Most people agree that, in general, pain is bad and should be avoided when the pain is not necessary for the achievement of some future benefit. Moreover, the badness of the pain seems to be directly related to the experience of pain; pains are bad, at least in part, because they feel bad. Yet for roughly the past fifty years, philosophers have been puzzled by reports of people who claimed that they were “feeling pain” but not “bothered by it.” These reports are surprising because on one common interpretation, pain is essentially bothersome; one cannot have a pain without having an experience that is unpleasant or aversive in some way.
One well-supported explanation of these reports is that the experience of pain has at least two distinct components: a sensory component and an affective component (Melzack and Casey 1968). Many experiments have shown that these two dimensions can be influenced independently of one another. As such, we can view reports of feeling pain but not minding it as instances where the affective dimension of pain is selectively impaired, but the sensory dimension is operating normally.
In this essay, after reviewing the importance of understanding the affective dimension of pain, I will describe what is known about this dimension of pain in other species. Ultimately, I will argue, the main impediment to progress in understanding the unpleasantness of pain is the lack of a sufficiently detailed investigation of cases where humans report feeling pains without finding them unpleasant. In reviewing the literature on pain in animals, I do not intend to suggest that current invasive and/or painful research is justified; indeed, it may be the case that what we learn from such research is enough in itself to provide an indictment of certain research practices. However, I do think we should use the information we currently have to improve our understanding of how pain relates to important philosophical issues.
It is generally thought that intentionally causing pain to others is morally problematic, and most people extend this reasoning to our treatment of nonhuman animals. This is not to say that any action that causes pain is automatically wrong, but rather that pains considered by themselves are a bad thing and causing pain to others, without having some reason that outweighs the harm caused by the pain, is therefore bad. For example, taking a dog to the vet to get a blood sample might cause some momentary pain, but because that pain is in the service of improving future quality of life, we can see that the overall action is good for the dog. So we can amend the above statement to the suggestion that most people would agree that causing unnecessary pains to others is morally wrong.
The idea that causing unnecessary pains is wrong has been at the heart of many debates about our treatment of animals. Critiques of factory farming and animal experimentation have referenced the pain caused to animals as primary reasons why those practices are wrong (Singer 1975, Regan 1983). And defenders of the practices typically do not say that causing pain doesn’t matter, but rather suggest either that the pain is minimal or that the pains are balanced out by other considerations.
However, the reports of people who feel pains but are not bothered by them suggest that the situation is even more complicated. It is not pain that is always bad, but rather a specific component of the experience of pain: the unpleasantness of pain. Pains that are not unpleasant, or that are not bothersome, are not bad in the same way as the typical pains we are familiar with.
In what follows, I describe the relevance of the affective/sensory dissociation in pain for our treatment of animals. Before highlighting the intersection with philosophical issues, however, I have to say a little more about our current understanding of the different dimensions of painful experience.
The sensory dimension of pain is generally described as consisting of three elements: the, “quality, intensity, and spatio-temporal characteristics,” of the pain sensation (Rainville et al. 1999, p. 159). When we experience a typical acute pain, we experience it as occurring in a particular part of our body and having certain temporal properties (for example, a “throbbing” pain rapidly fluctuates in intensity); this is the spatio-temporal aspect referred to by Rainville. Our experience also typically represents pains as being of a certain type: a “cutting pain” or a “burning pain” or a “pinching pain,” for example. These different types of pains typically result from the activation of nerve fibers in the skin, called nociceptors, that respond to different forms of potentially damaging events, such as extreme temperatures, chemical substances, or tissue damage. The representation of these types of pain is the “quality” of the pain referenced in the quote above. Finally, pains vary in degrees of intensity. Some pains, of course, are stronger than others.
Somewhat surprisingly, however, these three sensory characteristics do not fully determine the immediate experienced unpleasantness of the pain. Under the right conditions, more intense pains can be less unpleasant, and less intense pains can be more unpleasant. If a person is expecting a pain, this can influence the perceived unpleasantness of a pain, even as the ratings of pain intensity stay the same (Sawamoto et al. 2000). Likewise, increased anxiety causes pains to feel more unpleasant even when the ratings of intensity stay the same (Ploghaus et al. 2001). Moreover, certain drugs appear to selectively influence the stated unpleasantness (Keats and Beecher 1950). And lesions to particular brain areas have resulted in patients who claim that they feel pains but no longer find the pains unpleasant (Foltz and White 1962, Grahek 2001, Aydede 2006). Indeed, the affective dimensions of pain can be manipulated independently of the sensory dimension, and two distinct activation patterns during brain imaging correspond to the different dimensions (Rainville et al. 1997, Rainville et al. 1999).
