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Rapid dopamine transmission within the nucleus accumbens: Dramatic difference between morphine and oxycodone delivery
dc.contributor.authorVander Weele, Caitlin M.en_US
dc.contributor.authorPorter‐stransky, Kirsten A.en_US
dc.contributor.authorMabrouk, Omar S.en_US
dc.contributor.authorLovic, Vedranen_US
dc.contributor.authorSinger, Bryan F.en_US
dc.contributor.authorKennedy, Robert T.en_US
dc.contributor.authorAragona, Brandon J.en_US
dc.date.accessioned2014-11-04T16:35:29Z
dc.date.availableWITHHELD_12_MONTHSen_US
dc.date.available2014-11-04T16:35:29Z
dc.date.issued2014-10en_US
dc.identifier.citationVander Weele, Caitlin M.; Porter‐stransky, Kirsten A. ; Mabrouk, Omar S.; Lovic, Vedran; Singer, Bryan F.; Kennedy, Robert T.; Aragona, Brandon J. (2014). "Rapid dopamine transmission within the nucleus accumbens: Dramatic difference between morphine and oxycodone delivery." European Journal of Neuroscience 40(7): 3041-3054.en_US
dc.identifier.issn0953-816Xen_US
dc.identifier.issn1460-9568en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/109299
dc.description.abstractWhile most drugs of abuse increase dopamine neurotransmission, rapid neurochemical measurements show that different drugs evoke distinct dopamine release patterns within the nucleus accumbens. Rapid changes in dopamine concentration following psychostimulant administration have been well studied; however, such changes have never been examined following opioid delivery. Here, we provide novel measures of rapid dopamine release following intravenous infusion of two opioids, morphine and oxycodone, in drug‐naïve rats using fast‐scan cyclic voltammetry and rapid (1 min) microdialysis coupled with high‐performance liquid chromatography ‐ tandem mass spectrometry ( HPLC ‐ MS ). In addition to measuring rapid dopamine transmission, microdialysis HPLC ‐ MS measures changes in GABA , glutamate, monoamines, monoamine metabolites and several other neurotransmitters. Although both opioids increased dopamine release in the nucleus accumbens, their patterns of drug‐evoked dopamine transmission differed dramatically. Oxycodone evoked a robust and stable increase in dopamine concentration and a robust increase in the frequency and amplitude of phasic dopamine release events. Conversely, morphine evoked a brief (~ 1 min) increase in dopamine that was coincident with a surge in GABA concentration and then both transmitters returned to baseline levels. Thus, by providing rapid measures of neurotransmission, this study reveals previously unknown differences in opioid‐induced neurotransmitter signaling. Investigating these differences may be essential for understanding how these two drugs of abuse could differentially usurp motivational circuitry and powerfully influence behavior. We provide novel measures of rapid dopamine and other neurotransmitter release following intravenous infusion of morphine and oxycodone using fast‐scan cyclic voltammetry and rapid microdialysis with mass spectrometry. Although both opioids increased dopamine in the nucleus accumbens, their evoked patterns of transmission differed dramatically. Oxycodone elicited a robust and stable increase in dopamine concentration and a significant increase in the frequency and amplitude of dopamine transients. Conversely, morphine evoked a brief, 1‐min increase in dopamine that was coincident with a surge in GABA before both transmitters returned to baseline levels. This study reveals previously unknown differences in opioid‐induced neurotransmitter signaling.en_US
