American Board of Veterinary Practitioners - Symposium 2002
May 17, 2002, Manhattan Beach, California
Pain, Stress, Distress and Fear
Emerging Concepts and Strategies in Veterinary Medicine
(Updated September 2003)
Fear operates in a more primitive subcortical brain circuit than pain. When the cortex is removed, an animal will no longer suffer from pain but it can still learn a conditional fear response. A review of the literature indicated that prefrontal cortex activation tends to increase pain perception but reduce fear responses. Fear is extremely aversive and it is likely that it causes suffering in all vertebrates and possibly invertebrates such as the octopus that has a well developed nervous system. Pain perception requires more higher association circuits than responses to fear. Therefore it is likely that as the phylogenetic scale is descended there may be animals which would suffer from fear but not pain.
Experiments need to be conducted to determine if lower vertebrates will seek pain relieving medication in the same manner as warm blooded animals.
It has long been argued that the capacity to experience pain and suffering is associated with the size and structure of an animal’s brain. Iggo (1984) suggested that although animals have similar brain structures, the size of those structures may be related to the capacity to experience pain. In this framework, a rat would suffer less than a cat, and a cat less than a dog. We disagree. More recently, Bermond (1997) proposed that an animal must posses a well developed prefrontal cortex and right neocortex. In this framework, only humans, higher apes and possibly dolphins can experience suffering. This paper provides evidence to refute these claims and offers suggestions for a more objective approach to assessing criteria used to decide whether an animal is capable of suffering. Whereas Bermond (1997) thinks many mammals are in a “gray area” when it comes to suffering from pain, we are proposing that only fish, amphibians, and some reptiles may represent the “gray area” of understanding for suffering from pain but that all vertebrates can suffer from fear.
The question is, how much circuitry linking subcortical and higher association areas is needed for an animal to suffer from pain? To make an analogy, the vast literature on pain tells us how the telephone lines and the switching equipment works, but it does not tell us how the cortex of an animal is interpreting this information. All the research on “wiring” and “switchboards” does not tell us if the animal suffers. A brief review of the higher association areas in the brains of mammals is followed by discussing possible ways to gain insight into the subjective experience of pain proper which Smith and Boyd (1991) define as; “the conscious emotional experience of pain which involves nerve pathways to the highest parts of the brain and cerebrum.” There will also be a discussion on fear and suffering.
Some scientists consider the dorsal lateral prefontal cortex to be the "true" prefontal cortex.
After a lobotomy, patients with chronic pain or depression often regained the ability to function normally and retained their general intelligence, but they lost all emotional depth and feeling (Freeman & Watts, 1950; Foltz & White, 1962; Hurt & Balliantine, 1974). Their emotional experience was greatly reduced after lesioning of the prefrontal cortex, and patients with the largest areas of the prefrontal cortex disconnected had the greatest effects. However, lobotomy patients retained normal pain reflexes and would pull away when a doctor manipulated an injured area of their body. They “disliked momentary pain yet were indifferent to the pain of their disease” (Freeman & Watts, 1950). A patient might scream when a doctor manipulated a tender body part, but the next minute he was smiling after the painful manipulation was stopped. Their behavioral reactions seemed disjointed. Lobotomy patients experienced pain, but did not experience the emotional feeling of pain. The patient’s reaction to a painful medical procedure was entirely in the present. They seemed to have lost the fear of pain.
More recently, pain research on humans show that a mildly painful stimulus applied to the hand increases blood flow in the frontal cortex (Smith and Boyd, 1991), and a PET scan study by Rainville, et al (1997) provided direct experimental evidence linking the PFC with the emotional component to pain. By using hypnotic suggestions to both increase and decrease a pain sensation, significant changes in pain-evoked activity was found in the anterior cingulate cortex. This is consistent with the clinical observations made in lobotomy patients. A more recent study on chronic pain which causes long-term suffering showed that activity in the frontal cortex was increased (Apkorian et al., 2001). Fulbright et al. (2001) found that pain and basic sensory input are processed in different parts of the brain. A painful cold water stimulus activates the anterior circulate and a non-painful cold stimulus only activates sensory areas.