Because people’s reports of pain intensity can diverge from their reports of unpleasantness, we should acknowledge that the two dimensions come apart. Nevertheless, there still are many questions remaining about the nature of unpleasantness. What role does unpleasantness, as opposed to other aspects of pain experience, play in our behavior? How was it useful from an evolutionary standpoint? Is there some other psychological capacity or behavioral indicator that could help us to understand what unpleasantness is actually doing?
Many pain researchers use the term “affective-motivational” to describe the pathway involved in unpleasantness, which implies that this pathway also underlies the motivational urge associated with pain. Some have suggested the unpleasantness of pain can be linked with the motivational force of pain; that is, if we find a pain unpleasant, we necessarily have some motivational urge to escape the pain. However, the science relevant to this claim is currently inconclusive, and thus it remains an open possibility that the affective and motivational aspects of pain are two separate components.
Beyond motivation, there are a host of other features that may or may not be correlated with the affective dimension of pain. Austen Clark has listed all of the following conceptually distinct variables as possible features linked to the affective dimension of pain: the desire to end the pain, the feeling of urgency to do something about it, the degree to which pain grabs one’s attention, the extent to which pain alters one’s preferences, the degree to which the reduction of pain can serve as a reward, and the degree to which the pain reduces the probability of future behaviors (2005, p. 185). All of these are potential correlates of pain’s unpleasantness that could potentially be used in third-person assessments of suffering, and therefore could be important for determining which nonhuman animals have the capacity to experience the unpleasantness of pain.
Making this determination has a number of important ethical implications. Consider animal agriculture, where there are a large number of practices that are extremely morally problematic if, as the animals’ behavior indicates, the animals involved are capable of suffering (see Rossi and Garner 2014 for a useful review). Undercover footage reveals that insufficient stunning prior to slaughter occurs frequently, leading to animals who are conscious as their throats are slit. Techniques such as the dehorning and branding of calves, the castration of boars, and the debeaking of chickens are frequently done without painkillers. Many animals are kept in cramped conditions where they are unable to engage in natural movements, which results in joint and bone damage. And animals are often fed extremely unnatural diets, which leads to digestive problems known to be extremely painful in humans. This is just a small sample of likely painful events in animal agriculture; but even from this limited set, it should be clear that if these animals feel the unpleasantness of pain in a manner similar to humans, it becomes extremely difficult to provide moral justification for an industrial agriculture system that is not necessary for human health or survival.
In the context of research on nonhuman animals, millions of animals in laboratory settings are reported to experience moderate to severe pain each year (Rowan 2012, p. 207). This includes many invasive procedures that fall under what is classified as “Category E” research in the United States, where animals known to be in distress are not given painkillers because it is believed they might interfere with the validity of the study’s findings. Even in cases where animals are given painkillers, it is often standard practice to, for example, give primates post-surgical analgesia for a period of one to two days after a procedure that would call for several weeks of painkillers in humans (Balcombe 2014). It should be clear that in animal agriculture and animal research, as well as many other practices such as hunting, trapping, and the use of animals for entertainment, determining which animals have the capacity to suffer will have enormous moral significance. But how do we go about determining which animals are capable of suffering? Our ability to determine this will depend, at least in part, on our understanding of the neural mechanisms underlying suffering.
For example, fish scientist James Rose (2002) has suggested that the fact that fish lack the brain areas involved in mammalian pain affect excludes them from moral consideration. Rose put his arguments in terms of consciousness in general; however, the areas he cited as crucial were specifically those that are associated with unpleasantness in humans. Craig (2009) has suggested that the insula (a structure involved in the affective dimension of pain) integrates bodily information (including information about pain) into a conscious representation of the body, and argues that only humans and possibly great apes have the relevant brain structures to support conscious awareness. And Allen et al. (2005) and Shriver (2006) have noted that all mammals appear to have many of the relevant brain areas underlying the affective dimension of pain in humans. On the other end of the spectrum, Klein and Barron (2016) recently argued that insects possess the relevant neural hardware required for sentience. Clearly, a better understanding of pain’s unpleasantness and the underlying neural activity will have extremely important implications for our moral obligations to other animals.
