% (3) A little: 28.39 (23) Used to: 0 |
| Can your child give hugs or kisses? | Yes: 19.73% (16) No: 66.66% (54) Sometimes: 11.11% (9) |
| Can your child cry? | Yes: 91.35% (74) No: 6.17% (5) |
| What is your child's general mood? | Happy: 56.79% (46) Irritable: 6.17% (5) Fussy: 13.58% (11) Quiet: 18.5% (15) Can't tell: 2.46% (2) |
| What was your child's mood as a baby? | Happy: 22% (18) Irritable: 46.91% (38) Fussy: 11.11% (9) Quiet: 14.8% (12) Couldn't tell: 0 |
| Is your child aware of his/her surroundings? | Yes: 74% (60) No: 2.46% (2) Sometimes: 14.8% (12) Used to be: 0 Can't tell: 6.17% (5) |
| Is your child aware of objects? | Yes: 40.74% (33) No: 17.28% (14) Sometimes: 38.27% (31) Used to be: 0 |
| Does your child have a favorite toy? | Yes: 48.14% (39) No: 46.91% (38) |
| Does your child have a security item? | Yes: 29.6% (24) No: 62.96% (51) |
| Can your child hear? | Yes: 92.59% (75) No: 1.23% (1) |
| Can your child make sounds? | Yes: 96.29% (78) |
| Does your child use any words meaningfully? | Yes: 9.87% (8) No: 83.95% (68) |
| Will your child echo you? | Yes: 23.45% (19) No: 65.43% (53) |
| Can your child see? | Yes: 27% (22) No: 16% (13) Sometimes: 12.34% (10) A little: 20.98% (17) Not sure: 19.73% (16) |
If we adhere to the methodology proposed for this thesis, then the appropriate way of assessing whether these children are indeed phenomenally conscious is to look for features of their behaviour that are readily explained by a "first-person" account, but can only accounted for with difficulty by a "third-person" account. For a scientist proposing a "third-person" account of these children's behaviour, the children's emotional responses (smiling, giggling and vocalisations) to familiar people and favourite objects, likings for favourite songs and dislikes for certain kinds of music, are certainly startling, unexpected behaviours that constitute a good prima facie case for affective consciousness without a functioning cerebral cortex.
However, it should be noted that some of the behaviours cited can be explained by non-conscious mechanisms. We have already concluded that associative learning does not require mental states, and Rose has suggested that the emotional responses to music and to familiar faces or voices emotional conditioning (personal email, 22 July 2004).
Conclusion: There is a good prima facie case that children with hydranencephaly are phenomenally conscious. However, the emotional behaviours displayed by these children are not conclusive indicators of phenomenal conscious, as some of these behaviours may be non-conscious. More research is needed to determine which behaviours are most likely to manifest conscious feelings.
It should also be noted that a list of defining criteria for "affective consciousness" has yet to be developed. I would like to propose the following indicators as most promising indicators for identifying phenomenal consciousness: musical preferences and singular preferences for individuals and objects.
Affective states in decorticate mammals
Decorticate mammals may behave in a way that is difficult to distinguish from their "normal" counterparts, suggesting that conscious feelings are also present in these animals. To quote Panksepp (2004):
In the '70s I did the following class experiment with 16 students in an advanced behavioral neuroscience class: Each student received two adult rats, one which had had all neocortex removed at day 3 of birth, and the other had sham surgery. Each student had a lab session to study their rat in whatever way they wished, and then to decide who was missing 25% of their brain (the conscious "thinking cap" so to speak). Surprisingly, 12 of 16 selected the decorticate as being the normal animal. Why this mistake that was statistically significant? Largely, because the decorticates were more emotionally active it seems (personal email, 24 June 2004).
On the other hand, Shewmon (1999) has proposed that vertical plasticity in the brains of juvenile rats can account for their recovery of function. On this interpretation, the program controlling neural development is more flexible in juvenile animals, and adapts to the loss of the cerebral cortex by enhancing the capacities of lower-level structures in the brain, to partially compensate for the loss. This would explain why "adult cats bilaterally hemispherectomized [subjected to a surgical removal of both cerebral hemispheres - V.T.] as kittens behave nearly indistinguishably from normal, in marked contrast to cats hemispherectomized as adults (which are severely disabled)" (1999, p. 372).
If Shewmon is right, subcortical regions in the brains of decerebrated juvenile animals may acquire neural features that are normally found only in the cerebral cortex - e.g. a high degree of intra- and inter-connectivity. In effect, these animals' brains become "corticised". The neural features that normally distinguish the cerebral cortex would still be required for consciousness.
The identification of affective consciousness in animals whose cerebral hemispheres have been removed as adults would certainly clinch the case for an affective consciousness that is independent of the cerebral cortex. The evidence to date is not promising:
[I]t has been demonstrated that removing the cerebral cortex from a cat or a rat ... leaves intact the ability to generate motivated behavior. The animal still searches for food, eats to maintain body weight, shivers when cold, fights or escapes when attacked, and so on. These behaviors appear awkward and clumsy when compared to controls and are often poorly adjusted to circumstances (Prescott et al., 1999).
The behaviour of these unfortunate animals certainly qualifies as emotional, but there is no reason to consider it phenomenally conscious. However, the case for affective consciousness would be much strengthened if it could be shown that these animals exhibited singular preferences such as are found in children with hydranencephaly, as these are unexpected phenomena on a "third person" account.
Conclusion: The apparently conscious behaviour shown by mammals whose cerebral hemispheres have been removed while very young, is compatible with the hypothesis that subcortical regions of their brains modified their development to compensate for the loss (vertical plasticity). This in no way weakens the generally accepted theory that certain neural features of the cerebral cortex (e.g. high intra- and inter-connectivity) are required for phenomenal consciousness.
Note: in this section, 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).
In this section, I address a paradox: the typical behavioural reactions that manifest 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 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.
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).
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.
Mindless 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: Behaviours which do NOT constitute 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 (2004) 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. |
Conclusion A stress response in an organism does not constitute a sufficient warrant for ascribing conscious feelings to it.
Conclusion Nociception per se does not constitute a sufficient warrant for ascribing conscious feelings to an animal.
Conclusion The presence of opiate receptors in an animal's brainstem does not constitute a sufficient warrant for ascribing conscious pain to it.
Conclusion An animal's ability to undergo flavour aversion learning does not constitute a sufficient warrant for ascribing conscious feelings to it.
