[en] Cocaine (benzoylmethylecgonine), a natural alkaloid, is a powerful psychostimulant and a highly addictive drug. Unfortunately, the relationships between its behavioral and electrophysiological effects are not clear. We investigated the effects of cocaine on the firing of midbrain dopaminergic (DA) neurons, both in anesthetized and awake rats, using pre-implanted multielectrode arrays and a recently developed telemetric recording system. In anesthetized animals, cocaine (10 mg/kg, intraperitoneally) produced a general decrease of the firing rate and bursting of DA neurons, sometimes preceded by a transient increase in both parameters, as previously reported by others. In awake rats, however, injection of cocaine led to a very different pattern of changes in firing. A decrease in firing rate and bursting was observed in only 14% of DA neurons. Most of the other DA neurons underwent increases in firing rate and bursting: these changes were correlated with locomotor activity in 52% of the neurons, but were uncorrelated in 29% of them. Drug concentration measurements indicated that the observed differences between the two conditions did not have a pharmacokinetic origin. Taken together, our results demonstrate that cocaine injection differentially affects the electrical activity of DA neurons in awake and anesthetized states. The observed increases in neuronal activity may in part reflect the cocaine-induced synaptic potentiation found ex vivo in these neurons. Our observations also show that electrophysiological recordings in awake animals can uncover drug effects, which are masked by general anesthesia.
Disciplines :
Pharmacy, pharmacology & toxicology
Author, co-author :
Koulchitsky, Stanislav ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Pharmacologie
DE BACKER, Benjamin ; Université de Liège - ULiège > Département de Pharmacie > Chimie toxicologique
Quertemont, Etienne ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Psychologie quantitative
Charlier, Corinne ; Université de Liège - ULiège > Département de pharmacie > Chimie toxicologique
Seutin, Vincent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Pharmacologie
Language :
English
Title :
Differential Effects of Cocaine on Dopamine Neuron Firing in Awake and Anesthetized Rats
Allen RM, Everett CV, Nelson AM, Gulley JM, Zahniser NR (2007). Low and high locomotor responsiveness to cocaine predicts intravenous cocaine conditioned place preference in male Sprague-Dawley rats. Pharmacol Biochem Behav 86: 37-44.
Argilli E, Sibley DR, Malenka RC, England PM, Bonci A (2008). Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J Neurosci 28: 9092-9100.
Beckstead RM, Domesick VB, Nauta WJ (1979). Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175: 191-217. (Pubitemid 10228475)
Belin D, Balado E, Piazza PV, Deroche-Gamonet V (2009). Pattern of intake and drug craving predict the development of cocaine addiction-like behavior in rats. Biol Psychiatry 65: 863-868.
Benuck M, Reith ME, Sershen H, Wiener HL, Lajtha A (1989). Oxidative metabolism of cocaine: comparison of brain and liver. Proc Soc Exp Biol Med 190: 7-13. (Pubitemid 19042401)
Berretta N, Bernardi G, Mercuri NB (2010). Firing properties and functional connectivity of substantia nigra pars compacta neurones recorded with a multi-electrode array in vitro. J Physiol 588(Part 10): 1719-1735.
Bowman BP, Vaughan SR, Walker QD, Davis SL, Little PJ, Scheffler NM et al (1999). Effects of sex and gonadectomy on cocaine metabolism in the rat. J Pharmacol Exp Ther 290: 1316-1323. (Pubitemid 29400275)
Bradberry CW, Roth RH (1989). Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis. Neurosci Lett 103: 97-102. (Pubitemid 19207489)
Broderick PA, Kornak Jr EP, Eng F, Wechsler R (1993). Real time detection of acute (IP) cocaine-enhanced dopamine and serotonin release in ventrolateral nucleus accumbens of the behaving Norway rat. Pharmacol Biochem Behav 46: 715-722.
Brodie MS, Dunwiddie TV (1990). Cocaine effects in the ventral tegmental area: evidence for an indirect dopaminergic mechanism of action. Naunyn-Schmiedeberg's ArchPharmacol 342: 660-665.
Bunney BS, Aghajanian GK, Roth RH (1973a). Comparison of effects of L-dopa, amphetamine and apomorphine on firing rate of rat dopaminergic neurones. Nature 245: 123-125.
Bunney BS, Walters JR, Roth RH, Aghajanian GK (1973b). Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. J Pharmacol Exp Ther 185: 560-571.