Since pain research on nonhuman animals has been a large target of research, one might hope that there would be a great deal of research to draw upon to learn about the unpleasantness of pain. Unfortunately, due to an emphasis on easily reproducible measurements, much of the research has focused on measurements that tell us very little about the affective dimension of pain. Several researchers (Vierck et al. 2008, Roughan et al. 2014, Gregory et al. 2013) have highlighted the fact that many preclinical studies involving animals rely on reflexive responses to pain controlled by neurons in the spinal cord rather than the brain, and as such have done a very poor job predicting the efficacy of various treatments on humans’ experiences of pain, and particularly the affective dimension of pain.
Relatedly, many ethicists and advocates have referenced the fact that many animals, when encountering noxious stimulation, display a similar behavioral repertoire to humans’, and infer from this fact that the animals are in pain. Though the observation of behavioral similarities combined with a principle of erring on the side of caution gives us strong reasons to treat animals as moral subjects, skeptics can object, and with some reason. Common examples of behavioral indicators of pain such as crying, moaning, wincing, and withdrawing from the source of the stimulation are not necessarily connected with the painful experience. For example, humans in vegetative states will sometimes cry out, withdraw, and/or exhibit facial contortions after noxious simulation (Laureys 2007), but these reactions are known to be reflexive. Similarly, many of the behavioral measures of pain in tests on animals, such as tail flicks and paw withdrawal, are known to be mediated by neurons in the spinal cord and don’t require the involvement of the brain, which is typically involved in affective pain. If we can understand the mechanisms that explain pain behavior in the absence of affect, and if we have information about the processes in the brain that are involved in conscious pain processing, we can shift our attention away from those behaviors that do not require unpleasantness and towards other activity that may depend on the conscious experience of unpleasantness to try to determine the essential mechanisms of affective processing.
In humans, the two brain areas that are most consistently activated during a wide variety of pains in imaging scans are the anterior cingulate cortex (ACC) and the insula cortex (along with the adjacent parietal operculum, which appears to be functionally continuous with parts of the posterior insula). Single-unit recordings in humans performed during surgeries, which measure the activity of individual neurons, have demonstrated that the anterior cingulate contains neurons that selectively respond to painful stimuli but not other forms of somatosensory stimulation (Hutchison1999). EEG recordings have also found that the posterior insula responds to painful stimulation (Garcia-Larrea 2012), and direct stimulation of regions of the insula results in pain reactions in humans (Ostrowsky et al. 2002). Research has also shown that selectively enhancing or diminishing the unpleasantness of pain also enhances or diminishes activity in these areas (Rainville et al. 1997, 1999). Moreover, patients with lesions in the ACC or insula have reported feeling pains but no longer being bothered by them (Foltz and White 1962, Berthier et al. 1988). Thus, there is good prima facie evidence that both of these regions play a role in the unpleasantness of pain, or at least of some pains.
It should be noted that for the ACC and for the insula, there are complications with any claims that the area is a “center of pain’s unpleasantness.” For one thing, both areas are involved in a huge number of other processes and emotions, and there are a number of competing hypotheses about what their precise role in cognition is. This worry can be diminished somewhat as the localization claims are made a bit more precise; for example “sadness” is often suggested to be localized in the ACC, but actually tends to occur in an area in front of and below (anterior and inferior in neuroscience speak) the area involved in pain (Vogt 2005). Similarly, the pain processing area of the insula can be kept distinct from other areas of the insula, including those that process gustatory information (Nieuwenhuys 2011). Nevertheless, at the level of precision detectable by our current best brain-imaging techniques, there are no voxels of neural tissue exclusively activated by pain or by unpleasantness.