Mindful behaviours that do not define the occurrence of pain
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: Behaviours which constitute evidence for the existence of non-conscious emotions in animals, but NOT phenomenally 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. |
Conclusion 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 An animal's ability to undergo operant conditioning does not constitute a sufficient warrant for ascribing conscious feelings to it.
Table: Behaviours which MAY constitute evidence for the existence of phenomenally conscious pain in animals
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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. |
Conclusion Absence of pain-guarding in certain kinds of animals is strong evidence that they are incapable of feeling conscious pain.
Conclusion Pain-guarding of a structurally sound limb is good prima facie evidence of conscious pain.
Conclusion An injured animal's preference for a bitter solution containing analgesics over a sweet solution constitutes suggestive but not conclusive evidence that it is consciously experiencing 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 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.
Models of animal pain
For a discussion of current animal models for various kinds of human pain, see Eaton, (2003), Schwei et al. (1999) and Honore et al. (2000). The criteria for two common kinds of 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 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 are sure indicators of phenomenal consciousness. 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 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 It is likely that only mammals and birds experience pain.
CASE STUDY: Pain in Fish?
Because the brain parts of vertebrate non-mammals are homologous at the gross level 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.
Pain-guarding in fish?
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.
Table: Behaviours which do NOT constitute evidence for the existence of phenomenally conscious feelings of pleasure in animals
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Kind of Behaviour: Self-stimulation
Description: A laboratory animal with electrodes in its brain has to do something in order to prolong the electrical arousal of its brain's SEEKING system. Alternatively, the animal may have to perform a complicated action (e.g. press a lever) in order to prolong the arousal of its brain's SEEKING system.
Found in which organisms? Self-stimulation has been identified in a wide variety of animals, including fish, crustaceans, and even snails (Panksepp, peronal communication, 30 May 2004).
More complex behaviours have been recorded in rats, who will self-stimulate themselves to death if not prevented from doing so.
Alternative, "third-person" explanation: Maybe the animal is 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). |
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Kind of Behaviour: Intoxication
Description:
Many animals seek out intoxicating substances that induce a narcotic state.
Found in which organisms? Beetles, honeybees, crayfish, spiders and fruit flies, as well as mammals.
Examples amenable to a Third-Person explanation: Japanese beetles, for instance, display a preference for the leaves of the geranium plant, and can "pass out" for 12 to 18 hours after feeding on them (Riggs, 2000).
Honeybees will readily consume 20% ethanol solutions, and even stronger solutions of 95% ethanol (so long as the antennae do not make contact with the solution). However, there is no evidence to date of addiction or tolerance (Abramson et al., 2000).
Crayfish which were placed in an aquarium with two kinds of visual environments - a floor and walls with stripes or a floor and walls without stripes - and which received intra-muscular injections of cocaine and/or amphetamines, displayed a conditioned place preference for the environment with similar visual stimuli to the one where they received the injection (Panksepp and Huber, 2004).
Explanation in Third-Person Terminology: Intoxicating substances may be sought because of their chemical resemblance to biologically useful substances: the brain's natural opiates (endorphins).
The pathways oriented to endorphins, sometimes called pleasure centers originated in small organisms such as insects, which rely on the neurological system to help them find familiar sources of food. |
Conclusion: An animal's tendency to engage in self-stimulation does not constitute a sufficient warrant for ascribing conscious feelings of pleasure to it.
Conclusion: An animal's tendency to seek out intoxicating substances that induce a narcotic state does not constitute a sufficient warrant for ascribing conscious feelings of pleasure to it.
Table: Behaviours which MAY constitute evidence for the existence of phenomenally conscious feelings in animals
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Kind of Behaviour: Drug addiction
Description:
Many animals seek out intoxicating substances that induce a narcotic state.
Found in which organisms? Beetles, honeybees, crayfish, spiders and fruit flies, as well as mammals.
Examples amenable to a Third-Person explanation: Japanese beetles, for instance, display a preference for the leaves of the geranium plant, and can "pass out" for 12 to 18 hours after feeding on them (Riggs, 2000).
Honeybees will readily consume 20% ethanol solutions, and even stronger solutions of 95% ethanol (so long as the antennae do not make contact with the solution). However, there is no evidence to date of addiction or tolerance (Abramson et al., 2000).
Crayfish which were placed in an aquarium with two kinds of visual environments - a floor and walls with stripes or a floor and walls without stripes - and which received intra-muscular injections of cocaine and/or amphetamines, displayed a conditioned place preference for the environment with similar visual stimuli to the one where they received the injection (Panksepp and Huber, 2004).
Explanation in Third-Person Terminology: Intoxicating substances may be sought because of their chemical resemblance to biologically useful substances: the brain's natural opiates (endorphins).
The pathways oriented to endorphins, sometimes called pleasure centers originated in small organisms such as insects, which rely on the neurological system to help them find familiar sources of food.
Description + Examples Better Construed as First-person Phenomema: In his book, "Intoxication: Life in Pursuit of Artificial Paradise," Ronald K. Siegel, a UCLA psychopharmacologist, describes how many animals will eat fermented fruits, vegetables, plants and other substances that have mind-altering qualities. Siegel noted that the mongoose eats a plant that has psychedelic qualities when grieving over the loss of a mate or when its burrows are destroyed by a monsoon; elephants become intoxicated from eating fermented marula fruit when they are stressed from the thinning of the herd or competition from other animals; and water buffalo have been seen eating poppies. (Source: Researchers Look For Addiction Clues. 3/26/1998. Web address: http://www.jointogether.org/sa/news/reader/0%2C1030%2C24946%2C00.html)
Grounds for preferring a First-person Interpretation: These animals are seeking out intoxicating substances to induce mind-altering euphoria, when they are stressed or sad. The behaviour is likely to be subjective, as it is specific to occasions that would normally induce sadness or anxiety in sentient beings. |
Conclusion: The occurrence of mood-specific drug-seeking behaviour in certain mammals is prima facie evidence that they are capable of feeling conscious pain.
Satiety in animals
The phenomenon of satiety is an interesting one: thirsty human beings who assuage their thirst feel satiated long before their bodies have had time to absorb the water they have imbibed. Denton (1996, 1999) suggests that this phenomenon represents a primal form of consciousness, and speculates that it would have been biologically useful for animals to experience this "full" feeling long before the water they drank had been absorbed into their bodies, so that they could depart from a waterhole as soon as possible, thereby avoiding predators.
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 may turn out to be explicable in terms of underlying chemical processes.
Conclusion: The phenomenon of satiety need not indicate conscious pleasure in animals.