Cain ME, Smith CM, Bardo MT (2004). The effect of novelty on amphetamine self-administration in rats classified as high and low responders. Psychopharmacology (Berl) 176: 129-138. (Pubitemid 39517942)
Cameron DL, Williams JT (1994). Cocaine inhibits GABA release in the VTA through endogenous 5-HT. J Neurosci 14(Part 1): 6763-6767. (Pubitemid 24333094)
Carelli RM (2002). Nucleus accumbens cell firing during goaldirected behaviors for cocaine vs natural reinforcement. Physiol Behav 76: 379-387. (Pubitemid 34765591)
Carelli RM, Deadwyler SA (1994). A comparison of nucleus accumbens neuronal firing patterns during cocaine selfadministration and water reinforcement in rats. J Neurosci 14: 7735-7746. (Pubitemid 24983711)
Chefer VI, Zakharova I, Shippenberg TS (2003). Enhanced responsiveness to novelty and cocaine is associated with decreased basal dopamine uptake and release in the nucleus accumbens: quantitative microdialysis in rats under transient conditions. J Neurosci 23: 3076-3084. (Pubitemid 36418643)
Chiodo LA, Bannon MJ, Grace AA, Roth RH, Bunney BS (1984). Evidence for the absence of impulse-regulating somatodendritic and synthesis-modulating nerve terminal autoreceptors on subpopulations of mesocortical dopamine neurons. Neuroscience 12: 1-16. (Pubitemid 14077673)
Clark D, Chiodo LA (1988). Electrophysiological and pharmacological characterization of identified nigrostriatal and mesoaccumbens dopamine neurons in the rat. Synapse 2: 474-485.
Clark D, Hjorth S, Carlsson A (1985a). Dopamine-receptor agonists: mechanisms underlying autoreceptor selectivity. I. Review of the evidence. J Neural Transm 62: 1-52. (Pubitemid 15072762)
Clark D, Hjorth S, Carlsson A (1985b). Dopamine receptor agonists: mechanisms underlying autoreceptor selectivity. II. Theoretical considerations. J Neural Transm 62: 171-207. (Pubitemid 15067983)
Cohen I, Miles R (2000). Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus. J Physiol 524(Part 2): 485-502. (Pubitemid 30229513)
Einhorn LC, Johansen PA, White FJ (1988). Electrophysiological effects of cocaine in the mesoaccumbens dopamine system: studies in the ventral tegmental area. J Neurosci 8: 100-112. (Pubitemid 18034995)
Fallon JH, Moore RY (1978). Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol 180: 545-580.
Ford CP, Williams JT (2008). Mesoprefrontal dopamine neurons distinguish themselves. Neuron 57: 631-632. (Pubitemid 351335353)
Freeman AS, Bunney BS (1987). Activity of A9 and A10 dopaminergic neurons in unrestrained rats: further characterization and effects of apomorphine and cholecystokinin. Brain Res 405: 46-55. (Pubitemid 17034931)
Freeman AS, Kelland MD, Rouillard C, Chiodo LA (1989). Electrophysiological characteristics and pharmacological responsiveness of midbrain dopaminergic neurons of the aged rat. J Pharmacol Exp Ther 249: 790-797. (Pubitemid 19166659)
Freye E, Levy JV (2009). Pharmacology and Abuse of Cocaine, Amphetamines, Ecstasy and Related Designer Drugs: A Comprehensive Review on Their Mode of Action. Treatment of Abuse and Intoxication Springer: Düsseldorf, Germany. .
Geisler S, Derst C, Veh RW, Zahm DS (2007). Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27: 5730-5743. (Pubitemid 350021081)
Geisler S, Marinelli M, Degarmo B, Becker ML, Freiman AJ, Beales M et al (2008). Prominent activation of brainstem and pallidal afferents of the ventral tegmental area by cocaine. Neuropsychopharmacology 33: 2688-2700.
Gessa GL, Muntoni F, Collu M, Vargiu L, Mereu G (1985). Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res 348: 201-203. (Pubitemid 16235764)
Gold C, Henze DA, Koch C, Buzsaki G (2006). On the origin of the extracellular action potential waveform: a modeling study. J Neurophysiol 95: 3113-3128.
