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A Common Neurobiology for Pain and Pleasure

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A Common Neurobiology for Pain and Pleasure PERS P ECTIVES religions, are often used to guide the balance SCIENCE & SOCIETY between seeking pleasure and avoiding pain (BOX 2). The subjective utility — or ‘mean- A common neurobiology for pain ing’ — of pain or pleasure for the individual is determined by sensory, homeostatic, cultural and other factors that, when com- and pleasure bined, bias the hedonic experience of pain or pleasure. Siri Leknes and Irene Tracey The Motivation-Decision Model Abstract | Pain and pleasure are powerful motivators of behaviour and have The processes that underlie the subjective historically been considered opposites. Emerging evidence from the pain and interpretation of a sensory event can be reward research fields points to extensive similarities in the anatomical substrates understood as the manifestation of an of painful and pleasant sensations. Recent molecular-imaging and animal studies unconscious decision process4,14. The deci- have demonstrated the important role of the opioid and dopamine systems sion process requires information about in modulating both pain and pleasure. Understanding the mutually inhibitory the homeostatic state of the individual (such as inflammation or hunger), sensory effects that pain and reward processing have on each other, and the neural input and knowledge about impending mechanisms that underpin such modulation, is important for alleviating threats and available rewards. According unnecessary suffering and improving well-being. to the Motivation-Decision Model of pain, as put forward by Fields4,14, the basic premise for the decision process is that “Nature has placed mankind under the The utility of pain and pleasure anything that is potentially more important governance of two sovereign masters, pain The large variability between the strength of for survival than pain should exert anti- and pleasure.” — Jeremy Bentham a sensory stimulus and the resulting hedonic nociceptive effects. This allows the animal feeling is of great medical and neuroscien- to ignore the pain and attend to the more Most of what is known about pain and tific interest. For instance, athletes can be important event. The Motivation-Decision pleasure derives from the study of each oblivious to pain in the heat of competition, Model predicts that pain–pleasure dilem- phenomenon in isolation. Recently, however, in which winning is the reward. A key factor mas in which a large reward is gained neuroscientists investigating opioid and for the interpretation of pain and pleasure is at the price of a small pain are resolved placebo analgesia1–3, drug addiction4 and subjective utility7. For example, the reward through the antinociceptive effects of learning5 have begun to bridge the gap value of a stimulus increases with the effec- the pleasurable reward (FIG. 1). In some between the pain and pleasure research tiveness of that stimulus in restoring bodily instances, threatening and pleasure-related fields. This development has been equilibrium (homeostasis)6,8. This effect, cues are more important for survival than strengthened by the increasing focus on known as alliesthesia6, is well-documented pain, and it is assumed that any antinocic- the subjective emotional feelings for food rewards, which are more pleasur- eptive effects are mediated by the descend- (hedonics) that are elicited by rewards able when they relieve a hunger state9. ing pain modulatory system, which is and punishments (BOX 1). As the experience of pain represents a located in the brainstem. This circuit, which Rewards and punishments are defined deviation from homeostatic balance10, the consists of excitatory and inhibitory cells, as something that an animal will work to same principle can be applied to pain and communicates with neurons in the pre- achieve or avoid, respectively. Pleasure the pleasantness of its relief 11. Similarly, frontal cortex, the hypothalamus and the represents the subjective hedonic value of when a perceived threat to an organism amygdala to control the nociceptive affer- rewards. The term ‘pain’ encompasses both becomes greater, pain unpleasantness ent pathway in the spinal and trigeminal the hedonic (suffering) and motivational increases, enhancing defensive and dorsal horn4,14,15 (FIG. 2). Opiate drugs and (avoidance) aspects of a painful experience. avoidance mechanisms12. endogenous opioids act on this descending Clearly, seeking pleasure and avoiding pain Pain and pleasure encourage the constant system to produce pharmacological, pla- is important for survival, and these two optimization of our internal homeostatic cebo, stress-induced and pleasure-related motivations probably compete for prefer- balance. Although pleasure-seeking and analgesia1,2,4,14–20. ence