dc.publisherWiley Periodicals, Inc.en_US
dc.subject.otherAddictionen_US
dc.subject.otherOpioiden_US
dc.subject.otherRewarden_US
dc.subject.otherMotivationen_US
dc.titleRapid dopamine transmission within the nucleus accumbens: Dramatic difference between morphine and oxycodone deliveryen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelNeurosciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/109299/1/ejn12709.pdf
dc.identifier.doi10.1111/ejn.12709en_US
dc.identifier.sourceEuropean Journal of Neuroscienceen_US
dc.identifier.citedreferenceRoitman, M.F., Stuber, G.D., Phillips, P.E., Wightman, R.M. & Carelli, R.M. ( 2004 ) Dopamine operates as a subsecond modulator of food seeking. J. Neurosci., 24, 1265 – 1271.en_US
dc.identifier.citedreferenceRobinson, D.L., Venton, B.J., Heien, M.L. & Wightman, R.M. ( 2003 ) Detecting subsecond dopamine release with fast‐scan cyclic voltammetry in vivo. Clin. Chem., 49, 1763 – 1773.en_US
dc.identifier.citedreferenceRouge‐Pont, F., Usiello, A., Benoit‐Marand, M., Gonon, F., Piazza, P.V. & Borrelli, E. ( 2002 ) Changes in extracellular dopamine induced by morphine and cocaine: crucial control by D2 receptors. J. Neurosci., 22, 3293 – 3301.en_US
dc.identifier.citedreferenceSaigusa, T., Aono, Y., Mizoguchi, N., Iwakami, T., Takada, K., Oi, Y., Ueda, K., Koshikawa, N. & Cools, A.R. ( 2008 ) Role of GABA B receptors in the endomorphin‐1‐, but not endomorphin‐2‐, induced dopamine efflux in the nucleus accumbens of freely moving rats. Eur. J. Pharmacol., 581, 276 – 282.en_US
dc.identifier.citedreferenceShen, H.W., Scofield, M.D., Boger, H., Hensley, M. & Kalivas, P.W. ( 2014 ) Synaptic glutamate spillover due to impaired glutamate uptake mediates heroin relapse. J. Neurosci., 34, 5649 – 5657.en_US
dc.identifier.citedreferenceSinkala, E., McCutcheon, J.E., Schuck, M.J., Schmidt, E., Roitman, M.F. & Eddington, D.T. ( 2012 ) Electrode calibration with a microfluidic flow cell for fast‐scan cyclic voltammetry. Lab Chip, 12, 2403 – 2408.en_US
dc.identifier.citedreferenceSombers, L.A., Beyene, M., Carelli, R.M. & Wightman, R.M. ( 2009 ) Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J. Neurosci., 29, 1735 – 1742.en_US
dc.identifier.citedreferenceSong, P., Mabrouk, O.S., Hershey, N.D. & Kennedy, R.T. ( 2012 ) In vivo neurochemical monitoring using benzoyl chloride derivatization and liquid chromatography‐mass spectrometry. Anal. Chem., 84, 412 – 419.en_US
dc.identifier.citedreferenceStoops, W.W., Hatton, K.W., Lofwall, M.R., Nuzzo, P.A. & Walsh, S.L. ( 2010 ) Intravenous oxycodone, hydrocodone, and morphine in recreational opioid users: abuse potential and relative potencies. Psychopharmacology, 212, 193 – 203.en_US
dc.identifier.citedreferenceSun, J.Y., Yang, J.Y., Wang, F., Wang, J.Y., Song, W., Su, G.Y., Dong, Y.X. & Wu, C.F. ( 2011 ) Lesions of nucleus accumbens affect morphine‐induced release of ascorbic acid and GABA but not of glutamate in rats. Addict. Biol., 16, 540 – 550.en_US