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. Reptiles and mammals - but not amphibians (Cabanac, 2003) are willing to make trade-offs whereby they expose themselves for a short time to an aversive stimulus in order to procure some attractive stimulus. Lizards will 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) which they do not need. Additionally, they appear to weigh up the relative costs and benefits of their choices: when it gets too cold, the lizards stay in their warm enclosure and eat the nearby food, but if the experimenters improve the quality of the food in the cold corner, the lizards prove willing to tolerate lower temperatures (Cabanac, 2003). Cabanac (2003) concludes that the lizards appear to be making decisions based on palatability, a form of pleasure.
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).
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".
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.
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. Cabanac himself employs such terminology: the lizards face "conflict between two motivations: a thermoregulatory drive (to avoid cold) and an attraction to palatable bait" (2003).
Conclusion: The willingness of certain kinds of animals to engage in hedonic trade-offs of pain for delayed pleasure constitutes prima facie evidence for conscious feelings on their part.
Rational and irrational pursuit in animals
Researchers working with rats (Berridge, 2001, 2003) have found ways of identifying and isolating both conscious and unconscious features of a rat's liking for sugar, in experiments where the rat has to work (press a lever) in order to obtain a reward - a sugar solution which is infused directly into the rat's mouth. Experienced utility, or the rat's actual liking for an outcome, is assessed by measuring its positive facial reactions (e.g. frequency of tongue protrusions) as it tastes the sugar solution. Remembered utility, or the rat's memory of its liking for an outcome in the past, is measured by its willingness to persist in working for the sugar reward, even under extinction conditions, when the reward no longer comes at all. Predicted utility, or the rat's expected liking for the outcome in the future, is defined as the rat's baseline level of lever pressing when the reward is absent. Finally, the rat's decision utility, or its manifest choice of the outcome, can be defined as as the amount of work it is willing to do in order to obtain the reward. If a rat's dopamine levels are activated by a micro-injection of amphetamine into a region of its brain (the nucleus acumbens), neither the rat's "liking" for the sugar reward (as measured by its positive reaction to the taste of sugar) nor its predicted utility (as measured by its willingness to press the lever when the sugar reward is absent) shows an increase, but when the cue (sugar) is presented to the rat, it engages in a frenzy of pursuit for the reward, which Berridge characterises as irrational pursuit. Berridge explains this not by saying that the dopamine makes the sugar seem more rewarding but by the hypothesis that dopamine increases the sugar's incentive salience.
Berridge's work suggests that wanting and liking are separable psychological processes, and indicates a scientific way of distinguishing between rational and irrational desires in animals. Berridge (2001) defines an animal's choice as rational if its decision utility matches its predicted utility, and its choice maximizes both. That is, an animal chooses rationally if it consistently chooses what it expects to like, even if its expectations happen to be wrong:
[T]he 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 (Berridge, 2001).
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. An animal under the influence of drugs may sometimes choose an outcome whose eventual hedonic value does not justify its choice:
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.
Berridge (2001, 2003) presents evidence from human studies that irrational desires need not be conscious: humans can be influenced to like or dislike something simply by subliminal exposure to stimuli which they report being unaware of.
Conclusion The phenomenon of rational pursuit in animals, which can be mathematically described in terms of four underlying kinds of utility, is suggestive but not conclusive evidence of phenomenally conscious choice in their part.
The role of the brain in phenomenal consciousness: what neurologists are still not certain about
I would like to begin my review of the literature by citing the response of one neuroscientist, Jaak Panksepp, to an email query of mine: "Is there currently a 'consensus' view among neurologists as to the minimum requirements for consciousness?" Panksepp's forthright reply was: "No there is not" (personal email, 15 June 2004).
The following is an overview of the current controversy among neurologists regarding consciousness:
Does consciousness require a high degree of neural connectivity?
The view that phenomenal consciousness is made possible by the high degree of connectivity between the brain's neurons, is a common but by no means universal one. On this view, consciousness is a property not of individual neurons but only of a very large collection of interacting neurons. Koch and Crick question this assumption:
An alternative hypothesis is that there are special sets of "consciousness" neurons distributed throughout cortex and associated systems. Such neurons represent the ultimate neuronal correlate of consciousness, in the sense that the relevant activity of an appropriate subset of them is both necessary and sufficient to give rise to an appropriate conscious experience or percept (Koch and Crick, 2001).If consciousness does not require a high degree of inter-connectivity and can reside in small sets of neurons, then the argument that it can only reside in the highly inter-connected regions of the cerebral cortex is undermined. It might then be the case that animals with a very primitive cortex - or none at all - are phenomenally conscious.
On the other hand, scientists who question the view that connectivity is what makes consciousness possible owe us an alternative explanation of recent studies (Laureys et al., 2002; Baars, 2003) showing that patients in a persistent vegetative state, none of whom were suffering from brainstem damage that was known to cause a loss of consciousness, displayed a marked reduction in connectivity between different regions of their cortex. Moreover, recovery in PVS patients is correlated with a return of function of the associative cortical areas (Rose, personal email, 22 July 2004). As far as I am aware, no alternative model has been put forward which would account for these phenomena.
Conclusion There is good prima facie evidence that primary consciousness requires a high degree of neural inter-connectivity.
What is the minimum number of neurons required to generate phenomenal consciousness in an animal's brain?
Edelman and Tononi (1999) list sufficient (nonsensory) cortical mass as one of the criteria required to support primary consciousness in animals (see Rose, 2002, p. 24). Koch (2003) is one prominent dissenter from this majority view:
Why be a cortical chauvinist? Do we really know that the cerebral cortex and its satellites are necessary for consciousness? Why not squids? Or bees? Endowed with one million neurons, bees can perform complicated actions, including amazing feats of visual pattern matching. For all I know, a couple of thousand neurons and their associated machinery may be sufficient to see, to smell, to feel pain and to enjoy life! Maybe even fruitflies are conscious, to a very limited extent. Today we just don't know (Koch, 2003, p 320).
As far as I know, Koch is the only neuroscientist to have suggested that insects may possess primary or phenomenal consciousness. and the view of David Edelman, that "it is not likely that the interaction of a couple of thousand, or even a million neurons in, say a honeybee, would yield something we would call consciousness" (personal email, 19 July 2004), is a much more representative one.
Conclusion: The minimum neural requirements for phenomenal consciousness remain unknown.
Do brain imaging studies reveal an affective consciousness that is independent of the cerebral cortex?
Is the cerebellum conscious?
