Illicit dopamine transients: Reconciling actions of abused drugs

Trends in Neurosciences

Volumn 37, Issue 4, 2014, Pages 200-210

  Covey, Dan P ^a   Roitman, Mitchell F ^b   Garris, Paul A ^a  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; COCAINE; DOPAMINE; DOPAMINE TRANSPORTER; ILLICIT DRUG; METHAMPHETAMINE; METHYLPHENIDATE; PSYCHOSTIMULANT AGENT; STREET DRUG;

APPETITE; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC NERVE CELL; DRUG ABUSE; DRUG BIOAVAILABILITY; DRUG CLASSIFICATION; DRUG SELF ADMINISTRATION; HUMAN; LONG TERM POTENTIATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; REVIEW; REWARD; SENSORY SYSTEM; SIGNAL TRANSDUCTION; STATE DEPENDENT LEARNING; UPREGULATION; BRAIN; DOPAMINE BRAIN LEVEL; DRUG MECHANISM; REINFORCEMENT; ADDICTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINERGIC NEURONS; HUMANS; MODELS, NEUROLOGICAL; STREET DRUGS; SUBSTANCE-RELATED DISORDERS;

EID: 84897406963     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2014.02.002     Document Type: Review

References (130)

1. Di Chiara G., Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:5274-5278.
2. Mogenson G.J., et al. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 1980, 14:69-97.
3. Goto Y., Grace A.A. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat. Neurosci. 2005, 8:805-812.
4. Luscher C., Ungless M.A. The mechanistic classification of addictive drugs. PLoS Med. 2006, 3:e437.
5. Sulzer D. How addictive drugs disrupt presynaptic dopamine neurotransmission. Neuron 2011, 69:628-649.
6. Hyman S.E., et al. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 2006, 29:565-598.
7. Willuhn I., et al. Dopamine signaling in the nucleus accumbens of animals self-administering drugs of abuse. Curr. Top. Behav. Neurosci. 2010, 3:29-71.
8. Dreyer J.K., et al. Influence of phasic and tonic dopamine release on receptor activation. J. Neurosci. 2010, 30:14273-14283.
9. Lammel S., et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 2012, 491:212-217.
10. Robinson D.L., et al. Monitoring rapid chemical communication in the brain. Chem. Rev. 2008, 108:2554-2584.
11. Schultz W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 2007, 30:259-288.
12. Fiorillo C.D., et al. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 2003, 299:1898-1902.
13. Tobler P.N., et al. Adaptive coding of reward value by dopamine neurons. Science 2005, 307:1642-1645.
14. Gan J.O., et al. Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine. Nat. Neurosci. 2010, 13:25-27.
15. Wanat M.J., et al. Delays conferred by escalating costs modulate dopamine release to rewards but not their predictors. J. Neurosci. 2010, 30:12020-12027.
16. Reynolds J.N., et al. A cellular mechanism of reward-related learning. Nature 2001, 413:67-70.
17. Arbuthnott G.W., Wickens J. Space, time and dopamine. Trends Neurosci. 2007, 30:62-69.
18. Fiorillo C.D. Two dimensions of value: dopamine neurons represent reward but not aversiveness. Science 2013, 341:546-549.
19. Flagel S.B., et al. A selective role for dopamine in stimulus-reward learning. Nature 2011, 469:53-57.
20. Berridge K.C. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl.) 2007, 191:391-431.
21. Zweifel L.S., et al. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:7281-7288.
22. Tsai H.C., et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 2009, 324:1080-1084.
23. Witten I.B., et al. Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 2011, 72:721-733.
24. Wall V.Z., et al. A behavioral genetics approach to understanding D1 receptor involvement in phasic dopamine signaling. Mol. Cell. Neurosci. 2011, 46:21-31.
25. Cheer J.F., et al. Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. J. Neurosci. 2004, 24:4393-4400.
26. Cheer J.F., et al. Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J. Neurosci. 2007, 27:791-795.
27. Robinson D.L., et al. Disparity between tonic and phasic ethanol-induced dopamine increases in the nucleus accumbens of rats. Alcohol. Clin. Exp. Res. 2009, 33:1187-1196.