dc.identifier.citedreferenceTakmakov, P., Zachek, M.K., Keithley, R.B., Bucher, E.S., McCarty, G.S. & Wightman, R.M. ( 2010 ) Characterization of local pH changes in brain using fast‐scan cyclic voltammetry with carbon microelectrodes. Anal. Chem., 82, 9892 – 9900.en_US
dc.identifier.citedreferenceTan, K.R., Yvon, C., Turiault, M., Mirzabekov, J.J., Doehner, J., Labouèbe, G., Deisseroth, K., Tye, K.M. & Lüscher, C. ( 2012 ) GABA neurons of the VTA drive conditioned place aversion. Neuron, 73, 1173 – 1183.en_US
dc.identifier.citedreferenceThompson, P.I., Joel, S.P., John, L., Wedzicha, J.A., Maclean, M. & Slevin, M.L. ( 1995 ) Respiratory depression following morphine and morphine‐6‐glucuronide in normal subjects. Brit. J. Clin. Pharmaco., 40, 145 – 152.en_US
dc.identifier.citedreferenceVander Weele, C.M., Lovic, V. & Aragona, B.J. ( 2011 ) Rapid dopamine signaling in response to a short‐acting opiatae, remifentanil. Society for Neuroscience. 41st Annual Meeting. Washington, District of Columbia.en_US
dc.identifier.citedreferenceVenton, B.J., Michael, D.J. & Wightman, R.M. ( 2003 ) Correlation of local changes in extracellular oxygen and pH that accompany dopaminergic terminal activity in the rat caudate‐putamen. J. Neurochem., 84, 373 – 381.en_US
dc.identifier.citedreferenceVillesen, H.H., Foster, D.J., Upton, R.N., Somogyi, A.A., Martinez, A. & Grant, C. ( 2006 ) Cerebral kinetics of oxycodone in conscious sheep. J. Pharm. Sci., 95, 1666 – 1676.en_US
dc.identifier.citedreferenceWightman, R.M., Heien, M.L., Wassum, K.M., Sombers, L.A., Aragona, B.J., Khan, A.S., Ariansen, J.L., Cheer, J.F., Phillips, P.E. & Carelli, R.M. ( 2007 ) Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens. Eur. J. Neurosci., 26, 2046 – 2054.en_US
dc.identifier.citedreferenceWill, M., Franzblau, E. & Kelley, A. ( 2003 ) Nucleus accumbens μ‐opioids regulate intake of a high‐fat diet via activation of a distributed brain network. J. Neurosci., 23, 2882 – 2888.en_US
dc.identifier.citedreferenceWilliams, J.T., Christie, M.J. & Manzoni, O. ( 2001 ) Cellular and synaptic adaptations mediating opioid dependence. Physiol. Rev., 81, 299 – 343.en_US
dc.identifier.citedreferenceWilluhn, I., Burgeno, L.M., Everitt, B.J. & Phillips, P.E. ( 2012 ) Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use. Proc. Natl. Acad. Sci. USA, 109, 20703 – 20708.en_US
dc.identifier.citedreferenceWydra, K., Golembiowska, K., Zaniewska, M., Kamińska, K., Ferraro, L., Fuxe, K. & Filip, M. ( 2013 ) Accumbal and pallidal dopamine, glutamate and GABA overflow during cocaine self‐administration and its extinction in rats. Addict. Biol., 18, 307 – 324.en_US
dc.identifier.citedreferencevan Zessen, R., Phillips, J.L., Budygin, E.A. & Stuber, G.D. ( 2012 ) Activation of VTA GABA neurons disrupts reward consumption. Neuron, 73, 1184 – 1194.en_US
dc.identifier.citedreferenceZhang, Y., Picetti, R., Butelman, E.R., Schlussman, S.D., Ho, A. & Kreek, M.J. ( 2009 ) Behavioral and neurochemical changes induced by oxycodone differ between adolescent and adult mice. Neuropsychopharmacology, 34, 912 – 922.en_US
dc.identifier.citedreferenceZhang, Y., Mayer‐Blackwell, B., Schlussman, S.D., Randesi, M., Butelman, E.R., Ho, A., Ott, J. & Kreek, M.J. ( 2014 ) Extended access oxycodone self‐administration and neurotransmitter receptor gene expression in the dorsal striatum of adult C57BL/6 J mice. Psychopharmacology, 231, 1277 – 1287.en_US