One region of the hind-brain which has recently attracted a great deal of scientific attention is the cerebellum, a phylogenetically ancient structure which is found in all vertebrates. Parsons et al. (2000, 2001) cite recent brain imaging studies indicating that the cerebellum, long considered strictly a motor control structure, plays and important role in sensation, cognition, language processing, affect, thirst and hunger, even in the absence of motor behaviour on the subject's part:
Neuroimaging and neurological studies ... suggest cerebellar involvement in the generation of words according to a semantic rule, timing of events, solving perceptual and spatial reasoning problems, mental rotation, visual information processing, cutaneous and tactile discrimination, kinesthetic sensation, and working memory, among other processes... It has been proposed that the lateral cerebellum may be activated during several motor, perceptual, and cognitive processes specifically because of the requirement to monitor and adjust the acquisition of sensory data... Furthermore, there are reports suggesting the involvement of posterior vermal cerebellum in affect (Parsons et al., 2000, p. 2332, italics mine).
Curiously, the size of an individual's cerebellum has also been shown to correlate well with his or her IQ, which is equal to or even higher than any other correlation between IQ and the brain. In rats, the volume of the cerebellum's outer molecular layer correlates with curiosity (Skoyles, 1999).
Neuroimaging studies show that the cerebellum also plays a vital role in air hunger, thirst and hunger for food - all of which stimulate the cerebellum in a similar manner (Parsons et al., 2001). The cerebellum has reciprocal ancient connections to the hypothalamus, a structure important in vegetative functions. The authors suggest four possible roles for the cerebellum in air hunger - it may (i) subserve implicit intentions to breathe, (ii) provide internal models to predict the consequences of inhaling carbon dioxide, (iii) modulate emotional responses, or (iv) monitor sensory data. In a related article, Parsons et al. discuss the role of the cerebellum in thirst and speculate that "cerebellar involvement in thirst may be related to the intention to drink, inextricably interwoven in the subjective state of thirst, together with a conscious state oriented toward satiation of a desire" (2000, p. 2334), but acknowledge that this is merely a hypothesis, and that more work needs to be done.
Additionally, lesions of the cerebellum in monkeys appear to affect their emotional dispositions, making them more docile (Parsons et al., 2000).
These results are highly suggestive. For the time being, all we can say is that the cerebellum plays a causal role in primal emotions and some cognitive tasks. However, the studies do not show whether activity in the cerebellum is an enabling factor, a modulating factor or part-and-parcel of the experiences themselves.
Although the cerebellum has a connection with higher cognitive functions, the most likely reason for this connection is that it is linked to higher association areas of the cerebral cortex, particularly the prefrontal cortex. Generally, the role of the cerebellum appears to be one of tracking inputs used by a wide range of processes, performed subcortically and cortically (Skoyles, 1999).
As we noted earlier, the fact that ablation of the cerebellum in animals destroys their motor co-ordination but leaves their sensations intact, constitutes one powerful argument that this region plays a minimal role in consciousness as such (Tononi, 2004; Panksepp, 1998, p. 314).
Although the cerebellum contains a large number of neurons and possesses high internal connectivity, the connectivity does not apply across disparate regions: "Individual patches of cerebellar cortex tend to be activated independently of one another, with little interaction between distant patches" (Tononi, 2004).
Conclusion: While there is increasing evidence that the cerebellum plays a significant role in various forms of conscious activity, its neural features, coupled with data from ablation studies, suggest that it probably could not support consciousness in the cerebral cortex were absent.
The role of the brainstem in affective states and vegetative functions: an overview of results
Summarising the data from animal studies, Liotti and Panksepp (2003) claim that at least seven core emtional systems have been provisionally identified in mammals, and that these emotional operating systems are regulated by subcortical regions of the mammalian brain. These systems were described in the previous chapter.
Liotti et al. (2001) also show that vegetative functions such as hunger for air, thirst, and hunger for food all activate similar regions of the brain: "There is evidence of commonality in structures involving these primal emotions" (2001, p. 2039). They conclude (2001, p. 2040) that "primary consciousness ... involves essential elements in the rhombencephalon [hind-brain], mesencephalon [mid-brain], hypothalamus, thalamus [upper brain stem], amygdala", and other areas, including the anterior cingulate, which borders the cerebral cortex.
Three comments are in order here. First, it is important not to over-state the evidence for conscious processing below the level of the cerebral cortex. A variety of regions of the brain are activated during thirst and air hunger, and some of these are likely to be merely enabling or modulating factors for consciousness. However, they do not show that consciousness can occur in the absence of a cortex.
Second, the fact that conscious feelings are controlled by core systems in the brainstem does not imply that these subcortical systems are sufficient for consciousness - a point acknowledged by Liotti and Panksepp (2003).
Third, it is the anterior cingulate cortex whose activity appears to correlate most consistently with so-called "primal" forms of consciousness such as air hunger and thirst (Liotti et al., 2001, Egan et al., 2003, Liotti and Panksepp, 2003). This region of the brain with a complex layered structure which borders the cerebral cortex:
A meta-analysis of neuroimaging studies involving basic drives (thirst, air hunger, hunger, impeded micturition) shows an overlap of activations in the regions of the dorsal anterior and middle cingulate gyrus (Liotti and Panksepp, 2003).
Conclusion: Conscious feelings and vegetative functions are controlled by core systems below the level of the cortex. The subcortical region whose activity appears to correlate most consistently with so-called "primal" forms of consciousness is the anterior cingulate cortex, a structure in the brain's limbic system.
Is the anterior cingulate complex subcortical?
Liotti and Panksepp (2003) propose the following interpretation of the results to date:
Several lines of evidence suggest that peri-conscious, affective processing of emotion takes place sub-cortically, in areas such as brainstem, hypothalamus and amygdala, while cognitive appraisal of emotions takes place in prefrontal cortex and anterior cingulate cortex (Liotti and Panksepp, 2003).But does the term "peri-conscious" signify phenomenal experience, or some state underlying it? The terminology introduced at this point is unclear.
Liotti and Panksepp suggest that the anterior cingulate cortex serves as an alarm centre, "alerting the organism that immediate conscious action needs to be taken in order to remove the threat" (2003).