Grace AA, Bunney BS (1984). The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4: 2877-2890. (Pubitemid 15224432)
Grenhoff J, North RA, Johnson SW (1995). Alpha 1-adrenergic effects on dopamine neurons recorded intracellularly in the rat midbrain slice. Eur J Neurosci 7: 1707-1713.
Grimm JW, See RE (1997). Cocaine self-administration in ovariectomized rats is predicted by response to novelty, attenuated by 17-beta estradiol, and associated with abnormal vaginal cytology. Physiol Behav 61: 755-761. (Pubitemid 27208373)
Gulley JM, Hoover BR, Larson GA, Zahniser NR (2003). Individual differences in cocaine-induced locomotor activity in rats: behavioral characteristics, cocaine pharmacokinetics, and the dopamine transporter. Neuropsychopharmacology 28: 2089-2101. (Pubitemid 37468177)
Hamilton ME, Mele A, Pert A (1992). Striatal extracellular dopamine in conscious vs. anesthetized rats: effects of chloral hydrate anesthetic on responses to drugs of different classes. Brain Res 597: 1-7.
Heym J, Steinfels GF, Jacobs BL (1984). Chloral hydrate anesthesia alters the responsiveness of central serotonergic neurons in the cat. Brain Res 291: 63-72. (Pubitemid 14221327)
Hinerth MA, Collins HA, Baniecki M, Hanson RN, Waszczak BL (2000). Novel in vivo electrophysiological assay for the effects of cocaine and putative 'cocaine antagonists' on dopamine transporter activity of substantia nigra and ventral tegmental area dopamine neurons. Synapse 38: 305-312.
Hooks MS, Jones GH, Smith AD, Neill DB, Justice Jr JB (1991). Response to novelty predicts the locomotor and nucleus accumbens dopamine response to cocaine. Synapse 9: 121-128.
Horger BA, Iyasere CA, Berhow MT, Messer CJ, Nestler EJ, Taylor JR (1999). Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor. J Neurosci 19: 4110-4122. (Pubitemid 29222283)
Hubner CB, Koob GF (1990). The ventral pallidum plays a role in mediating cocaine and heroin self-administration in the rat. Brain Res 508: 20-29. (Pubitemid 20042060)
Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R (2002). Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114: 475-492. (Pubitemid 35245426)
Ikemoto 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. (Pubitemid 350110353)
Johnson SW, Mercuri NB, North RA (1992). 5-Hydroxytryptamine1B receptors block the GABAB synaptic potential in rat dopamine neurons. J Neurosci 12: 2000-2006.
Kalivas PW (1993). Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Rev 18: 75-113. (Pubitemid 23090012)
Kelland MD, Chiodo LA, Freeman AS (1990). Anesthetic influences on the basal activity and pharmacological responsiveness of nigrostriatal dopamine neurons. Synapse 6: 207-209. (Pubitemid 20304539)
Kelland MD, Freeman AS, Chiodo LA (1989). Chloral hydrate anesthesia alters the responsiveness of identified midbrain dopamine neurons to dopamine agonist administration. Synapse 3: 30-37. (Pubitemid 19042511)
Kiyatkin EA (2002). Dopamine in the nucleus accumbens: cellular actions, drug- and behavior-associated fluctuations, and a possible role in an organism's adaptive activity. Behav Brain Res 137: 27-46. (Pubitemid 35346427)
Kiyatkin EA, Rebec GV (2000). Dopamine-independent action of cocaine on striatal and accumbal neurons. Eur J Neurosci 12: 1789-1800. (Pubitemid 30258887)
Klitenick MA, Deutch AY, Churchill L, Kalivas PW (1992). Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum. Neuroscience 50: 371-386.
Koob GF (1992). Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13: 177-184.
Krebs RM, Heipertz D, Schuetze H, Duzel E (2011). Novelty increases the mesolimbic functional connectivity of the substantia nigra/ventral tegmental area (SN/VTA) during reward anticipation: evidence from high-resolution fMRI. NeuroImage 58: 647-655.
Kreuter JD, Mattson BJ, Wang B, You ZB, Hope BT (2004). Cocaine-induced Fos expression in rat striatum is blocked by chloral hydrate or urethane. Neuroscience 127: 233-242. (Pubitemid 38829168)
Kuhar MJ, Ritz MC, Boja JW (1991). The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 14: 299-302.