dc.identifier.citedreferenceAndersson, J.L., Nomikos, G.G., Marcus, M., Hertel, P., Mathe, J.M. & Svensson, T.H. ( 1995 ) Ritanserin potentiates the stimulatory effects of raclopride on neuronal activity and dopamine release selectivity in the mesolimbic dopaminergic system. N.‐S. Arch. Pharmacol., 352, 374 – 385.en_US
dc.identifier.citedreferenceAono, Y., Saigusa, T., Mizoguchi, N., Iwakami, T., Takada, K., Gionhaku, N., Oi, Y., Ueda, K., Koshikawa, N. & Cools, A.R. ( 2008 ) Role of GABA A receptors in the endomorphin‐1‐, but not endomorphin‐2‐, induced dopamine efflux in the nucleus accumbens of freely moving rats. Eur. J. Pharmacol., 580, 87 – 94.en_US
dc.identifier.citedreferenceAragona, B.J., Cleaveland, N.A., Stuber, G.D., Day, J.J., Carelli, R.M. & Wightman, R.M. ( 2008 ) 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., 28, 8821 – 8831.en_US
dc.identifier.citedreferenceAragona, B.J., Day, J.J., Roitman, M.F., Cleaveland, N.A., Wightman, R.M. & Carelli, R.M. ( 2009 ) Regional specificity in the real‐time development of phasic dopamine transmission patterns during acquisition of a cue‐cocaine association in rats. Eur. J. Neurosci., 30, 1889 – 1899.en_US
dc.identifier.citedreferenceBadrinarayan, A., Wescott, S.A., Vander Weele, C.M., Saunders, B.T., Couturier, B.E., Maren, S. & Aragona, B.J. ( 2012 ) Aversive stimuli differentially modulate real‐time dopamine transmission dynamics within the nucleus accumbens core and shell. J. Neurosci., 32, 15779 – 15790.en_US
dc.identifier.citedreferenceBerridge, K.C. & Kringelbach, M.L. ( 2013 ) Neuroscience of affect: brain mechanisms of pleasure and displeasure. Curr. Opin. Neurobiol., 23, 294 – 303.en_US
dc.identifier.citedreferenceBoström, E., Simonsson, U.S. & Hammarlund‐Udenaes, M. ( 2006 ) In vivo blood‐brain barrier transport of oxycodone in the rat: indications for active influx and implications for pharmacokinetics/pharmacodynamics. Drug Metab. Dispos., 34, 1624 – 1631.en_US
dc.identifier.citedreferenceBoström, E., Hammarlund‐Udenaes, M. & Simonsson, U.S. ( 2008 ) Blood–brain barrier transport helps to explain discrepancies in in vivo potency between oxycodone and morphine. Anesthesiology, 108, 495 – 505.en_US
dc.identifier.citedreferenceCheer, J.F., Wassum, K.M., Sombers, L.A., Heien, M.L., Ariansen, J.L., Aragona, B.J., Phillips, P.E. & Wightman, R.M. ( 2007 ) Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J. Neurosci., 27, 791 – 795.en_US
dc.identifier.citedreferenceChen, Z.R., Irvine, R.J., Somogyi, A.A. & Bochner, F. ( 1991 ) Mu receptor binding of some commonly used opioids and their metabolites. Life Sci., 48, 2165 – 2171.en_US
dc.identifier.citedreferenceComer, S.D., Sullivan, M.A., Whittington, R.A., Vosburg, S.K. & Kowalczyk, W.J. ( 2008 ) Abuse liability of prescription opioids compared to heroin in morphine‐maintained heroin abusers. Neuropsychopharmacology, 33 1179 – 1191.en_US
dc.identifier.citedreferenceComer, S.D., Metz, V.E., Cooper, Z.D., Kowalczyk, W.J., Jones, J.D., Sullivan, M.A., Manubay, J.M., Vosburg, S.K., Smith, M.E., Peyser, D. & Saccone, P.A. ( 2013 ) Comparison of a drug versus money and drug versus drug self‐administration choice procedure with oxycodone and morphine in opioid addicts. Behav. Pharmacol., 24, 504 – 516.en_US
