Cocaine‐induced dopamine overflow within the nucleus accumbens measured by in vivo microdialysis: A meta‐analysis

A meta‐analysis was conducted on data obtained from published articles which used in vivo microdialysis to assess dose‐response curves of cocaine on dopamine (DA) overflow within the nucleus accumbens (NAC). Different experimental and biological parameters such as route of administration (ip, sc, iv, local), rat and mouse strains, gender, age aspects, and regions cannulated (NAC core and shell) were considered. Data from 116 experiments involving 833 animals (out of 266 publications) fulfilled our selection criteria and were analyzed in relation to absolute basal DA levels, the maximum peak of DA overflow (peak [%] baseline) and the time when this peak (peak time) occurred. Our meta‐analysis revealed that absolute basal DA levels lie at 2.39 nM (median of all experiments) and that cocaine‐induced DA overflow in the NAC is significantly enhanced in a linear dose‐response fashion within the applied dose range as the regression function increases following either iv or ip administration. Peak time was reached fastest in iv experiments and slowest following local application. Furthermore, it was shown in ip experiments that the higher the dose, the longer it took to reach the zenith. Results from the NAC shell region displayed greater DA overflow as compared with the NAC core. DA overflow properties following cocaine treatment in mice did not differ from that in rats. Thus, neither species differences nor other biological factors such as, age, gender, and rat/mouse strain have a pronounced impact on cocaine‐induced DA overflow. Technical parameters of the microdialysis procedure such as calcium concentration of the perfusion medium and collected sample amount have also no significant effect in terms of DA overflow properties (peak [%] baseline and peak time) following cocaine treatment. In conclusion, these data may be deemed useful for textbook knowledge and a better comparability of data given by the generalization of already existing data as well as for investigators in maximizing the effect of cocaine‐induced DA overflow. Finally, this study examplifies how meta‐analyses may be applied to a wide range of data within the field of neurochemistry. Synapse 62:243–252, 2008. © 2008 Wiley‐Liss, Inc.

[1]  M. Bardo,et al.  Conditioned place preference using opiate and stimulant drugs: A meta-analysis , 1995, Neuroscience & Biobehavioral Reviews.

[2]  S. D. Glick,et al.  Interactions between ibogaine and cocaine in rats: in vivo microdialysis and motor behavior. , 1992, European journal of pharmacology.

[3]  N. Nagao,et al.  Suppressive effects of trihexyphenidyl on methamphetamine‐induced dopamine release as measured by in vivo microdialysis , 2003, Synapse.

[4]  J. B. Justice,et al.  Individual differences in basal and cocaine-stimulated extracellular dopamine in the nucleus accumbens using quantitative microdialysis , 1992, Brain Research.

[5]  L. Parsons,et al.  Serotonin1B Receptors in the Ventral Tegmental Area Modulate Cocaine-Induced Increases in Nucleus Accumbens Dopamine Levels , 2004, Journal of Pharmacology and Experimental Therapeutics.

[6]  M. L. Smith,et al.  Meta-analysis of psychotherapy outcome studies. , 1977, The American psychologist.

[7]  H. Fibiger,et al.  Behavioral and neurochemical interactions between cocaine and buprenorphine: implications for the pharmacotherapy of cocaine abuse. , 1991, The Journal of pharmacology and experimental therapeutics.

[8]  G. Di Chiara,et al.  Selective psychostimulant sensitization by food restriction: differential changes in accumbens shell and core dopamine , 2003, The European journal of neuroscience.

[9]  L. Ahtee,et al.  5-HT3 receptor antagonist MDL 72222 dose-dependently attenuates cocaine- and amphetamine-induced elevations of extracellular dopamine in the nucleus accumbens and the dorsal striatum. , 1996, Pharmacology & toxicology.

[10]  T. Svensson,et al.  Effects of amperozide on psychostimulant-induced hyperlocomotion and dopamine release in the nucleus accumbens , 1993, Pharmacology Biochemistry and Behavior.

[11]  R. Strecker,et al.  The 5-HT3 antagonist zacopride attenuates cocaine-induced increases in extracellular dopamine in rat nucleus accumbens , 1993, Pharmacology Biochemistry and Behavior.

[12]  N. Goeders,et al.  Effects of corticotropin‐releasing hormone receptor antagonists on cocaine‐induced dopamine overflow in the medial prefrontal cortex and nucleus accumbens of rats , 2005, Synapse.

[13]  J. Nation,et al.  Attenuation of cocaine-induced elevation of nucleus accumbens dopamine in lead-exposed rats , 1994, Brain Research Bulletin.

[14]  J. Franck,et al.  Ethanol administration potentiates cocaine-induced dopamine levels in the rat nucleus accumbens , 2001, Brain Research.