The authors seem to share the assumption that because the anterior cingulate cortex is part of the "limbic system" of the brain, it is a subcortical structure that predates the cerebral cortex. However, Allman et al. (2001) have recently challenged the commonly held assumption that the anterior cingulate cortex has a more primitive laminar structure than neocortex and preceded it in evolution:
[W]e propose that the anterior cingulate cortex is a specialization of neocortex rather than a more primitive stage of cortical evolution. The evidence from single neuron recording, electrical stimulation, EEG, PET, fMRI and lesion studies indicate that the anterior cingulate cortex has an important role in emotional self-control as well as focused problem solving, error recognition, and adaptive response to changing conditions (Allman, Hakeem, Erwin, Nimchinsky and Hof, 2001).It should also be pointed out that the anterior cingulate cortex is not found in birds or reptiles.
Conclusion: As the anterior cingulate cortex is unique to mammals, and may in fact be part of the neocortex, the discovery that this structure may support so-called "primal" forms of consciousness, lends no support whatsoever to the case for phenomenal consciousness in birds and reptiles.
Can affective consciousness occur in individuals lacking a cerebral cortex?
Brain imaging studies have failed to establish that consciousness can occur in the absence of a cerebral cortex. However, the identification of consciousness in individuals lacking a cerebral cortex would certainly clinch the case. I propose to examine the evidence for consciousness in human children suffering from hydranencephaly and from decorticate animals.
Evidence from hydranencephalic children
Merker (2003) defines the condition of hydranencephaly as follows:
Basically hydranencephaly indicates that a child is missing much or most of their cerebral hemispheres, that is, the two masses of folded brain tissue (cortex) that surround the brain stem. Literally "anencephaly" means "without brain", but this is technically incorrect as a term for the cases to which it is applied, which almost invariably have a brain stem (Merker, 2003).
Despite a current consensus among neurologists that "[p]ain and suffering are attributes requiring cerebral cortical functioning" (American Academy of Neurology, 1989) and that "[i]nfants with anencephaly, lacking functioning cerebral cortex, are permanently unconscious" (Medical Task Force on Anencephaly, 1990), Panksepp and "quite a few other neurologists" consider that the behaviours exhibited by anencephalic infants and decorticate human beings, "have a high probability of reflecting affective experience" (personal email, 15 June 2004).
As evidence, Panksepp cites an article by Shewmon (1999) describing three cases of children born with hydranencephaly (a rare condition in which the brain's cerebral hemispheres are absent and replaced by sacs filled with cerebrospinal fluid) and another child born with a similar condition. "Each of these children defied a prognosis of permanent vegetative state, rendered with absolute certainty by multiple physicians, including pediatric neurologists and neurosurgeons" (Shewmon, 1999, p. 370). Despite the total or near-total absence of a cerebral cortex in these children, they proved to be capable of a variety of forms of discriminative awareness, including "distinguishing familiar from unfamiliar people and environments, social interaction, functional vision, orienting, musical preferences, appropriate affective responses, and associative learning" (Shewmon, 1999, p. 364). The two children with rudimentary limbic structures were more affective and sociable, and possessed more motor function (Shewmon, 1999, p. 371).
Despite these interesting results, there are two reasons for caution. First, the usefulness of these results in arguing for consciousness without a cerebral cortex is limited by the fact that some children suffering from hydranencephaly still possess residual cerebral cortex:
[M]any children have some of their cerebral hemispheres so can use these and learn to do more than would be expected by this diagnosis. Just as all children are different, all children with hydranencephaly are different as well (Merker, 2003).
The fact that hydranencephaly varies in degree of severity from one individual to another may account in part for some of the abilities displayed.
Second, Shewmon (1999, p. 372) has raised the possibility that vertical plasticity (the ability of subcortical regions of the brain to take over functions that the cortical regions normally handle) may explain these children's emotional behaviour. If this is the case, then it could still be argued that certain neural features that are normally possessed only by the cerebral cortex (e.g. high intra- and inter-connectivity) are required for phenomenal consciousness.
Conclusion: There is a good prima facie case that children with hydranencephaly are phenomenally conscious. However, the emotional behaviours displayed by these children does not conclusively establish that a functioning cerebral cortex is not required for consciousness in normal human beings, as: (i) some of the emotional behaviours may be non-conscious, (ii) hydranencephaly varies considerably in degree of severity from one individual to another, and (iii) vertical plasticity (whereby other regions of their brains become "corticised") may account for some of their emotional behaviour. More research is needed to correlate the emotional capacities of children with hydranencephaly with their degree of cerebral damage, and to determine which behaviours are most likely to manifest conscious feelings.
It should also be noted that a list of defining criteria for "affective consciousness" has yet to be developed. I would like to propose the following indicators as most promising indicators for identifying phenomenal consciousness: musical preferences and singular preferences for individuals and objects.
Affective states in decorticate mammals
Decorticate mammals may behave in a way that is difficult to distinguish from their "normal" counterparts, suggesting that conscious feelings are also present in these animals.
However, Shewmon (1999) has proposed that vertical plasticity in the brains of juvenile rats can account for their recovery of function. On this interpretation, the program controlling neural development is more flexible in juvenile animals, and adapts to the loss of the cerebral cortex by enhancing the capacities of lower-level structures in the brain, to partially compensate for the loss. This would explain why "adult cats bilaterally hemispherectomized [subjected to a surgical removal of both cerebral hemispheres - V.T.] as kittens behave nearly indistinguishably from normal, in marked contrast to cats hemispherectomized as adults (which are severely disabled)" (1999, p. 372).
If Shewmon is right, subcortical regions in the brains of decerebrated juvenile animals may acquire neural features that are normally found only in the cerebral cortex - e.g. a high degree of intra- and inter-connectivity. In effect, these animals' brains become "corticised". The neural features that normally distinguish the cerebral cortex would still be required for consciousness.
The identification of affective consciousness in animals whose cerebral hemispheres have been removed as adults would certainly clinch the case for an affective consciousness that is independent of the cerebral cortex. The evidence to date is not promising:
[I]t has been demonstrated that removing the cerebral cortex from a cat or a rat ... leaves intact the ability to generate motivated behavior. The animal still searches for food, eats to maintain body weight, shivers when cold, fights or escapes when attacked, and so on. These behaviors appear awkward and clumsy when compared to controls and are often poorly adjusted to circumstances (Prescott et al., 1999).
Conclusion: The apparently conscious behaviour shown by mammals whose cerebral hemispheres have been removed while very young, is compatible with the hypothesis that subcortical regions of their brains modified their development to compensate for the loss (vertical plasticity). This in no way weakens the generally accepted theory that certain neural features of the cerebral cortex (e.g. high intra- and inter-connectivity) are required for phenomenal consciousness.