Since there is good evidence that parts of the insula and ACC are playing some important role related to the unpleasantness of pain in humans, how could it be assessed whether these brain areas, or analogous areas, are playing a similar role in other animals? Given the problem of other minds (Hyslop 2016) and the specific difficulties of assessing mental states in nonlinguistic animals, there is no perfect answer to this question. However, by combining behavioral measures with knowledge of neural similarities and responsiveness to known human analgesics, we can generate plausible answers.
A converging set of evidence has suggested that the anterior cingulate cortex is involved in some affective aspects of pain perception in other mammals. As noted above, studies relying on spinally mediated behaviors have tended to be very poor predictors of the clinical efficacy of pain drugs. However, several authors have presented data arguing that a more successful method can be used based on measurements of escape and avoidance.
Sufka (1994) developed one of the earliest avoidance-based operant conditioning models of the effectiveness of analgesics. On his model, animals exposed to repeated noxious stimuli are confined to one location while under the influence of a particular drug and are confined to a different area, still exposed to the same noxious stimulation, while not under the influence of the drug. The animals are then offered a series of choices between the two locations, and the outcomes of the choices are measured. The rationale is that if animals experience more pain when not under the influence of the analgesic, they will form a negative association with the location, and as such will be more likely to choose the location paired with drugs that are effective analgesics than the other location. Of course, one worry is that because many analgesics also have positive reward properties independent of any pain relief, these tests might simply be measuring the rewarding effects of the drugs, rather than pain relief. However, Sufka later cites a number of studies demonstrating that the conditioned place-aversion effects of pain relief can be dissociated from the place preference caused by the reward value of the drugs, suggesting that a separate mechanism is involved in learning to avoid aversive stimuli (Roughan et al. 2014).
The efficacy of conditioned place preference tasks, however, depends on a crucial assumption, namely that there is a link between the unpleasantness of pain and learning to avoid the pain in the future. Unquestionably, these are conceptually distinct from one another, whether or not they are reliably correlated. As such, it is difficult to evaluate how successful this approach is at indicating the existence of the unpleasantness of pain in other animals.
For this reason, several authors have expanded upon the conditioned place-preference task by also adding an escape component that more closely captures the immediate feeling of unpleasantness (as opposed to a future motivation to avoid cues that were previously paired with noxious stimuli). On these models (Vierk et al. 2008, Morgan et al. 2008, Gregory et al. 2013), animals are offered an opportunity to escape from a potentially noxious environment by moving to a new location. In contrast to reflexive behaviors such as crying out, tail flicks, immediate paw withdrawal, etc., the assumption in these studies is that the animal has to recognize the negative stimulus and then use this information to make a decision to move to a new location. Again, of course, this behavior does not prove the existence of unpleasantness or even conscious pain, since it’s possible that the animals have unconscious mechanisms for motivating behavior (even complicated behavior) away from threatening features of the environment.
Interestingly, however, the effects of opiates and targeted lesions in the ACC on escape and conditioned place preference in nonhuman mammals mirror the dissociation observed in humans. Lesioning the anterior cingulate results in mice who still withdraw from painful stimuli, but no longer choose to escape from areas where the pain should be greater nor learn to avoid these areas (LaGraize et al. 2004). Similarly, giving the rats opioids produces the same dissociation (LaGraize et al. 2006). Thus, there’s at least a prima facie argument by analogy that in most mammals, the affective pain pathways are operating very similarly to how they operate in humans, since damage and activation of similar brain regions results in similar behavioral profiles (Shriver 2006).
Nevertheless, important questions remain. In particular, it’s not clear what brain activity is really necessary for pain affect. One interpretation of the available data is that activity in the network formed by the cingulate and insula, or perhaps one of those brain areas individually, appears to mediate the unpleasantness of pain. One could then claim that only animals who have these brain areas feel the unpleasantness of pain in a manner similar to humans. This, however, would lead to the counterintuitive result that only mammals truly have the affective component of pain, since these brain areas have not been found in other species.
Alternatively, one might instead suggest that there are analogous areas that operate in a similar enough manner to the cingulate and/or insula in other species to generate unpleasantness (Shriver 2016). On this interpretation, the human cingulate and insula have specialized to perform additional operations in humans, but still play a role in the experience of pain that is played by other brain regions in other species. This is plausible, since it appears the insula involves a specialization of pain-perception processes that also exist in a number of other species (Garcia-Larrea 2012, Nieuwenhuys 2011). Moreover, many other species, including birds, fish, reptiles, and possibly even crabs, have been shown to demonstrate conditioned place-preference behaviors.