[15]  D. Segal,et al.  Dynamic changes in sensitivity occur during the acute response to cocaine and methylphenidate , 1999, Psychopharmacology.

[16]  T. Robinson,et al.  The effects of methamphetamine and cocaine on motor behavior and extracellular dopamine in the ventral striatum of Lewis versus Fischer 344 rats , 1994, Brain Research.

[17]  R. Rothman,et al.  Phentermine pretreatment antagonizes the cocaine‐induced rise in mesolimbic dopamine , 1996, Neuroreport.

[18]  S. Dewey,et al.  Repeated administration of 3,4-methylenedioxymethamphetamine augments cocaine's action on dopamine in the nucleus accumbens: a microdialysis study. , 1997, European journal of pharmacology.

[19]  S. Dewey,et al.  Sub-chronic low dose γ-vinyl GABA (vigabatrin) inhibits cocaine-induced increases in nucleus accumbens dopamine , 2003, Psychopharmacology.

[20]  A. Michael,et al.  Theory for the impact of basal turnover on dopamine clearance kinetics in the rat striatum after medial forebrain bundle stimulation and pressure ejection , 2005, Journal of neurochemistry.

[21]  A. Newman,et al.  Behavioral and neurochemical effects of the dopamine transporter ligand 4-chlorobenztropine alone and in combination with cocaine in vivo. , 1999, The Journal of pharmacology and experimental therapeutics.

[22]  Hua Yang,et al.  Voltammetric study of extracellular dopamine near microdialysis probes acutely implanted in the striatum of the anesthetized rat , 2005, Journal of Neuroscience Methods.

[23]  L. Pellegrino,et al.  stereotaxic atlas of the rat brain , 1967 .

[24]  R. Roth,et al.  Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis , 1989, Neuroscience Letters.

[25]  E. Meririnne,et al.  5-HT3 receptor antagonist MDL 72222 attenuates cocaine- and mazindol-, but not methylphenidate-induced neurochemical and behavioral effects in the rat , 2002, Psychopharmacology.

[26]  S. D. Glick,et al.  U50,488, a κ opioid receptor agonist, attenuates cocaine-induced increases in extracellular dopamine in the nucleus accumbens of rats , 1994, Neuroscience Letters.

[27]  J. B. Justice,et al.  Response to novelty predicts the locomotor and nucleus accumbens dopamine response to cocaine , 1991, Synapse.

[28]  Zachariah Jonasson,et al.  Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data , 2005, Neuroscience & Biobehavioral Reviews.

[29]  G. Di Chiara,et al.  Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  N. Volkow,et al.  Direct approach for attenuating cocaine's effects on extracellular dopamine: Targeting the dopamine transporter , 1997, Synapse.

[31]  N. Goeders,et al.  Pretreatment with corticosterone attenuates the nucleus accumbens dopamine response but not the stimulant response to cocaine in rats , 2002, Behavioural pharmacology.

[32]  R. Post,et al.  Carbamazepine attenuates cocaine-induced increases in dopamine in the nucleus accumbens: an in vivo dialysis study. , 1993, European journal of pharmacology.

[33]  G. Glass.  Primary, Secondary, and Meta-Analysis of Research1 , 1976 .

[34]  M. Schäfer,et al.  Sensitization to the behavioural effects of cocaine: alterations in tyrosine hydroxylase or endogenous opioid mRNAs are not necessarily involved , 2001, Naunyn-Schmiedeberg's Archives of Pharmacology.

[35]  S. Dewey,et al.  Effects of pharmacologic increases in brain GABA levels on cocaine‐induced changes in extracellular dopamine , 1998, Synapse.

[36]  J. Feldon,et al.  Effects of cocaine on dopamine in subregions of the rat prefrontal cortex and their efferents to subterritories of the nucleus accumbens. , 1999, European journal of pharmacology.

[37]  L. Parsons,et al.  Simple microbore high-performance liquid chromatographic method for the determination of dopamine and cocaine from a single in vivo brain microdialysis sample. , 1998, Journal of chromatography. B, Biomedical sciences and applications.

[38]  G. Chiara.  Nucleus accumbens shell and core dopamine: differential role in behavior and addiction , 2002, Behavioural Brain Research.

[39]  D. Reboussin,et al.  Comparison of a novel tropane analog of cocaine, 2 beta-propanoyl-3 beta-(4-tolyl) tropane with cocaine HCl in rats: nucleus accumbens extracellular dopamine concentration and motor activity. , 1995, The Journal of pharmacology and experimental therapeutics.

[40]  B. Moghaddam,et al.  Differential effect of cocaine on extracellular dopamine levels in rat medial prefrontal cortex and nucleus accumbens: Comparison to amphetamine , 1989, Synapse.