Lesion studies in rats indicate that the frontal cortex has similar functions in rodents and humans. Lesions in the frontal cortex of rats impairs behavioral flexibility and the organization of species typical behaviors (Kolb and Tees, 1990). In both humans and rats, frontal cortex lesions cause behaviors to become disjointed and fragmented (Freeman and Watts, 1950; Kolb and Tees, 1990). Even the small frontal cortex in the rat brain performs the same functions as mammals with more complex brains (Kolb and Tees, 1990). Therefore, it is likely that the frontal cortex in rats is involved in pain perception in a similar manner as humans.
The ability to learn complex associations seems to be a prerequisite for “a human like” suffering to occur in other mammals. Even the smallest mammals seem to have the required associative circuitry to learn complex associations. Holland and Straub (1979) made rats ill by injecting them with lithium chloride after eating a type of food they had previously learned to associate with a tone. Afterwards, the rats approached the feeder much slower after hearing the tone compared to rats made ill without any association with the food. It appears that the tone reminded the rats of the food, which then reminded them of feeling ill. Although interpreting evidence of declarative representations of knowledge in animals is difficult, it is most relevant when considering criteria for suffering. The rats in the Colpaert et al (1980, 1982, 2001) experiments must have “known” that even though the analgesic solution was unpalatable, drinking it would make them feel better.
Grandin (1997) and Bateson (1991) stress the importance of separating fear stress from physical stress such exertion from running or overheating. Fear has a powerful ability to override pain in the chicken. The work by Gentle and Corr (1995) shows that a chicken that was pain guarding by holding it’s leg up will stop pain guarding when it is placed in a scary novel place. When electric shocks are used as an aversive stimulus on cattle, the effects of fear can not be separated from pain. When wild cattle that are not accustomed to handling are held in a restraining device for branding, the fear stress induced by restraint will raise their cortisol levels almost as high as the hot iron branding (Lay, et al 1992a, 1992b). In tame cattle who do not react fearfully to restraint, the pain from branding is probably the main component of the animal’s distress because branding will increase cortisol levels significantly more than restraint. Training an animal to voluntarily allow itself to be restrained can almost eliminate or greatly reduce fear stress (Phillips, et al 1998; Grandin and Deesing, 1998; Boissy, 1998; LeDoux, 1994).
Research with humans and monkeys indicates that the old primitive fear system will operate independently of the prefrontal cortex and more complex emotions such as anxiety or worry depend on the prefrontal cortex. Lesioning the amygdala in a monkey will reduce its response to an unconditional fear stimuli such as a snake, but this lesion has little effect on the behavioral and physiological responses that characterize an anxious temperament (Kalin et al., 2001). However, in humans a larger anterior cingulate is associated with more anxiety and worry (Pujol et al., 2002). Therefore, the anterior cingulate in the frontal cortex may have a duel role of helping to shut off primitive fear responses but it may increase a more complex generalized anxiety.
The second author’s observation of pain guarding in horses is an example of chronic pain related behavior that is definitely not caused by fear. When horseshoes are put on a horse, nails are driven through the insensitive hoof wall. A fine line exists where nails can be driven safely, but sometimes a nail may pierce the sensitive tissue. When this happens, the horse may or may not react. It depends on how deeply the nail pierces the sensitive tissue. This is like the difference between getting a small sliver versus a large sliver under your fingernail. You may or may not feel pain at the time, but within twenty-four hours the area becomes infected and starts to hurt. Immediately after shoeing the horse walks normally and there is no pain guarding. It is the next day when infection sets in that the horse begins to limp. This may happen while it is quietly grazing. As the abscess grows the limp gets worse. Because the abscess begins to cause pain twenty-four hours after the shoeing, the horse’s reaction is not due to fear. This is an example of true pain guarding that is not reflex. Since the pain occurs the next day, the horse would not associate it with shoeing. The horse is reacting to pain and not fear. The reaction is not just reflex like jerking your hand off a hot stove. As the foot heals the horse will limp less and less. It has a graded response to the pain. Reflexes tend to be all or none. The reflex is either performed or it is not performed.
Do reptiles or amphibians suffer from pain? Research shows that the nervous system of amphibians responds to analgesic drugs. Amphibians will respond to a painful stimulus applied to the skin. Many different types of analgesic drugs will reduce the response (Stevens et al., 1994; Stevens et al., 2001). Is this true suffering from pain or is it just a reflex like touching a hot stove?