Lacey MG, Mercuri NB, North RA (1990). Actions of cocaine on rat dopaminergic neurones in vitro. Br J Pharmacol 99: 731-735. (Pubitemid 20111315)
Lammel 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. (Pubitemid 351335346)
Lammel S, Ion DI, Roeper J, Malenka RC (2011). Projectionspecific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70: 855-862.
Lange RA, Hillis LD (2001). Cardiovascular complications of cocaine use. N Engl J Med 345: 351-358. (Pubitemid 32703239)
Li MY, Yan QS, Coffey LL, Reith ME (1996). Extracellular dopamine, norepinephrine, and serotonin in the nucleus accumbens of freely moving rats during intracerebral dialysis with cocaine and other monoamine uptake blockers. J Neurochem 66: 559-568. (Pubitemid 26036690)
Mandt BH, Zahniser NR (2010). Low and high cocaine locomotor responding male Sprague-Dawley rats differ in rapid cocaineinduced regulation of striatal dopamine transporter function. Neuropharmacology 58: 605-612.
Marinelli M, Cooper DC, Baker LK, White FJ (2003). Impulse activity of midbrain dopamine neurons modulates drug-seeking behavior. Psychopharmacology (Berl) 168: 84-98. (Pubitemid 36851166)
Marinelli M, Rudick CN, Hu XT, White FJ (2006). Excitability of dopamine neurons: modulation and physiological consequences. CNS Neurol Disord Drug Targets 5: 79-97. (Pubitemid 43803125)
Marinelli M, White FJ (2000). Enhanced vulnerability to cocaine self-administration is associated with elevated impulse activity of midbrain dopamine neurons. J Neurosci 20: 8876-8885.
Mathon DS, Kamal A, Smidt MP, Ramakers GM (2003). Modulation of cellular activity and synaptic transmission in the ventral tegmental area. Eur J Pharmacol 480: 97-115. (Pubitemid 37419969)
McCutcheon JE, White FJ, Marinelli M (2009). Individual differences in dopamine cell neuroadaptations following cocaine self-administration. Biol Psychiatry 66: 801-803.
Melis M, Mereu G, Lilliu V, Quartu M, Diana M, Gessa GL (1998). Haloperidol does not produce dopamine cell depolarizationblock in paralyzed, unanesthetized rats. Brain Res 783: 127-132. (Pubitemid 28131430)
Mercuri NB, Calabresi P, Bernardi G (1989). The mechanism of amphetamine-induced inhibition of rat substantia nigra compacta neurones investigated with intracellular recording in vitro. Br J Pharmacol 98: 127-134. (Pubitemid 19225211)
Mercuri NB, Calabresi P, Bernardi G (1991). Dopamine uptake inhibition potentiates the effects of L-DOPA on rat substantia nigra zona compacta neurons. Neurosci Lett 126: 79-82.
Mercuri NB, Calabresi P, Bernardi G (1992). The electrophysiological actions of dopamine and dopaminergic drugs on neurons of the substantia nigra pars compacta and ventral tegmental area. Life Sci 51: 711-718.
Mereu G, Fanni B, Gessa GL (1984). General anesthetics prevent dopaminergic nerve stimulation by neuroleptics. In: Usdin E, Carlsson A, Dahlstrdm A, Engel J (eds). Neurology and Neurobiology. Alan R. Liss: New York, Vol. 8B, pp 353-358.
Mereu G, Yoon KW, Boi V, Gessa GL, Naes L, Westfall TC (1987). Preferential stimulation of ventral tegmental area dopaminergic neurons by nicotine. Eur J Pharmacol 141: 395-399. (Pubitemid 17150133)
Mets B, Diaz J, Soo E, Jamdar S (1999). Cocaine, norcocaine, ecgonine methylester and benzoylecgonine pharmacokinetics in the rat. Life Sci 65: 1317-1328. (Pubitemid 29425968)
Nelson AM, Larson GA, Zahniser NR (2009). Low or high cocaine responding rats differ in striatal extracellular dopamine levels and dopamine transporter number. J Pharmacol Exp Ther 331: 985-997.