As we have seen, there are good neurological grounds for believing that phenomenal consciousness in mammals is impossible in the absence of either a neocortex or anterior cingulate cortex. Neither of these structures, or any obvious homologs (structures reflecting a common ancestry) can be found in birds, reptiles, amphibia and fish. This is the cardinal obstacle to the decisive identification of phenomenally conscious states in non-mammals.
A causal argument analogical argument for consciousness in non-mammals
Despite the failure of the argument from homology, a strong analogical case for the occurrence of consciousness in non-mammals can still be made if it can be shown that:
(a) their brains possess structures that are comparable in their degree of complexity to those that support consciousness in mammals;
(b) the structures also play an analogous causal role in regulating these creatures' behaviour; and
(c) their behaviour either:
(i) fulfils the criteria for primary consciousness (Baars, 2001; Rose, 2002) or
(ii) is of a level of complexity comparable with that of mammals.
Neurological requirements for consciousness in birds
It is not currently known if birds possess an analogue to the reentrant pattern of interaction in the mammalian thalamocortical system (Kavanau, 1997, p. 257; Cartmill, 2000; Edelman, personal email, 19 July 2004).
However, birds' waking and sleeping EEG patterns are similar to those of mammals. For other vertebrates, the situation is different:
Among vertebrates, true sleep, involving a shift from fast to slow waves in the forebrain, appears to be limited to mammals and birds, though there are hints of it in some reptiles (Cartmill, 2000).
In reptiles and birds, the dorsal ventricular ridge serves as a principal integratory centre and exhibits a pattern of auditory and visual connections with sensory centres and the thalamus which is broadly similar to that of the sensory neocortex in mammals. Fish and amphibians lack this structure (Russell, 1999; Aboitiz, Morales and Montiel, 2000). In birds, the dorsal ventricular ridge includes two areas: the hyperstriatum ventrale and neostriatum (Medina, 2002). There is good evidence that the mammalian neocortex and the neostriatum-hyperstriatum ventrale complex in birds have similar integrative roles. Interestingly, the relative size of the hyperstriatum ventrale in different species is the best predictor of their feeding innovation rate (Timmermans et al., 2000).
The ventricular ridges of birds are well-developed, but not laminated (Kavanau, 1997, p. 258).
However, even though largely non-laminated, the avian telencephalon [forebrain] can generate visual performances of a complexity rivaling and even exceeding those of mammals, previously thought to have been correlated uniquely with cortical lamination... The mechanisms of visual information processing in the brains of birds are ... at least as efficient as those in the mammalian striate cortex (Kavanau, 1997, p. 257).
On neurological grounds, the case for primary consciousness in birds is still only suggestive.
Behavioural complexity in birds
It is worth noting that none of the scientists and researchers whom I contacted by email were able to nominate even a single kind of behaviour which might serve to identify phenomenally conscious states or feelings in animals, and which is found only in mammals.
At least some birds and mammals do, however, share a number of distinctive complex behaviours that have not been found in other vertebrates:
Interestingly, there are really only six animal groups capable of vocal learning: humans, cetaceans, bats, parrots, songbirds, and hummingbirds (see Jarvis et al., 2000). Parrots, in particular, represent an interesting case. The studies by Pepperberg and her colleagues (see Pepperberg, 1998; Pepperberg & Shive, 2001; Pepperberg & Wilcox, 2000) have shown that parrots are capable of acquiring a level of word comprehension rivalled in nonhuman species only by pygmy chimpanzees (see Savage-Rumbaugh, McDonald, Sevcik, Hopkins, & Rubert, 1986; Savage-Rumbaugh, Rumbaugh, & McDonald, 1985; Savage-Rumbaugh, Sevcik, Rumbaugh, & Rubert, 1985) (Edelman, personal email, 19 July 2004).
Edelman also notes that "[a] good number of avian species migrate mind boggling distances with incredible fidelity year after year" (personal email, 19 July 2004) - a feat which is thought to be cognitively taxing.
The behaviour described above suggests that the brains of birds have a neural complexity that is currently under-estimated.
Conclusion: There is a powerful analogical argument, based on neurology and behaviour, for the occurrence of phenomenal consciousness in birds.
Neurological requirements for consciousness in reptiles, fish and amphibia
Reptiles, like birds, possess a dorsal ventricular ridge serves as a principal integratory centre and exhibits a pattern of auditory and visual connections with sensory centres and the thalamus which is broadly similar to that of the sensory neocortex in mammals. Only in birds does the ridge contain the hyperstriatum ventrale and neostriatum (Medina, 2002); in reptiles these features are absent. Fish and amphibia do not have a dorsal ventricular ridge
The only neurological feature of conscious in mammals that is even partially satisfied by reptiles is true or brain sleep:
Among vertebrates, true sleep, involving a shift from fast to slow waves in the forebrain, appears to be limited to mammals and birds, though there are hints of it in some reptiles (Cartmill, 2000).
A few researchers (Panksepp, Cabanac) nevertheless consider reptiles to possess a rudimentary affective form of consciousness which, they claim, does not presuppose the existence of a cerebral cortex.
Behavioural complexity in reptiles, amphibia and fish
There are certain complex behaviours that might be relevant to the possession of phenomenal consciousness, which are found in mammals, but not in reptiles, amphibians or fish:
It seems that a snake does not have a central representation of a mouse but relies solely on transduced information. The snake exploits three different sensory systems in relation to prey, like a mouse. To strike the mouse, the snake uses its visual system (or thermal sensors). When struck, the mouse normally does not die immediately, but runs away for some distance. To locate the mouse, once the prey has been struck, the snake uses its sense of smell. The search behavior is exclusively wired to this modality. Even if the mouse happens to die right in front of the eyes of the snake, it will still follow the smell trace of the mouse in order to find it. This unimodality is particularly evident in snakes like boas and pythons, where the prey often is held fast in the coils of the snake's body, when it e.g. hangs from a branch. Despite the fact that the snake must have ample proprioceptory information about the location of the prey it holds, it searches stochastically for it, all around, only with the help of the olfactory sense organs (Sjolander, 1993, p. 3).
Finally, after the mouse has been located, the snake must find its head in order to swallow it. This could obviously be done with the aid of smell or sight, but in snakes this process uses only tactile information. Thus the snake uses three separate modalities to catch and eat a mouse (Dennett, 1995b, p. 691).
A snake has no ability to anticipate that a mouse running behind a rock will reappear. Cats and other predatory mammals are able to anticipate that the prey will reappear (Grandin, 1998).