Do reptiles and amphibians pain guard or seek analgesics? Both these areas need to be researched. The antedotes below may provide some insights for guiding future research. Discussions with reptile specialists indicate that reptiles may or may not pain guard. Friend (1998 personal communication) indicates that igaunas will walk on a severely damaged leg and make no attempt to reduce weight on the damaged limb. Igaunas are physically capable of lifting a leg to favor it, but they do not. Lizards react to noxious stimuli which may cause acute pain, but may have little reaction to injuries that would cause long term pain. However, Friend (1998) was adamant that reptiles experience pain, but when we discussed pain guarding behavior and chronic pain, she stated; “I never thought about that before.” Discussions with Dr, Fredrick Fry a reptile veterinarian at the University of California indicated that there are signs of pain guarding in other reptiles. A tortoise with a sore mouth will not eat and if it has a sore toe it will not walk. This is likely to be true pain guarding. Snakes with a damaged mouth may refuse to eat or lie on their backs to avoid pain. A tortoise with an abscess in it’s head will refuse to eat. Eating resumes shortly after the abscess is drained. Even fish pain guard. Dr. Steve Kestin, University of Bristol states that a fish with an inflamed gut will reduce activity. Maybe this can be explained by weakness from sickness. However, the fish will swim normally when it is chased with a net. Dr. Kestin also says a fish will avoid the place where it has been hooked or shocked. Rakover (1979) reports that fish can easily learn to avoid an aversive fear arousing stimulus by swimming away. In these situations it is impossible to separate fear from pain. Feelings of fear are very aversive and subjecting any animal to situations which cause it to be highly fearful would be very detrimental to its welfare.
The author concludes that the pain related behaviors were not simple reflexes (Sneddon, 2003). Sneddon et al. states that the pain receptors in fish have the same properties as the receptors in mammals. The fish also engaged in true pain guarding behavior. Fish injected with acetic acid took significantly longer to start feeding compared to saline injected controls. These studies indicate that to insure a reasonable level of welfare providing pain relief should be considered for fish.
This excellent research study separated the variables of pain from fear by having a saline injected control. Further studies on long term chronic pain are needed.
Studying of pain guarding behavior in different animals may help separate the variables of stress and fear from pain. Due to ethical concerns, pain guarding behavior and reactions to chronic pain in mammals should be studied under field conditions or in veterinary clinics. Individual cases can be observed when clients bring their animals in. This would avoid deliberately subjecting animals to chronic long term pain. Careful observations of painful conditions in client animals and farm animals subjected to routine painful husbandry procedures may provide added insights. Pain guarding should be studied using a video camera when the animal is undisturbed. Many animals, especially prey species such as cattle and horses will stop pain guarding when they are threatened or excited. The need to escape from a predator overrides the need to prevent further damage to the injured limb. We observed this behavior recently in a bull that was being castrated with a large rubber band. When he was unaware of being watched, he laid on his side and was moaning. As soon as he saw us, he jumped up and behaved as if he was not in pain until we left.
The authors hypothesize that an animal will suffer from pain if it has sufficient circuits that merge pain signals with structures involved with emotion. Even if scientific research were to prove that some reptiles or fish perceive pain in a manner similar to the lobotomy patients, there would still be a need to avoid subjecting them to stimuli that causes fear. Fear inducing stimuli are very aversive and fish will avoid them. Fear is an old primitive emotion and the authors speculate that fear may cause suffering further down the phylogenetic scale than pain. For example, a fish might have attenuated perception of pain but it could suffer greatly from fear. Whereas a dog would suffer greatly from both pain and fear and a chicken could suffer greatly from either pain or fear depending upon the situation. We propose that there is probably a certain minimum amount of associative circuits between circuits processing emotion and the cortex are required for an animal to suffer from pain and even fewer association circuits are required to suffer from fear. It is our opinion that animals that display true pain guarding behaviors and actively seek analgesic drugs have this required minimum. A further analogy can be made to computers. Both the cheapest personal computer and a super computer can do word processing. They both do it equally well, but a calculator can not do word processing under certain conditions. An animal that has prefrontal functions at the “calculator” level may suffer less from pain than an animal with the “cheap computer” level. It appears that the chicken is different than mammals. Possibly it suffers fully from pain when it is undisturbed, but pain is easily overridden by fear or feeding motivation. It is likely that it’s small associative circuits can only process one emotion at a time.
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