dc.identifier.citedreferenceCompton, W.M. & Volkow, N.D. ( 2006 ) Major increases in opioid analgesic abuse in the United States: concerns and strategies. Drug Alcohol Depen., 81, 103 – 107.en_US
dc.identifier.citedreferenceCovey, D.P., Roitman, M.F. & Garris, P.A. ( 2014 ) Illicit dopamine transients: reconciling actions of abused drugs. Trends Neurosci., 37, 200 – 210.en_US
dc.identifier.citedreferenceDaberkow, D.P., Brown, H.D., Bunner, K.D., Kraniotis, S.A., Doellman, M.A., Ragozzino, M.E., Garris, P.A. & Roitman, M.F. ( 2013 ) Amphetamine paradoxically augments exocytotic dopamine release and phasic dopamine signals. J. Neurosci., 33, 452 – 463.en_US
dc.identifier.citedreferenceDahchour, A., Quertemont, E. & De Witte, P. ( 1994 ) Acute ethanol increases taurine but neither glutamate nor GABA in the nucleus accumbens of male rats: a microdialysis study. Alcohol Alcoholism, 29, 485 – 487.en_US
dc.identifier.citedreferenceDavis, M.P., Varga, J., Dickerson, D., Walsh, D., LeGrand, S.B. & Lagman, R. ( 2003 ) Normal‐release and controlled‐release oxycodone: pharmacokinetics, pharmacodynamics, and controversy. Support. Care Cancer, 11, 84 – 92.en_US
dc.identifier.citedreferenceDi Chiara, G. & Imperato, A. ( 1988 ) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA, 85, 5274 – 5278.en_US
dc.identifier.citedreferenceFenu, S., Spina, L., Rivas, E., Longoni, R. & Di Chiara, G. ( 2006 ) Morphine‐conditioned single‐trial place preference: role of nucleus accumbens shell dopamine receptors in acquisition, but not expression. Psychopharmacology, 187, 143 – 153.en_US
dc.identifier.citedreferenceFrank, S.T., Krumm, B. & Spanagel, R. ( 2008 ) Cocaine‐induced dopamine overflow within the nucleus accumbens measured by in vivo microdialysis: a meta‐analysis. Synapse, 62, 243 – 252.en_US
dc.identifier.citedreferenceGarris, P.A. & Wightman, R.M. ( 1994 ) Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J. Neurosci., 14, 442 – 450.en_US
dc.identifier.citedreferenceGysling, K. & Wang, R.Y. ( 1983 ) Morphine‐induced activation of A10 dopamine neurons in the rat. Brain Res., 277, 119 – 127.en_US
dc.identifier.citedreferenceHeien, M.L., Khan, A.S., Ariansen, J.L., Cheer, J.F., Phillips, P.E., Wassum, K.M. & Wightman, R.M. ( 2005 ) Real‐time measurement of dopamine fluctuations after cocaine in the brain of behaving rats. Proc. Natl. Acad. Sci. USA, 102, 10023 – 10028.en_US
dc.identifier.citedreferenceHyman, S.E., Malenka, R.C. & Nestler, E.J. ( 2006 ) Neural mechanisms of addiction: the role of reward‐related learning and memory. Annu. Rev. Neurosci., 29, 565 – 598.en_US
dc.identifier.citedreferenceIkemoto, S. ( 2007 ) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens‐olfactory tubercle complex. Brain Res. Rev., 56, 27 – 78.en_US
dc.identifier.citedreferenceIto, R., Dalley, J.W., Howes, S.R., Robbins, T.W. & Everitt, B.J. ( 2000 ) Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine‐seeking behavior in rats. J. Neurosci., 20, 7489 – 7495.en_US
dc.identifier.citedreferenceJohnson, S.W. & North, R.A. ( 1992 ) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci., 12, 483 – 488.en_US