Nicoll RA, Madison DV (1982). General anesthetics hyperpolarize neurons in the vertebrate central nervous system. Science 217: 1055-1057. (Pubitemid 12059106)
O'Dell LE, Khroyan TV, Neisewander JL (1996). Dose-dependent characterization of the rewarding and stimulant properties of cocaine following intraperitoneal and intravenous administration in rats. Psychopharmacology (Berl) 123: 144-153. (Pubitemid 26041912)
O'Leary ME, Chahine M (2002). Cocaine binds to a common site on open and inactivated human heart (Na(v)1.5) sodium channels. J Physiol 541(Part 3): 701-716. (Pubitemid 35190234)
Pan WH, Lai YJ, Chen NH (1995). Differential effects of chloral hydrate and pentobarbital sodium on a cocaine level and its catecholamine response in the medial prefrontal cortex: a comparison with conscious rats. J Neurochem 64: 2653-2659.
Pederson CL, Wolske M, Peoples LL, West MO (1997). Firing rate dependent effect of cocaine on single neurons of the rat lateral striatum. Brain Res 760: 261-265 (Pubitemid 27304162)
Peoples LL, Gee F, Bibi R, West MO (1998). Phasic firing time locked to cocaine self-infusion and locomotion: dissociable firing patterns of single nucleus accumbens neurons in the rat. J Neurosci 18: 7588-7598. (Pubitemid 28425840)
Peoples LL, West MO (1996). Phasic firing of single neurons in the rat nucleus accumbens correlated with the timing of intravenous cocaine self-administration. J Neurosci 16: 3459-3473. (Pubitemid 26142375)
Piazza PV, Deminiere JM, Le Moal M, Simon H (1989). Factors that predict individual vulnerability to amphetamine self-administration. Science 245: 1511-1513. (Pubitemid 19243245)
Piazza PV, Deminiere JM, Maccari S, Mormede P, Le Moal M, Simon H (1990). Individual reactivity to novelty predicts probability of amphetamine self-administration. Behav Pharmacol 1: 339-345.
Piazza PV, Deroche-Gamonent V, Rouge-Pont F, Le Moal M (2000). Vertical shifts in self-administration dose-response functions predict a drug-vulnerable phenotype predisposed to addiction. J Neurosci 20: 4226-4232. (Pubitemid 30365693)
Pierce RC, Kumaresan V (2006). The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev 30: 215-238. (Pubitemid 41821810)
Pierre PJ, Vezina P (1997). Predisposition to self-administer amphetamine: the contribution of response to novelty and prior exposure to the drug. Psychopharmacology (Berl) 129: 277-284. (Pubitemid 27085399)
Porrino LJ (1993). Functional consequences of acute cocaine treatment depend on route of administration. Psychopharmacology (Berl) 112: 343-351. (Pubitemid 23278299)
Reith ME, Li MY, Yan QS (1997a). 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. Psychopharmacology (Berl) 134: 309-317. (Pubitemid 27520985)
Reith ME, Meisler BE, Sershen H, Lajtha A (1986). Structural requirements for cocaine congeners to interact with dopamine and serotonin uptake sites in mouse brain and to induce stereotyped behavior. Biochem Pharmacol 35: 1123-1129. (Pubitemid 16075529)
Reith ME, Xu C, Chen NH (1997b). Pharmacology and regulation of the neuronal dopamine transporter. Eur J Pharmacol 324: 1-10. (Pubitemid 27160902)
Richelson E, Pfenning M (1984). Blockade by antidepressants and related compounds of biogenic amine uptake into rat brain synaptosomes: most antidepressants selectively block norepinephrine uptake. Eur J Pharmacol 104: 277-286. (Pubitemid 14006365)
Ritz MC, Cone EJ, Kuhar MJ (1990). Cocaine inhibition of ligand binding at dopamine, norepinephrine and serotonin transporters: a structure-activity study. Life Sci 46: 635-645. (Pubitemid 20056887)
Ross SB, Renyi AL (1967). Inhibition of the uptake of tritiated catecholamines by antidepressant and related agents. Eur J Pharmacol 2: 181-186.
Sabeti J, Gerhardt GA, Zahniser NR (2002). Acute cocaine differentially alters accumbens and striatal dopamine clearance in low and high cocaine locomotor responders: behavioral and electrochemical recordings in freely moving rats. J Pharmacol Exp Ther 302: 1201-1211. (Pubitemid 34920244)
Schilstrom B, Yaka R, Argilli E, Suvarna N, Schumann J, Chen BT et al (2006). Cocaine enhances NMDA receptor-mediated currents in ventral tegmental area cells via dopamine D5 receptor-dependent redistribution of NMDA receptors. J Neurosci 26: 8549-8558. (Pubitemid 44316184)
Shepard PD, German DC (1988). Electrophysiological and pharmacological evidence for the existence of distinct subpopulations of nigrostriatal dopaminergic neuron in the rat. Neuroscience 27: 537-546.
