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Understanding How Opioids Contribute to Reward and Analgesia

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Understanding How Opioids Contribute to Reward and Analgesia Understanding How Opioids Contribute to Reward and Analgesia Howard L. Fields, M.D., Ph.D. Opioids acting at the mu opioid (MOP) receptor produce powerful analgesia. They also produce an intensely rewarding effect that can lead to addiction. The analgesic effect of MOP receptor agonists derives from a direct inhibitory effect on pain transmission at the spinal-cord level and through activation of a descending pain- modulatory pathway. The rewarding effect of MOP agonists is the result of their actions in the mesostriatal dopamine pathway classically associated with both natural and drug rewards. Both the analgesic and rewarding effect of MOP agonists are best understood in the context of decision making under conditions of conflict. Pain is one of many competing motivational states, and endogenous opioids suppress responses to noxious stimuli in the presence of conflicting motivations, such as hunger or a threatening predator. When a food reward is available, MOP agonists microinjected into the mesostriatal circuit promote its consumption, while concomitantly suppressing responses to noxious stimulation. The mesostriatal “reward” circuit, thus, appears to perform a function critical to decision making and can either amplify or suppress responses to noxious stimuli. Reg Anesth Pain Med 2007;32:242-246. Key Words: Morphine, Pain modulation, Accumbens, Medulla, Periaqueductal gray, Threat, Palatability. ecause pain is ubiquitous and is associated with play a major role in determining what an individual Brobust objective and subjective responses, it experiences. Clinicians who see patients with long- has been conceptualized in many different ways. standing pain problems are often struck by exacer- One broadly accepted concept is that pain is the bations and remissions in the severity of the pa- sensation that results from somatic stimuli of suffi- tient’s pain that are independent of objective cient intensity to threaten tissue damage (see Sher- changes in a peripheral pathologic process. To the rington, p. 2291). According to this view, the rele- contrary, these fluctuations in pain level are often vant events for understanding pain revolve around correlated with life stresses or changes in mood. the properties of the noxious stimulus. Because Some painful conditions (e.g., migraine headache stimulus intensity typically correlates with the like- or fibromyalgia) have no identified tissue-damaging lihood of significant tissue injury, this view has process. The opposite also occurs; individuals (ath- been affirmed by careful psychophysical studies letes during a competition or soldiers in battle4,5) that demonstrate human reports of perceived pain commonly sustain a significant acute injury without intensity are a robust and reproducible function of experiencing any immediate pain. Furthermore, pla- 2 stimulus intensity. Furthermore, when one studies cebo treatment often gives potent analgesia.6,7 the neurons of the afferent pathways that mediate These seemingly disparate observations show pain sensation, their firing rate is also a reliable that a comprehensive framework for understanding 3 function of stimulus intensity. pain must encompass not only the reliable re- These study results are all well and good; how- sponses to controlled stimuli observed in the psy- ever, in the real world, when tissue injuries occur, chophysical laboratory but also the perplexing vari- factors other than the properties of the stimulus ability that is seen by physicians in clinical practice. An important step toward such a comprehensive From the Departments of Neurology and Physiology, Univer- view begins by asking the following question: What sity of California, San Francisco, CA. biological purpose could possibly be served by hav- Accepted for publication January 10, 2007. ing such variable responses to similar tissue-dam- Presented at the 2006 Bonica Lecture, 2006 American Society of Regional Anesthesia and Pain Medicine Fall Pain Meeting, aging stimuli? One simplifying framework that November 18, 2006, San Francisco, CA. moves us in that direction is to consider that pain is Reprint requests: Howard L. Fields, M.D., Ph.D., Department of Neurology, University of California, 5858 Horton Ave, Suite just one of the many motivations that determine 200, Emeryville, CA 94608. E-mail: [email protected] the behavior of an individual. Within this larger © 2007 by the American Society of Regional Anesthesia and framework, pain can be conceptualized as a moti- Pain Medicine. 