dc.identifier.citedreferenceKalso, E. ( 2007 ) How different is oxycodone from morphine? Pain, 132, 227 – 228.en_US
dc.identifier.citedreferenceKeithley, R.B. & Wightman, R.M. ( 2011 ) Assessing principal component regression prediction of neurochemicals detected with fast‐scan cyclic voltammetry. ACS Chem. Neurosci., 2, 514 – 525.en_US
dc.identifier.citedreferenceKeithley, R.B., Heien, M.L. & Wightman, R.M. ( 2009 ) Multivariate concentration determination using principal component regression with residual analysis. TRAC‐Trend. Anal. Chem., 28, 1127 – 1136.en_US
dc.identifier.citedreferenceKeithley, R.B., Carelli, R.M. & Wightman, R.M. ( 2010 ) Rank estimation and the multivariate analysis of in vivo fast‐scan cyclic voltammetric data. Anal. Chem., 82, 5541 – 5551.en_US
dc.identifier.citedreferenceKelley, A.E. ( 2004 ) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward‐related learning. Neurosci. Biobehav. R., 27, 765 – 776.en_US
dc.identifier.citedreferenceLalovic, B., Kharasch, E., Hoffer, C., Risler, L., Liu‐Chen, L.‐Y. & Shen, D.D. ( 2006 ) Pharmacokinetics and pharmacodynamics of oral oxycodone in healthy human subjects: role of circulating active metabolites*. Clin. Pharmacol. Ther., 79, 461 – 479.en_US
dc.identifier.citedreferenceLammel, S., Hetzel, A., Hackel, O., Jones, I., Liss, B. & Roeper, J. ( 2008 ) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron, 57, 760 – 773.en_US
dc.identifier.citedreferenceLammel, S., Ion, D.I., Roeper, J. & Malenka, R.C. ( 2011 ) Projection‐specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron, 70, 855 – 862.en_US
dc.identifier.citedreferenceLemberg, K.K., Heiskanen, T.E., Kontinen, V.K. & Kalso, E.A. ( 2009 ) Pharmacology of oxycodone: does it explain why oxycodone has become a bestselling strong opioid? Scand. J. Pain, 1, S18 – S23.en_US
dc.identifier.citedreferenceLester, P.A. & Traynor, J.R. ( 2006 ) Comparison of the in vitro efficacy of μ, δ, κ and ORL 1 receptor agonists and non‐selective opioid agonists in dog brain membranes. Brain Res., 1073, 290 – 296.en_US
dc.identifier.citedreferenceLüscher, C. & Ungless, M.A. ( 2006 ) The mechanistic classification of addictive drugs. PLoS Med., 3, e437.en_US
dc.identifier.citedreferenceMatsui, A. & Williams, J.T. ( 2011 ) Opioid‐sensitive GABA inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons. J. Neurosci., 31, 17729 – 17735.en_US
dc.identifier.citedreferenceMatthews, R.T. & German, D.C. ( 1984 ) Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine. Neuroscience, 11, 617 – 625.en_US
dc.identifier.citedreferenceMayer‐Blackwell, B., Schlussman, S.D., Butelman, E.R., Ho, A., Ott, J., Kreek, M.J. & Zhang, Y. ( 2014 ) Self administration of oxycodone by adolescent and adult mice affects striatal neurotransmitter receptor gene expression. Neuroscience, 258, 280 – 291.en_US
dc.identifier.citedreferenceMcCabe, S.E., West, B.T. & Boyd, C.J. ( 2013a ) Leftover prescription opioids and nonmedical use among high school seniors: a multi‐cohort national study. J. Adolescent Health, 52, 480 – 485.en_US
dc.identifier.citedreferenceMcCabe, S.E., West, B.T. & Boyd, C.J. ( 2013b ) Medical use, medical misuse, and nonmedical use of prescription opioids: results from a longitudinal study. Pain, 154, 708 – 713.en_US