As I suggested earlier in this chapter, the kind of consciousness presupposed here might be perhaps best thought of as an integrative consciousness.
Sjolander (1993) argued that the lack of these abilities he described should count as evidence against an animal's being phenomenally conscious, and I am inclined to agree with him, if the lack is permanent and life-long: a conscious newborn baby lacks the concept of object permanence, and an autistic person suffering from sensory overload is unable to integrate information (Grandin, 1998).
On the other hand, in section 1.7.3 of this appendix, I examined evidence cited in support of the view that reptiles possess conscious emotions, while fish and amphibians do not (Cabanac, 1999, 2003). Briefly, reptiles exhibit certain forms of hedonic behaviour, whereas amphibia lack them. For this reason, Cabanac considers reptiles to be the most primitive creatures with phenomenal consciousness.
Just as we proposed a causal analogical argument in support of phenomenal consciousness in birds, we can now propose a similar argument against its occurrence in reptiles, fish and amphibians:
(i) the brains of fish and amphibians satisfy none of the neural requirements of consciousness described earlier in this chapter. The EEGs of reptiles share a few points of commonality with those of mammals and birds, but they also fall far short of meeting the requirements;(ii) the brains of fish and amphibians have no brain structure whose causal role is analogous to the mammalian neocortex, while the structure in reptiles whose causal role is analogous to that of the neocortex is very rudimentary;
(iii) additionally, reptiles, amphibians and fish appear to lack certain behavioural capacities that one might reasonably expect of a phenomenally conscious animal, therefore
(iv) it is likely that these animals are not phenomenally conscious.
Conclusion: There is a powerful analogical argument, based on neurology and behaviour, against the occurrence of phenomenal consciousness in reptiles, and an overwhelmingly strong argument against its occurrence in amphians and fish.
CASE STUDY - fish welfare
It has been argued in this thesis that fish lack phenomenal consciousness, but nevertheless can be said to take an interest in whatever they pursue, as well as having certain biological interests. The follwing four tables illustrate some welfare indicators for these animals, as well as ways in which the practices of aquaculture, angling and keeping ornamental fish may adversely impact on their welfare.
The source of the information listed below is: FSBI. 2002. Fish Welfare. Briefing Paper No. 2, Fisheries Society of the British Isles, Granta Information Systems, Cambridge, UK.
TABLE 1: Sensitive and easily applied welfare indicators for fish
| Changes in colour: Stress-induced changes in skin or eye colour (with a complex hormonal background) have been reported in a number of fish species, including ornamental species (Etscheidt 1992), and so could be a sign of exposure to adverse events. Eye colour as an index of social stress/subordinate status in salmonids provides an example. |
| Changes in ventilation rate: A high oxygen demand is reflected by rapid irrigation of the gills. The rate of opercular beats is therefore increased by stress and can be counted, automatically or by eye. This, together with a visual assessment of gill status, is used as a sign of incipient problems in ornamental fish (Etscheidt 1992) and to monitor exposure to pollutants in salmonid fish. |
| Changes in swimming and other behaviour patterns: Fish may respond to unfavourable conditions by adopting different speeds of swimming and by using of different regions of a tank or cage (Morton 1990, Etscheidt 1992, Juell1995). Abnormal swimming has been used as a sign of poor welfare in farmed fish (Holm et al. 1998). Known behavioural responses to adverse events and conditions are potential signs of both general and specific trouble (Morton1990). These include excessive activity or immobility (Etscheidt 1992), body positions that protect injured fins, escapeattempts in confined conditions and chafing movements to dislodge ecto-parasites (Furevik et al.1993). |
| Reduced food intake: Notwithstanding that there are many reasons why a fish might not eat, the fact that feeding is suppressed by acute and chronic stress means that loss of appetite is potentially a sign of impaired welfare. |
| Slow growth: Notwithstanding that growth rates in fish are flexible and naturally variable, sustained reductions in growth may be indicative of chronic stress. Thus where fish are regularly weighed or where size can be assessed by eye (or by underwater camera) slow growth can be used as a possible sign of trouble. |
| Loss of condition: Fish change shape and/or lose weight for many reasons, but because reduced feeding and mobilisation of reserves are secondary stress responses, where fish are regularly weighed and measured, or where body shape can be assessed by eye (for example by the visibility of the vertebrae, Escheidt 1992) loss of condition can be used as a possible sign of trouble. |
| Morphological abnormalities: Because adverse conditions can interfere with normal development, the occurrence of morphological abnormalities can be used as an indicator of poor larval rearing conditions (Boglione et al. 2001). |
| Injury: Injury may be a direct consequence of an adverse event, in which case, the presence of such injuries is a sign of poor welfare. For example, dorsal fin injury in salmonids is often caused by attacks from conspecifics (Turnbull et al. 1998) and scales that are dislodged rather than lying flat are a sign of poor welfare in ornamental fish (Etscheidt 1992). In addition, because immune responses can be suppressed by cortisol, slow recovery from injury (or a high incidence of injury) may be a sign of generally poor conditions. However, fin erosion has multiple causes and these are not fully understood. |
| Disease states: Since the causes of most aquatic diseases are complex and dependent on environmental conditions, a diseased state can indicate an underlying problem with the environment or management. Increased incidence of disease in any population of fish should be treated as a warning that there may be other underlying problems. However, interpreting the welfare implications of an observed disease requires a detailed understanding of the natural history of the disease and in some cases diseases are not sufficiently well understood to interpret their implications for welfare. |
| Reduced reproductive performance: For many farmed species, reproduction is prevented or avoided in growing stock. Where this is not the case, for example, in brood stock or where ornamental fish are concerned, because chronic stress impairs reproductive function, failure of adult fish to breed or to display normal patterns of reproductive behaviour. |
Overview of current scientific understanding of the impact of common practice in aquaculture, angling and the keeping of ornamental fish, with a few representative examples
TABLE 2: AQUACULTURE: SOME DEMONSTRATED EFFECTS ON WELFARE
| Transportation | Certain kinds of transportation induce physiological stress responses and a prolonged recovery period may be necessary (Bandeen & Leatherland 1997, Barton 2000, Rouger et al. 1998, Iversen et al. 1998, Sandodden et al. 2001). |