1098-7339/07/3203-0012$32.00/0 vation that often occurs in the setting of other doi:10.1016/j.rapm.2007.01.001 conflicting motivations. For example, consider that 242 Regional Anesthesia and Pain Medicine, Vol 32, No 3 (May–June), 2007: pp 242–246 Understanding Opioid Contributions • Fields 243 you are hanging on a ledge by your fingers, the pain spinal cord.3 When active, the spinal-cord terminals in your hands and arms is growing, but if you let go, of primary afferent nociceptors release glutamate, the consequences are extreme, so survival demands and many also corelease a peptidergic neurotrans- that you tolerate much greater pain. Consider a less mitter. These neurotransmitters combine to pro- extreme example: You are sitting in an uncomfort- duce prolonged firing of the second-order and able chair. However, dessert is about to be served, third-order neurons in the dorsal horn. Activity in and it is your favorite. Chances are, you will endure these spinal-cord projection neurons then propa- the discomfort a little while longer. gates to the brain stem and thalamus, where their Ethologists and experimental psychologists have axons terminate. The brain-stem and thalamic neu- studied such conflict situations in simplified form in rons that receive the nociceptive message from the animals. They have demonstrated that behavioral spinal cord project to a variety of forebrain struc- responses to pain can be suppressed under a variety tures, including the amygdala, the hypothalamus, of conditions; for example, during micturition,8 in and the somatosensory, anterior cingulate, and in- the presence of a predator, or when confined to an sular cortices.14,15 Imaging studies have shown ro- environment in which severe pain has previously bust correlations between stimulus intensity, acti- been experienced.9,10 Pain responses are also sup- vation of these cortical areas, and patient reports of pressed in situations in which rodents anticipate pain.16 reward.11 Under many circumstances, such sup- Opioids control the pain-transmission pathway pression of pain responses can be prevented by directly through actions in the superficial layers of administration of nonselective opioid-receptor an- the dorsal horn.17 Both primary afferent terminals tagonists such as naloxone. Interestingly, in this and second-order dorsal-horn neurons bear mu regard, placebo analgesia can also be reversed by opioid (MOP) and delta opioid (DOP) receptors.18 naloxone.7,12 This finding indicates that endoge- Spinal application of MOP agonists reduces excita- nous opioids are a key signaling molecule for pain tory neurotransmitter release from primary afferent suppression and that pain suppression often occurs terminals by inhibiting a voltage-gated calcium in clinical situations in which the patient believes a channel.19,20 Opioids also directly depolarize sec- treatment effective for pain has been given. ond-order dorsal-horn neurons by opening an in- This critical role of endogenous opioids in pain wardly rectifying potassium channel.21 These ac- suppression provides an important insight about tions of opioids in the dorsal horn make a major the biology of opioid analgesics. Opioid analgesics contribution to the clinical efficacy of spinal appli- such as morphine do not simply inhibit pain-trans- cation of MOP agonists such as morphine. mission pathways; they mimic the action of endog- enous opioids that are released in response to specific Opioids and Pain-Modulatory Systems conflict situations; that is, when a noxious stimulus is present, but a compelling reason exists to avoid Although spinal opioids are highly effective for responding. These compelling reasons include the pain relief, the opioid story has much more to it. threat of even greater injury or death or the possible Very early on, investigators discovered that su- loss of some highly desired reward. In this article, I praspinal sites contribute to the analgesic effect of will briefly describe current views of where and systemically administered opioids.17 In fact, careful how opioids act to reduce responses to pain. mapping of the forebrain by microinjection of MOPs showed very significant hot spots for analge- The Pain Sensory System and Spinal sia in cortex, hypothalamus, midbrain periaqueduc- tal gray (PAG) matter, and rostral ventromedial Opioid Analgesia medulla (RVM).17,22,23 Furthermore, either lesions Throughout the body are primary afferent noci- or microinjection of opioid antagonists into some of ceptors with terminals that contain receptor mole- these same sites blocked the analgesic effect of sys- cules sensitive to mechanical deformation, temper- temic MOPs. These studies demonstrated that when ature extremes, lowering of pH, and a variety of morphine is given systemically, it acts in a distrib- activating substances released by inflammation or uted and simultaneous manner at multiple su- other pathologic processes.13 With appropriate praspinal sites. Furthermore, cutting the dorsolat- stimuli, these receptor molecules depolarize the pe- eral funiculus of the spinal
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