Steffensen SC, Taylor SR, Horton ML, Barber EN, Lyle LT, Stobbs SH et al (2008). Cocaine disinhibits dopamine neurons in the ventral tegmental area via use-dependent blockade of GABA neuron voltage-sensitive sodium channels. Eur J Neurosci 28: 2028-2040.
Stoffel EC, Cunningham KA (2008). The relationship between the locomotor response to a novel environment and behavioral disinhibition in rats. Drug Alcohol Depend 92: 69-78. (Pubitemid 350213237)
Strichartz G (1976). Molecular mechanisms of nerve block by local anesthetics. Anesthesiology 45: 421-441.
Stuber GD, Wightman RM, Carelli RM (2005). Extinction of cocaine self-administration reveals functionally and temporally distinct dopaminergic signals in the nucleus accumbens. Neuron 46: 661-669. (Pubitemid 40797389)
Swanson LW (1982). The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9: 321-353. (Pubitemid 13225278)
Thierry AM, Tassin JP, Blanc G, Glowinski J (1976). Selective activation of mesocortical DA system by stress. Nature 263: 242-244.
Trulson ME, Trulson VM (1983a). Chloral hydrate anesthesia alters the responsiveness of dorsal raphe neurons to psychoactive drugs. Life Sci 32: 949-956. (Pubitemid 13193205)
Trulson ME, Trulson VM (1983b). Chloral hydrate anesthesia blocks the excitatory response of dorsal raphe neurons to phasic auditory and visual stimuli in cats. Brain Res 265: 129-133. (Pubitemid 13120297)
Ungless MA, Whistler JL, Malenka RC, Bonci A (2001). Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411: 583-587. (Pubitemid 32531404)
Vezina P (2004). Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci Biobehav Rev 27: 827-839. (Pubitemid 38199613)
Wang RY (1981). Dopaminergic neurons in the rat ventral tegmental area. II. Evidence for autoregulation. Brain Res Rev 3: 141-151.
Warenycia MW, McKenzie GM (1984). Responses of striatal neurons to anesthetics and analgesics in freely moving rats. Gen Pharmacol 15: 517-522. (Pubitemid 15197579)
Westerink BH, Lejeune B, Korf J, Van Praag HM (1977). On the significance of regional dopamine metabolism in the rat brain for the claksification of centrally acting drugs. Eur J Pharmacol 42: 179-190. (Pubitemid 8053606)
White FJ (1996). Synaptic regulation of mesocorticolimbic dopamine neurons. Annu Rev Neurosci 19: 405-436. (Pubitemid 26080834)
White FJ, Kalivas PW (1998a). Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Depend 51: 141-153. (Pubitemid 28353762)
White FJ, Wang RY (1983). Comparison of the effects of LSD and lisuride on A10 dopamine neurons in the rat. Neuropharmacology 22: 669-676. (Pubitemid 13069039)
White FJ, Wang RY (1984a). A10 dopamine neurons: role of autoreceptors in determining firing rate and sensitivity to dopamine agonists. Life Sci 34: 1161-1170. (Pubitemid 14161730)
White FJ, Wang RY (1984b). Pharmacological characterization of dopamine autoreceptors in the rat ventral tegmental area: microiontophoretic studies. J Pharmacol Exp Ther 231: 275-280. (Pubitemid 15213833)
White FJ, Wang RY (1986). Electrophysiological evidence for the existence of both D-1 and D-2 dopamine receptors in the rat nucleus accumbens. J Neurosci 6: 274-280. (Pubitemid 16149240)
White IM, Doubles L, Rebec GV (1998b). Cocaine-induced activation of striatal neurons during focused stereotypy in rats. Brain Res 810: 146-152. (Pubitemid 29003400)
Windels F, Kiyatkin EA (2006). General anesthesia as a factor affecting impulse activity and neuronal responses to putative neurotransmitters. Brain Res 1086: 104-116.
Wise RA, Bozarth MA (1984). Brain reward circuitry: four circuit elements 'wired' in apparent series. Brain Res Bull 12: 203-208. (Pubitemid 14104723)