28. Aragona B.J., et al. Preferential enhancement of dopamine transmission within the nucleus accumbens shell by cocaine is attributable to a direct increase in phasic dopamine release events. J. Neurosci. 2008, 28:8821-8831.
29. Robinson D.L., et al. Frequency of dopamine concentration transients increases in dorsal and ventral striatum of male rats during introduction of conspecifics. J. Neurosci. 2002, 22:10477-10486.
30. Stuber G.D., et al. Extinction of cocaine self-administration reveals functionally and temporally distinct dopaminergic signals in the nucleus accumbens. Neuron 2005, 46:661-669.
31. Stuber G.D., et al. Rapid dopamine signaling in the nucleus accumbens during contingent and noncontingent cocaine administration. Neuropsychopharmacology 2005, 30:853-863.
32. Porter-Stransky K.A., et al. Cocaine must enter the brain to evoke unconditioned dopamine release within the nucleus accumbens shell. Neurosci. Lett. 2011, 504:13-17.
33. Wise R.A., Kiyatkin E.A. Differentiating the rapid actions of cocaine. Nat. Rev. Neurosci. 2011, 12:479-484.
34. Phillips P.E., et al. Subsecond dopamine release promotes cocaine seeking. Nature 2003, 422:614-618.
35. Aragona B.J., et al. Regional specificity in the real-time development of phasic dopamine transmission patterns during acquisition of a cue-cocaine association in rats. Eur. J. Neurosci. 2009, 30:1889-1899.
36. Brown H.D., et al. Primary food reward and reward-predictive stimuli evoke different patterns of phasic dopamine signaling throughout the striatum. Eur. J. Neurosci. 2011, 34:1997-2006.
37. Schultz W. Potential vulnerabilities of neuronal reward, risk, and decision mechanisms to addictive drugs. Neuron 2011, 69:603-617.
38. Redish A.D. Addiction as a computational process gone awry. Science 2004, 306:1944-1947.
39. Ciccocioppo R., et al. Stimuli associated with a single cocaine experience elicit long-lasting cocaine-seeking. Nat. Neurosci. 2004, 7:495-496.
40. Wightman R.M., et al. Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens. Eur. J. Neurosci. 2007, 26:2046-2054.
41. Schank J.R., et al. Dopamine beta-hydroxylase knockout mice have alterations in dopamine signaling and are hypersensitive to cocaine. Neuropsychopharmacology 2006, 31:2221-2230.
42. Daberkow D.P., et al. Amphetamine paradoxically augments exocytotic dopamine release and phasic dopamine signals. J. Neurosci. 2013, 33:452-463.
43. Koulchitsky S., et al. Differential effects of cocaine on dopamine neuron firing in awake and anesthetized rats. Neuropsychopharmacology 2012, 37:1559-1571.
44. Shi W.X., et al. Psychostimulants induce low-frequency oscillations in the firing activity of dopamine neurons. Neuropsychopharmacology 2004, 29:2160-2167.
45. Shi W.X., et al. Dual effects of D-amphetamine on dopamine neurons mediated by dopamine and nondopamine receptors. J. Neurosci. 2000, 20:3504-3511.
46. Park J., et al. In vivo voltammetric monitoring of catecholamine release in subterritories of the nucleus accumbens shell. Neuroscience 2010, 169:132-142.
47. Paladini C.A., et al. Amphetamine selectively blocks inhibitory glutamate transmission in dopamine neurons. Nat. Neurosci. 2001, 4:275-281.
48. Brown M.T., et al. Drug-driven AMPA receptor redistribution mimicked by selective dopamine neuron stimulation. PLoS ONE 2010, 5:e15870.
49. Kalivas P.W., Duffy P. D1 receptors modulate glutamate transmission in the ventral tegmental area. J. Neurosci. 1995, 15:5379-5388.
