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Dopamine in Drug Abuse and Addiction: Results of Imaging

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Dopamine in Drug Abuse and Addiction: Results of Imaging NEUROLOGICAL REVIEW Dopamine in Drug Abuse and Addiction Results of Imaging Studies and Treatment Implications Nora D. Volkow, MD; Joanna S. Fowler, PhD; Gene-Jack Wang, MD; James M. Swanson, PhD; Frank Telang, MD maging studies have provided new insights on the role of dopamine (DA) in drug abuse and addiction in the human brain. These studies have shown that the reinforcing effects of drugs of abuse in human beings are contingent not just on DA increases per se in the striatum (in- cluding the nucleus accumbens) but on the rate of DA increases. The faster the increases, the Imore intense the reinforcing effects. They have also shown that elevated levels of DA in the dorsal striatum are involved in the motivation to procure the drug when the addicted subject is exposed to stimuli associated with the drug (conditioned stimuli). In contrast, long-term drug use seems to be associated with decreased DA function, as evidenced by reductions in D2 DA receptors and DA re- lease in the striatum in addicted subjects. Moreover, the reductions in D2 DA receptors in the stria- tum are associated with reduced activity of the orbitofrontal cortex (region involved with salience at- tribution and motivation and with compulsive behaviors) and of the cingulate gyrus (region involved with inhibitory control and impulsivity), which implicates deregulation of frontal regions by DA in the loss of control and compulsive drug intake that characterizes addiction. Because DA cells fire in response to salient stimuli and facilitate conditioned learning, their activation by drugs will be expe- rienced as highly salient, driving the motivation to take the drug and further strengthening condi- tioned learning and producing automatic behaviors (compulsions and habits). Arch Neurol. 2007;64(11):1575-1579 Dopamine (DA) is the neurotransmitter that brain regions (limbic, cortical, and stria- has been classically associated with the re- tal) it modulates. inforcing effects of drugs of abuse and may Herein, we summarize findings from have a key role in triggering the neurobio- imaging studies that used positron emis- logical changes associated with addiction. sion tomography (PET) to investigate the This notion reflects the fact that all of the role of DA in the reinforcing effects of drugs, drugs of abuse increase the extracellular con- the long-term brain changes in drug- centration of DA in the nucleus accum- addicted subjects, and the vulnerability to bens. Increases in DA levels have an impor- addiction. Though most of the PET stud- tant role in coding reward and prediction ies on addiction have focused on DA, it is of reward, in the motivational drive to pro- clear that drug-induced adaptations in other cure the reward, and in facilitating learn- neurotransmitters (ie, glutamate, ␥-amino- ing.1 It is also believed that DA codes not butyric acid, opioids, and cannabinoids) are just for reward but for saliency, which, in also involved, but the lack of radioligands addition to reward, includes aversive, novel, has limited their investigation. and unexpected stimuli. The diversity of DA effects is likely translated by the specific ROLE OF DA ON THE REINFORCING EFFECTS Author Affiliations: National Institute on Drug Abuse (Dr Volkow) and National OF DRUGS IN THE HUMAN BRAIN Institute on Alcohol Abuse and Alcoholism (Drs Volkow and Telang), Bethesda, Maryland; Medical Department, Brookhaven National Laboratory, Upton, New The effects of short-term drug exposure York (Drs Fowler and Wang); and Department of Pediatrics, University of on extracellular DA concentrations in the California, Irvine (Dr Swanson). human brain can be studied using PET and (REPRINTED) ARCH NEUROL / VOL 64 (NO. 11), NOV 2007 WWW.ARCHNEUROL.COM 1575 ©2007 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 tration per se that was associated with getting high.5 The Table 1. Summary of Findings of PET Studies Comparing dependency of the reinforcing effects of drugs on brain Various Targets Involved in DA Neurotransmission Between pharmacokinetic properties suggests a possible associa- Substance Abusersa and Non–Drug-Abusing Control Subjects for Which Statistical Differences Between tion with phasic DA cell firing (fast-burst firing at fre- the Groups Were Identifiedb quencies Ͼ30 Hz), which also leads to fast changes in DA concentration and whose function is to highlight the 6 Target Investigated Drug Used Finding saliency of stimuli. This is in contrast to tonic DA cell D2 DA receptors Cocaine ↓ Acute withdrawal firing (slow firing at frequencies around 5 Hz), which ↓ Detoxified maintains baseline steady-state DA levels and whose func- Alcohol ↓ Acute withdrawal tion