Nevertheless, we are faced with the problem that neither any one particular measure of behavior, including conditioned place-preference tasks, nor the involvement of any particular brain region, such as the insula, has been shown to reliably indicate the presence or absence of the affective dimension of pain. Only by learning more about the specific way neural activity underlies behaviors associated with pain affect can we hope to abstract the processes involved in causing pain’s unpleasantness. And this, in turn, will require far more research aimed at conceptually understanding the nature of pain affect in humans. For example, though there have been a number of reports of people who “feel pain but don’t mind it,” most notably in cases of pain asymbolia, there has ultimately been very little investigation of what the full behavioral profile of such patients is, and how reliably this profile is linked to damage of specific brain areas. If we could discover that pain affect, but not sensory pain, was necessarily linked to a particular type of learning, or to a certain form of attentional process, this could give us a better target for understanding what precisely needs to be sought out in other species. In particular, if it was demonstrated clearly in humans that the unpleasantness of pain is reliably correlated to escape impulses or conditioning, this would make an important difference in how confidently we could interpret the results from other mammals.
It is only after we have detailed knowledge of the correlations that the real questions of philosophy of mind come in. For example, let’s say we discover that self-reports of unpleasantness in humans turn out to be perfectly correlated with a particular type of neural activity and with a particular behavioral profile. Even then, we can question how we should view the central processes involved. Does the particular type of neuron involved in the activity matter, or does it only matter that certain information was transmitted? Can aspects of the phenomenal character be explained by describing the activity of the neurons, or are we left with only a correlation that is not fully understood? These questions, I believe, can only be fully addressed after a detailed scientific investigation that narrows down the true nature of unpleasantness by precisely determining the neural and behavioral features that reliably correlate with human reports of unpleasantness.
As such, though I think philosophers can usefully discuss these issues in the philosophy of mind and in ethics, the conclusions that can be reached are currently limited by the absence of crucial information from the sciences. My belief is that philosophers’ most useful role in this context at the present, aside from producing arguments about how we ought to interpret limited and uncertain information, is to help think of experiments conceptually clarifying the nature of pain’s unpleasantness, with an eye towards addressing issues of pressing philosophical and social significance.
I envision philosophers and scientists working together as follows: philosophers can be helpful in keeping the focus on important theoretical questions about the nature of experience and the nature of (dis)value, and on how the findings of empirical research can inform a number of practical ethics questions. However, the theorizing of philosophers is limited in at least two significant ways that require contributions from the sciences. First, we don’t yet know how important psychological concepts are related to one another, and how they should best be “lumped” and “split.” For example: is the unpleasantness of pain always accompanied by a motivational signal, or by some other relevant psychological feature? And second, we don’t know how the absence of various features would influence people’s assessments of their own pains: if we were to selectively inhibit the motivational system of a person, how would that influence her interpretation of pain? Thus, I see progress in understanding the unpleasantness of pain as depending upon an ongoing conversation between cognitive scientists and philosophers.
Understanding pain is important for a number of philosophical projects. And the unpleasantness of pain is of particular importance. Though the science of pain has helped us to learn quite a bit about the unpleasant dimension of pain, we still lack crucial information needed to provide complete answers to questions in value theory, applied ethics, and the philosophy of mind.
Given these limitations, the most important role philosophers can be playing is to be collaborating with scientists to help nudge research towards answering some of these questions. Neither a pain science devoted exclusively to chasing clinically relevant results nor philosophers working primarily from intuitions can answer the most important questions about pain on their own. It is only through a collaboration that progress on the most important issues surrounding the unpleasantness of pain will occur.1
1 Thanks to David Bain, Michael Brady, Jennifer Corns, Kristin Andrews, and audiences at the University of Glasgow, York University, the University of Michigan-Flint, Penn State University, and the University of Pennsylvania for helpful comments on this essay.
See Colin Allen’s “Animal Pain” (2004); Chapter 5 of Gary Varner’s Personhood, Ethics, and Animal Cognition (2012); and Victoria Braithwaite’s Do Fish Feel Pain (2010) for interesting discussions of these issues.
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