50. Bocklisch C., et al. Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science 2013, 341:1521-1525.
51. Ingram S.L., et al. Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat. Neurosci. 2002, 5:971-978.
52. Branch S.Y., Beckstead M.J. Methamphetamine produces bidirectional, concentration-dependent effects on dopamine neuron excitability and dopamine-mediated synaptic currents. J. Neurophysiol. 2012, 108:802-809.
53. Jones S.R., et al. Different effects of cocaine and nomifensine on dopamine uptake in the caudate-putamen and nucleus accumbens. J. Pharmacol. Exp. Ther. 1995, 274:396-403.
54. Kile B.M., et al. Synapsins differentially control dopamine and serotonin release. J. Neurosci. 2010, 30:9762-9770.
55. Ramsson E.S., et al. High doses of amphetamine augment, rather than disrupt, exocytotic dopamine release in the dorsal and ventral striatum of the anesthetized rat. J. Neurochem. 2011, 119:1162-1172.
56. Covey D.P., et al. Amphetamine elicits opposing actions on readily releasable and reserve pools for dopamine. PLoS ONE 2013, 8:e60763.
57. Venton B.J., et al. Cocaine increases dopamine release by mobilization of a synapsin-dependent reserve pool. J. Neurosci. 2006, 26:3206-3209.
58. Oleson E.B., et al. Real-time voltammetric detection of cocaine-induced dopamine changes in the striatum of freely moving mice. Neurosci. Lett. 2009, 467:144-146.
59. Chadchankar H., et al. Methylphenidate modifies overflow and presynaptic compartmentalization of dopamine via an alpha-synuclein-dependent mechanism. J. Pharmacol. Exp. Ther. 2012, 341:484-492.
60. Avelar A.J., et al. Amphetamine augments vesicular dopamine release in the dorsal and ventral striatum through different mechanisms. J. Neurochem. 2013, 125:373-385.
61. John C.E., Jones S.R. Voltammetric characterization of the effect of monoamine uptake inhibitors and releasers on dopamine and serotonin uptake in mouse caudate-putamen and substantia nigra slices. Neuropharmacology 2007, 52:1596-1605.
62. Krasnova I.N., et al. Methamphetamine self-administration is associated with persistent biochemical alterations in striatal and cortical dopaminergic terminals in the rat. PLoS ONE 2010, 5:e8790.
63. Brown J.M., et al. Cocaine-induced increases in vesicular dopamine uptake: role of dopamine receptors. J. Pharmacol. Exp. Ther. 2001, 298:1150-1153.
64. Sandoval V., et al. Methylphenidate redistributes vesicular monoamine transporter-2: role of dopamine receptors. J. Neurosci. 2002, 22:8705-8710.
65. Volz T.J., et al. Methylphenidate administration alters vesicular monoamine transporter-2 function in cytoplasmic and membrane-associated vesicles. J. Pharmacol. Exp. Ther. 2007, 323:738-745.
66. Riddle E.L., et al. Therapeutic doses of amphetamine and methylphenidate selectively redistribute the vesicular monoamine transporter-2. Eur. J. Pharmacol. 2007, 571:25-28.
67. Volz T.J., et al. Methylphenidate-induced increases in vesicular dopamine sequestration and dopamine release in the striatum: the role of muscarinic and dopamine D2 receptors. J. Pharmacol. Exp. Ther. 2008, 327:161-167.
68. Mundorf M.L., et al. Amine weak bases disrupt vesicular storage and promote exocytosis in chromaffin cells. J. Neurochem. 1999, 73:2397-2405.
69. Rothman R.B., et al. Dopamine transport inhibitors based on GBR12909 and benztropine as potential medications to treat cocaine addiction. Biochem. Pharmacol. 2008, 75:2-16.
70. Schmitt K.C., et al. Non-classical pharmacology of the dopamine transporter: atypical inhibitors, allosteric modulators and partial substrates. J. Pharmacol. Exp. Ther. 2013, 346:2-10.