[41]  A. Grace,et al.  Acute and Chronic Corticotropin-Releasing Factor 1 Receptor Blockade Inhibits Cocaine-Induced Dopamine Release: Correlation with Dopamine Neuron Activity , 2005, Journal of Pharmacology and Experimental Therapeutics.

[42]  N. Volkow,et al.  Selegiline potentiates cocaine‐induced increases in rodent nucleus accumbens dopamine , 2003, Synapse.

[43]  J. Brodie,et al.  gamma-aminobutyric acid mimetic drugs differentially inhibit the dopaminergic response to cocaine. , 2000, European journal of pharmacology.

[44]  L. Parsons,et al.  RU 24969, a 5‐HT1B/1A receptor agonist, potentiates cocaine‐induced increases in nucleus accumbens dopamine , 1999, Synapse.

[45]  P. Jatlow,et al.  Cocaine and Cocaethylene: Microdialysis Comparison of Brain Drug Levels and Effects on Dopamine and Serotonin , 1993, Journal of neurochemistry.

[46]  L. Parsons,et al.  Enhanced Locomotor, Reinforcing, and Neurochemical Effects of Cocaine in Serotonin 5-Hydroxytryptamine 2C Receptor Mutant Mice , 2002, The Journal of Neuroscience.

[47]  J. Steketee,et al.  Injection of the protein kinase inhibitor H7 into the A10 dopamine region blocks the acute responses to cocaine: Behavioral and in vivo microdialysis studies , 1993, Neuropharmacology.

[48]  P. Kalivas,et al.  The NMDA antagonist, dizocilpine, enhances cocaine reinforcement without influencing mesoaccumbens dopamine transmission , 1997, Psychopharmacology.

[49]  I. Lucki,et al.  Serotonergic properties of cocaine: Effects on a 5-HT2 receptor-mediated behavior and on extracellular concentrations of serotonin and dopamine , 1994, Pharmacology Biochemistry and Behavior.

[50]  J. Mikkola,et al.  Effects of repeated cocaine treatment on striatal dopamine release in alcohol-preferring AA and alcohol-avoiding ANA rats , 2001, Naunyn-Schmiedeberg's Archives of Pharmacology.

[51]  U. Spampinato,et al.  Selective serotonin reuptake inhibitors enhance cocaine-induced locomotor activity and dopamine release in the nucleus accumbens , 2003, Neuropharmacology.

[52]  K. Rice,et al.  GBR12909 attenuates cocaine-induced activation of mesolimbic dopamine neurons in the rat. , 1994, The Journal of pharmacology and experimental therapeutics.

[53]  J. Huston,et al.  The selective serotonin1A-receptor antagonist WAY 100635 blocks behavioral stimulating effects of cocaine but not ventral striatal dopamine increase , 2002, Behavioural Brain Research.

[54]  Christine M Andrews,et al.  Effects of cocaine on extracellular dopamine and serotonin levels in the nucleus accumbens , 2001, Psychopharmacology.

[55]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[56]  F. Leri,et al.  Effects of Cocaine in Rats Exposed to Heroin , 2003, Neuropsychopharmacology.

[57]  M. Lennon,et al.  Dopamine responsiveness to drugs of abuse: A shell‐core investigation in the nucleus accumbens of the mouse , 2003, Synapse.

[58]  M. Collu,et al.  Baclofen antagonizes nicotine‐, cocaine‐, and morphine‐induced dopamine release in the nucleus accumbens of rat , 2003, Synapse.

[59]  F. Weiss,et al.  The dopamine hypothesis of reward: past and current status , 1999, Trends in Neurosciences.

[60]  M. Reith,et al.  Extracellular dopamine, norepinephrine, and serotonin in the ventral tegmental area and nucleus accumbens of freely moving rats during intracerebral dialysis following systemic administration of cocaine and other uptake blockers , 1997, Psychopharmacology.

[61]  C. Beyer,et al.  Intra-medial prefrontal cortex injection of quinpirole, but not SKF 38393, blocks the acute motor-stimulant response to cocaine in the rat , 2000, Psychopharmacology.

[62]  Mingsheng Huang,et al.  Dopamine‐dependent responses to cocaine depend on corticotropin‐releasing factor receptor subtypes , 2003, Journal of neurochemistry.

[63]  Christine M Andrews,et al.  The 5-HT1A receptor modulates the effects of cocaine on extracellular serotonin and dopamine levels in the nucleus accumbens. , 2005, European journal of pharmacology.

[64]  R. Rothman,et al.  Inhibition of MAO-A fails to alter cocaine-induced increases in extracellular dopamine and norepinephrine in rat nucleus accumbens. , 2001, Brain research. Molecular brain research.

[65]  C. Duvauchelle,et al.  Conditioned increases in behavioral activity and accumbens dopamine levels produced by intravenous cocaine. , 2000, Behavioral neuroscience.