| Handling/netting | Physical disturbance evokes physiological stress responses in many species of farmed fish (reviewed by Pickering 1998) and reduces disease resistance (Stangeland et al. 1996). |
| Confinement and short-term crowding | Physical confinement in otherwise favourable conditions increases cortisol and glucose levels and alters macrophage activity in various species (Garci-Garbi et al. 1998). Carp show a mild, physiological stress response to crowding that declined as the fish adapted, but crowded fish are more sensitive to an additional acute stressor (confinement in a net; Ruane et al. 2002). Crowding during grading increases cortisol levels for up to 48h (Barnett & Pankhurst 1998). |
| Inappropriate densities | High densities impair welfare in some species (trout, salmon: Ewing & Ewing 1995, bass: Vazzana 2002, red porgy: Rotllani & Tori 1997), but enhance it in others (catfish and Arctic charr, Jorgensen et al. 1993). Halibut suffer less injury at high densities (Greaves 2002) but show more abnormal swimming (Kristiansen & Juell 2002). The relationship between welfare and density may be non-linear; low densities may harm rainbow trout, in salmon negative effects start to appear at a critical density and density interacts with other factors such as disturbance or water quality (Ewing & Ewing 1995, Bell 2002, Scott et al. 2001). |
| Enforced social contact | Aggression can cause injury in farmed fish, especially when competition for food is strong (Greaves & Tuene 2001). Subordinate fish can be prevented from feeding (Cubitt 2002), may grow poorly and are more vulnerable to disease (reviewed by Wedermeyer 1996). |
| Water quality deterioration | Many adverse effects of poor water quality have been described, with different variables interacting, e.g. undisturbed salmonids use c. 300 mg of oxygen per kg of fish per hour and this can double if the fish are disturbed. For such species, access to aerated water is essential for health (Wedermeyer 1996). Immunoglobulin levels fall in sea bass held at low oxygen levels (Scapigliati et al.1999). Heavy metals cause extensive gill damage in acidic water but are non-toxic in hard, alkaline water (see Wedermeyer 1996). |
| Altered light regimes | Atlantic salmon avoid bright surface lights, except when feeding (Fernoe et al.1995). Continuous light increases growth in several species (e.g. cod: Puvanendran & Brown 2002). |
| Food deprivation | Dorsal fin erosion increases during fasting in steelhead trout (Winfree et al.1998). Plasma glucose increase in Atlantic salmon after 7 days without food, but other welfare indices are unaffected (Bell 2002). Atlantic salmon deprived of food for longer periods (up to 86 days) lose weight and condition, stabilising after 30 days (Einen et al. 1998). Farmed Atlantic salmon swim slower and fight less during feeding bouts when fed on demand (Andrews et al. 2002). |
| Disease treatment | Therapeutic treatments themselves may be stressful to fish (e.g. Griffin et al. 1999, 2002, Thorburn et al. 2001, Yildiz & Pulatsu, 1999). |
| Unavoidable contact with predators | Brief exposure to a predator causes increased cortisol levels and respiration rate and suppressed feeding (eg Metcalfe et al. 1987). Mortality and injury due to attacks by birds and seals can be high among farmed fish (eg Carss 1993). |
| Slaughter | All slaughter methods are stressful, but some are lees so than others (Robb et al.2000). Small, warm water fish such as sea bass killed by chilling in ice water had lower plasma glucose and lactate levels and showed less marked behavioural responses than those killed by other methods, in particular asphyxia (Poli et al. 2002, Skjervold et al. 2001). Electostunning may be less harmful for larger fish such as trout. |
TABLE 3: ANGLING: SOME DEMONSTRATED EFFECTS ON WELFARE
| Capture - hooking | Injury and mortality following hooking is common, primarily in deep-hooked fish (Dubois et al.1994; Hulbert & Engstrom-Heg 1980, Muonehke & Childress 1994). |
| Capture - playing / landing | Capture of fish by rod and line elicits a stress response of short duration (Gustaveson et al. 1991, Pankhurst & Dedual 1994, Pottinger 1998). Estradiol levels are suppressed in rainbow trout within 24h of capture by rod and line (Pankhurst & Dedual 1994). |
| Capture - handling | Exposure of exercised fish to air can have severe metabolic effects (lactate increase and altered acid-base balance), especially in larger fish (Ferguson et al. 1993). Capture and handling suppress reproductive function in brown trout (Melotti et al. 1992). |
| Retention / constraint / release | Retention of fish post-capture in either keepnets or stringers induces physiological stress responses, but recovery following release can be rapid (Pottinger 1998, Sobchuk & Dawson 1988). Hooking and handling for release can increase scale damage by 16% (Broadhurst & Barker 2000), possibly making released fish liable to infection. Abnormal behaviour can occur following release after a stressful event (Mesa & Schreck 1989, Olla & Davis 1989). |
TABLE 4: KEEPING ORNAMENTAL FISH - SOME DEMONSTRATED EFFECTS ON WELFARE
| Capture. Exposure to Poisons. | Marine tropical fish captured by sodium cyanide suffer very high mortality for several weeks after capture (Hignette 1984). Clove oil is a better alternative (Erdmann 2002). |
| Transportation | Estimates for mortality during capture of ornamental fish from South America range from 5 to 10% but may be as high as 30%. A further 5 to 10% mortality is estimated to occur during transportation and at the holding facilities (Ferraz de Olivera 1995). During the acclimation period following importation mortalities can be up to 30% (FitzGibbon 1993). However, in all these aspects of the ornamental fish trade there is a great deal of variability. The Ornamental Fish Trade Association has regulations to improve all aspects of capture and transport of fish (www.aquariumcouncil.org). |
| After purchase, constraint in a confined space | See above, under aquaculture. |
| Handling | See above, under aquaculture. |
| Inappropriate densities/species combinations | Lack of appropriate social environment (wrong species or inappropriate numbers) is an important cause of poor health in ornamental fish (Etscheidt 1995). |
| Poor water quality | 81% of ornamental fish are held outside the optimal pH range, 36% at inappropriate temperatures (Etscheidt & Manz 1992). Poor water quality is the commonest cause of mortality in ornamental fish (Schunck 1980). |
| Deprivation of social contact | Angelfish transferred singly to a new tank take longer to resume feeding than those transferred in groups of 3 or 5 (Gomez-Laplaza & Morgan 1993). |
| Inappropriate feeding regimes | Inappropriate range and types of food can cause poor health in ornamental fish (Etscheidt 1995). Inappropriate feeding is not usually a direct cause of mortality in ornamental fish, but can be a contributory factor (Schunck 1980). |
| Unavoidable contact with a predator | In 19% ornamental tanks prey were housed in small tanks in direct contact with predators (Escheidt & Manz 1992, Foggitt 1997). See above under aquaculture. |
| Disease treatment | See above under aquaculture. |