71. Jones S.R., et al. Effect of moderate ethanol dose on dopamine uptake in rat nucleus accumbens in vivo. Synapse 2006, 60:251-255.
72. Holden J.M., Peoples L.L. Effects of acute amphetamine exposure on two kinds of Pavlovian approach behavior. Behav. Brain Res. 2010, 208:270-273.
73. Sombers L.A., et al. Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J. Neurosci. 2009, 29:1735-1742.
74. Maskos U., et al. Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 2005, 436:103-107.
75. Mansvelder H.D., et al. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 2002, 33:905-919.
76. Tolu S., et al. Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement. Mol. Psychiatry 2013, 18:382-393.
77. Morikawa H., Morrisett R.A. Ethanol action on dopaminergic neurons in the ventral tegmental area: interaction with intrinsic ion channels and neurotransmitter inputs. Int. Rev. Neurobiol. 2010, 91:235-288.
78. Xiao C., et al. Ethanol facilitates glutamatergic transmission to dopamine neurons in the ventral tegmental area. Neuropsychopharmacology 2009, 34:307-318.
79. Ungless M.A., et al. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 2001, 411:583-587.
80. Saal D., et al. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 2003, 37:577-582.
81. Oleson E.B., et al. Endocannabinoids shape accumbal encoding of cue-motivated behavior via CB1 receptor activation in the ventral tegmentum. Neuron 2012, 73:360-373.
82. Lupica C.R., Riegel A.C. Endocannabinoid release from midbrain dopamine neurons: a potential substrate for cannabinoid receptor antagonist treatment of addiction. Neuropharmacology 2005, 48:1105-1116.
83. Oleson E.B., Cheer J.F. A brain on cannabinoids: the role of dopamine release in reward seeking. Cold Spring Harb. Perspect. Med. 2012, 2:a012229.
84. Badiani A., et al. Opiate versus psychostimulant addiction: the differences do matter. Nat. Rev. Neurosci. 2011, 12:685-700.
85. Ungless M.A., Grace A.A. Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci. 2012, 35:422-430.
86. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35:217-238.
87. Everitt B.J., et al. Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008, 363:3125-3135.
88. Luscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
89. Nestler E.J. Is there a common molecular pathway for addiction?. Nat. Neurosci. 2005, 8:1445-1449.
90. Pontieri F.E., et al. Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the 'shell' as compared with the 'core' of the rat nucleus accumbens. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:12304-12308.
91. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 2005, 8:1481-1489.
92. Di C.G., Bassareo V. Reward system and addiction: what dopamine does and doesn't do. Curr. Opin. Pharmacol. 2007, 7:69-76.
93. Lammel S., et al. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 2011, 70:855-862.
94. Jones S., Bonci A. Synaptic plasticity and drug addiction. Curr. Opin. Pharmacol. 2005, 5:20-25.
95. Luscher C. Cocaine-evoked synaptic plasticity of excitatory transmission in the ventral tegmental area. Cold Spring Harb. Perspect. Med. 2013, 3:a012013.
96. Mameli M., et al. Cocaine-evoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat. Neurosci. 2009, 12:1036-1041.
97. Haber S.N., et al. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci. 2000, 20:2369-2382.
98. Willuhn I., et al. Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:20703-20708.
99. Belin D., Everitt B.J. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 2008, 57:432-441.
100. Ito R., Hayen A. Opposing roles of nucleus accumbens core and shell dopamine in the modulation of limbic information processing. J. Neurosci. 2011, 31:6001-6007.
101. Saunders B.T., et al. Cue-evoked cocaine 'craving': role of dopamine in the accumbens core. J. Neurosci. 2013, 33:13989-14000.
102. Kalivas P.W., O'Brien C. Drug addiction as a pathology of staged neuroplasticity. Neuropsychopharmacology 2008, 33:166-180.
103. Ikemoto S., Bonci A. Neurocircuitry of drug reward. Neuropharmacology 2014, 76(Pt B):329-341.
104. Torres G.E., et al. Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 2003, 4:13-25.
105. Howell L.L., Kimmel H.L. Monoamine transporters and psychostimulant addiction. Biochem. Pharmacol. 2008, 75:196-217.