is to set the overall responsiveness of the DA sys- ↓ Detoxified tem. This led us to speculate that drugs of abuse induce Methamphetamine ↓ Detoxified changes in DA concentration that mimic but exceed those Heroin ↓ Active user produced by phasic DA cell firing. DA transporters Cocaine ↑ Acute withdrawal 0 Detoxified Alcohol ↓ Acute withdrawal ROLE OF DA ON THE LONG-TERM EFFECTS 0 Detoxified OF DRUGS OF ABUSE IN THE HUMAN BRAIN: Methamphetamine ↓ Detoxified INVOLVEMENT IN ADDICTION Cigarettes 0 Active user Vesicular transporters-2 Methamphetamine ↓ Detoxified Synaptic increases in DA concentration occur during drug ↓ Metabolism (MAOB) Cigarettes Active user intoxication in both addicted and nonaddicted subjects. Synthesis (dopa Cocaine ↓ Detoxified decarboxylase) Alcohol 0 Detoxified However, a compulsive drive to continue drug taking DA releasec Cocaine ↓ Detoxified when exposed to the drug is not triggered in all sub- Alcohol ↓ Detoxified jects. Inasmuch as it is the loss of control and the com- pulsive drug taking that characterizes addiction, the short- Abbreviations: DA, dopamine; MAOB, monoamine oxidase B; PET, positron term drug-induced DA level increase alone cannot explain emission tomography; arrows correspond to lower values (↓) and higher this condition. Because drug addiction requires long- values (↑) than in non–drug-abusing control subjects; 0 indicates no statistical difference. term drug administration, we suggest that in vulnerable a Tested during acute withdrawal, detoxification, or active use. individuals (because of genetic, developmental, or envi- b Differences were reported in the striatum for all DA targets except MAOB, ronmental factors), addiction is related to the repeated for which changes were reported throughout the entire brain (cortical and subcortical areas). perturbation of DA-regulated brain circuits involved with c DA release was assessed by measuring changes in specific binding of reward/saliency, motivation/drive, inhibitory control/ raclopride labeled with carbon 11 induced by pharmacologic challenge with executive function, and memory/conditioning. Herein, methylphenidate or amphetamine. we discuss findings from imaging studies on the nature of these changes. Many radioactive tracers have been used to assess D2 DA receptor radioactive ligands that are sensitive to changes in targets involved in DA neurotransmission competition with endogenous DA, such as raclopride la- (Table 1). Using 18-N-methylspiroperidol or [11C]ra- beled with carbon 11 (11C). The relationship between the clopride, we and others have shown that subjects with a effects of drugs on DA and their reinforcing properties wide variety of drug addictions (cocaine, heroin, alco- in the human brain (assessed by self-reports of “high” hol, and methamphetamine) have significant reduc- and “euphoria”) was studied for the stimulant drugs meth- tions in D2 DA receptor availability in the striatum (in- ylphenidate and amphetamine. Methylphenidate, like co- cluding the ventral striatum) that persist months after caine, increases DA by blocking DA transporters, whereas protracted detoxification (reviewed in Volkow et al2). We amphetamine, like methamphetamine, increases DA by have also revealed evidence of decreased DA cell activ- releasing it from the terminal via DA transporters. Intra- ity in cocaine abusers. Specifically, we showed that the venous methylphenidate (0.5 mg/kg) and amphetamine striatal increases in DA level induced by intravenous meth- (0.3 mg/kg) increased the extracellular DA concentra- ylphenidate (assessed with [11C]raclopride) in cocaine tion of DA in the striatum, and these increases were as- abusers were substantially blunted when compared with sociated with increases in self-reports of high and eu- DA level increases in control subjects (50% lower).7 Be- phoria.2 In contrast, when given orally, methylphenidate cause DA concentration increases induced by methyl- (0.75-1 mg/kg) also increased DA but was not perceived phenidate are dependent on DA release, a function of DA as reinforcing.3 Because intravenous administration leads cell firing, we speculated that this difference likely re- to fast DA changes, whereas oral administration in- flects decreased DA cell activity in the cocaine abusers. creases DA slowly, the failure to observe the high with Similar findings have been reported in alcohol abusers.8 oral methylphenidate likely reflects its slow pharmaco- These brain-imaging studies suggest 2 abnormalities kinetics. Indeed, the speed at which drugs of abuse en- in addicted subjects that would result in decreased out- ter the brain is recognized as affecting their reinforcing put of DA circuits related to reward; that is, decreases in effects.4 This association has also been shown in PET stud- D2 DA receptors and decreases in DA release in the stria-
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