in the brain. Put simply, which of two pain-avoidance generally increase our coinciding pain and pleasure events should chances for survival, it is easy to envisage Pain–pleasure interactions be processed and acted on first? Consistent scenarios in which these two motivations Evidence of pleasure-related analgesia with the idea that a common currency of are in competition. A simple case would has been reported in various human and emotion6 enables the comparison of pain involve a large reward that is only accessible animal studies: pain is decreased by pleas- and pleasure in the brain, the evidence at the ‘price’ of a small pain. Sometimes it ant odours21, images22, pleasurable music23, reviewed here points to there being exten- seems that overcoming a small amount palatable food16,17 and sexual behaviour18,19. sive overlap in the neural circuitry and of pain might even enhance the pleasure, In addition, considerable evidence suggests chemistry of pain and pleasure processing as reflected perhaps by the common that expectation of treatment effect, which at the systems level. This article summarizes expression ‘no pain, no gain’ or the pleasure contributes to placebo analgesia, is a type of current research on pain–pleasure interac- of eating hot curries. Pain–pleasure dilem- reward expectation24,25. Interestingly, when tions and the consequences for human mas abound in social environments13, and subjects who were not expecting an injec- behaviour. culture-specific moral systems, such as tion of pain-relieving morphine received 314 | apriL 2008 | VOLUme 9 www.nature.com/reviews/neuro © 2008 Nature Publishing Group PERS P ECTIVES Box 1 | The increasing focus on pain and reward hedonics access to our own hedonic and motivational processes, which are thought to be primarily Hedonic feelings — also known as qualia — subconscious31. Importantly, however, the drive motivation and behaviour. Qualia motivation and hedonic subsystems seem to determine what it is like to be a human being87. No theory of the relationship between the be mediated by different neurotransmitters. brain and the mind is complete without Carefully controlled studies have found accounting for hedonic feelings. In recent specific effects for two neurotransmitter years, several exciting research directions have systems: dopamine increases motivation emerged in the pain and reward research fields for, but not the pleasure of, eating palatable that successfully combine the need for foods32,33, whereas the opioid system influ- carefully controlled, ‘objective’ research ences motivation indirectly by modulating methodologies with a focus on hedonics. One subjective emotional feelings of pain and example is a body of work on ‘liking’ and reward34. In summary, opioids are neces- ‘wanting’ — two subconscious reward sary for hedonic experience (‘liking’) but processes that are thought to underpin conscious pleasure and motivation31. Using taste reactivity as a primary outcome measure (see dopamine motivates you to get ready for it Nature Reviews | Neuroscience 31,35 figure), this research has used pharmacological stimulation and lesion techniques to determine (‘wanting’) . causal relationships between neuronal signalling and hedonic feelings. In the pain field there is µ-opioids have been shown to cause a growing recognition that the ‘subjective interpretation’ or ‘meaning’ of pain determines the positive shift in affect across the hedonic amount of pain-related suffering15,88. The definition of pain, according to the International spectrum: they enhance the pleasantness of Association for the Study of Pain, emphasizes the ‘unpleasant’ and ‘emotional’ aspects, and also sweet tastes and decrease the aversiveness includes subjective feelings of pain, which are not caused by tissue damage. Other research of pain and bitter foods31. Both painful and 89 areas that are turning their attention to hedonic feelings include the fields of obesity research pleasant events are associated with the and decision making: the shift in focus from ‘cold’ rational consideration to ‘hot’ emotion-based release of endogenous µ-opioids in decision making has influenced cognitive neuroscience for more than a decade90,91. Even the brain and, importantly, in the NAc19,36 economists are now looking to hedonic feelings to explain human behaviour such as the ‘warm (FIG. 1). Blocking of µ-opioid signalling glow’ that accompanies donations to charity92. Figure modified, with permission, from REF. 31 (2003) Academic Press. with naloxone decreases the pleasantness of food rewards34 and sexual behaviour37 and reverses reward-related analgesia16,18,26. a hidden injection, its analgesic effects Opioids and hedonic feelings Interestingly, a recent conditional gene- were significantly reduced26. Although the Pain and reward are complex constructs knockout
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