106. Kravitz A.V., Kreitzer A.C. Striatal mechanisms underlying movement, reinforcement, and punishment. Physiology 2012, 27:167-177.
107. Schultz W., et al. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
108. Clark J.J., et al. Chronic microsensors for longitudinal, subsecond dopamine detection in behaving animals. Nat. Methods 2010, 7:126-129.
109. Howard C.D., et al. Methamphetamine-induced neurotoxicity disrupts naturally occurring phasic dopamine signaling. Eur. J. Neurosci. 2013, 38:2078-2088.
110. Melis M., et al. Different mechanisms for dopaminergic excitation induced by opiates and cannabinoids in the rat midbrain. Prog. Neuropsychopharmacol. Biol. Psychiatry 2000, 24:993-1006.
111. Turner T.J. Nicotine enhancement of dopamine release by a calcium-dependent increase in the size of the readily releasable pool of synaptic vesicles. J. Neurosci. 2004, 24:11328-11336.
112. Rice M.E., Cragg S.J. Nicotine amplifies reward-related dopamine signals in striatum. Nat. Neurosci. 2004, 7:583-584.
113. Britt J.P., McGehee D.S. Presynaptic opioid and nicotinic receptor modulation of dopamine overflow in the nucleus accumbens. J. Neurosci. 2008, 28:1672-1681.
114. Pons S., et al. Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J. Neurosci. 2008, 28:12318-12327.
115. Liu L., et al. Nicotinic acetylcholine receptors containing the alpha6 subunit contribute to ethanol activation of ventral tegmental area dopaminergic neurons. Biochem. Pharmacol. 2013, 86:1194-1200.
116. Stuber G.D., et al. Optogenetic modulation of neural circuits that underlie reward seeking. Biol. Psychiatry 2012, 71:1061-1067.
117. Jentsch J.D., Pennington Z.T. Reward, interrupted: Inhibitory control and its relevance to addictions. Neuropharmacology 2014, 76(Pt B):479-486.
118. Watabe-Uchida M., et al. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 2012, 74:858-873.
119. Margolis E.B., et al. Midbrain dopamine neurons: projection target determines action potential duration and dopamine D(2) receptor inhibition. J. Neurosci. 2008, 28:8908-8913.
120. Lammel S., et al. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008, 57:760-773.
121. Volman S.F., et al. New insights into the specificity and plasticity of reward and aversion encoding in the mesolimbic system. J. Neurosci. 2013, 33:17569-17576.
122. Sofuoglu M., et al. Pharmacological treatment of comorbid PTSD and substance use disorder: Recent progress. Addict. Behav. 2013, 39:428-433.
123. Berridge C.W., Devilbiss D.M. Psychostimulants as cognitive enhancers: the prefrontal cortex, catecholamines, and attention-deficit/hyperactivity disorder. Biol. Psychiatry 2011, 69:e101-e111.
124. Bales J.W., et al. Persistent cognitive dysfunction after traumatic brain injury: A dopamine hypothesis. Neurosci. Biobehav. Rev. 2009, 33:981-1003.
125. Borland L.M., et al. Voltammetric study of extracellular dopamine near microdialysis probes acutely implanted in the striatum of the anesthetized rat. J. Neurosci. Methods 2005, 146:149-158.
126. Kulagina N.V., et al. Glutamate regulates the spontaneous and evoked release of dopamine in the rat striatum. Neuroscience 2001, 102:121-128.
127. Owesson-White C.A., et al. Sources contributing to the average extracellular concentration of dopamine in the nucleus accumbens. J. Neurochem. 2012, 121:252-262.
128. Eriksen J., et al. Regulation of dopamine transporter function by protein-protein interactions: new discoveries and methodological challenges. J. Neurochem. 2010, 113:27-41.
129. Roeper J. Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci. 2013, 36:336-342.
130. Bromberg-Martin E.S., et al. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.