dc.identifier.citedreferenceMelief, E.J., Miyatake, M., Bruchas, M.R. & Chavkin, C. ( 2010 ) Ligand‐directed c‐Jun N‐terminal kinase activation disrupts opioid receptor signaling. Proc. Natl. Acad. Sci. USA, 107, 11608 – 11613.en_US
dc.identifier.citedreferenceMichael, D.J., Joseph, J.D., Kilpatrick, M.R., Travis, E.R. & Wightman, R.M. ( 1999 ) Improving data acquisition for fast‐scan cyclic voltammetry. Anal. Chem., 71, 3941 – 3947.en_US
dc.identifier.citedreferenceMierzejewski, P., Koros, E., Goldberg, S.R., Kostowski, W. & Stefanski, R. ( 2003 ) Intravenous self‐administration of morphine and cocaine: a comparative study. Pol. J. Pharmacol., 55, 713 – 726.en_US
dc.identifier.citedreferenceNestler, E.J. & Malenka, R.C. ( 2004 ) The addicted brain. Sci. Am., 290, 78 – 85.en_US
dc.identifier.citedreferenceNielsen, C.K., Ross, F.B., Lotfipour, S., Saini, K.S., Edwards, S.R. & Smith, M.T. ( 2007 ) Oxycodone and morphine have distinctly different pharmacological profiles: radioligand binding and behavioural studies in two rat models of neuropathic pain. Pain, 132, 289 – 300.en_US
dc.identifier.citedreferenceNiikura, K., Ho, A., Kreek, M.J. & Zhang, Y. ( 2013 ) Oxycodone‐induced conditioned place preference and sensitization of locomotor activity in adolescent and adult mice. Pharmacol. Biochem. Be., 110, 112 – 116.en_US
dc.identifier.citedreferenceOwesson‐White, C.A., Roitman, M.F., Sombers, L.A., Belle, A.M., Keithley, R.B., Peele, J.L., Carelli, R.M. & Wightman, R.M. ( 2012 ) Sources contributing to the average extracellular concentration of dopamine in the nucleus accumbens. J. Neurochem., 121, 252 – 262.en_US
dc.identifier.citedreferenceParker, L.A., Cyr, J.A., Santi, A.N. & Burton, P.D. ( 2002 ) The aversive properties of acute morphine dependence persist 48 h after a single exposure to morphine: evaluation by taste and place conditioning. Pharmacol. Biochem. Be., 72, 87 – 92.en_US
dc.identifier.citedreferencePeckham, E.M. & Traynor, J.R. ( 2006 ) Comparison of the antinociceptive response to morphine and morphine‐like compounds in male and female Sprague‐Dawley rats. J. Pharmacol. Exp. Ther., 316, 1195 – 1201.en_US
dc.identifier.citedreferencePhillips, P.E., Robinson, D.L., Stuber, G.D., Carelli, R.M. & Wightman, R.M. ( 2003a ) Real‐time measurements of phasic changes in extracellular dopamine concentration in freely moving rats by fast‐scan cyclic voltammetry. Method. Mol. Med., 79, 443 – 464.en_US
dc.identifier.citedreferencePhillips, P.E., Stuber, G.D., Heien, M.L., Wightman, R.M. & Carelli, R.M. ( 2003b ) Subsecond dopamine release promotes cocaine seeking. Nature, 422, 614 – 618.en_US
dc.identifier.citedreferencePontieri, F.E., Tanda, G. & Di Chiara, G. ( 1995 ) 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. USA, 92, 12304 – 12308.en_US
dc.identifier.citedreferencePorter‐Stransky, K.A., Wescott, S.A., Hershman, M., Badrinarayan, A., Vander Weele, C.M., Lovic, V. & Aragona, B.J. ( 2011 ) Cocaine must enter the brain to evoke unconditioned dopamine release within the nucleus accumbens shell. Neurosci. Lett., 504, 13 – 17.en_US
dc.identifier.citedreferenceRobinson, T.E. & Berridge, K.C. ( 2003 ) Addiction. Annu. Rev. Psychol., 54, 25 – 53.en_US
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