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Neurochemistry and Molecular Neurobiology of Reward

  • J. B. Becker
  • R. L. Meisel

Abstract:

The reward system consists of multiple interactive neural systems. This chapter provides an overview of the neurotransmitters and brain regions involved with reward. The neural systems important for reward include brain areas involved in learning that a stimulus is rewarding or associated with reward and separate neural systems that mediate “wanting” and “liking” for a stimulus. The ascending dopamine systems are thought to be necessary for “wanting,” whereas “liking” is mediated by GABAergic and opioid neurons in the nucleus accumbens shell in association with the ventral pallidum and parabrachial nucleus. The specific systems and molecular mechanisms mediating food reward versus the rewarding aspects of drugs of abuse are discussed. Sex differences in the reward system are highlighted.

Notes

Acknowledgments

This research was supported by grants from the USPHS to JBB (DA12677 & NS48141) and to RLM (DA 13680).

References

  1. Ackerman JM, White FJ. 1990. A10 somatodendritic dopamine autoreceptor sensitivity following withdrawal from repeated cocaine treatment. Neurosci Lett 117: 181–187.PubMedGoogle Scholar
  2. Adams JP, Roberson ED, English JD, Selcher JC, Sweatt JD. 2000. MAPK regulation of gene expression in the central nervous system. Acta Neurobiol Exp 60: 377–394.Google Scholar
  3. Adler NT. 1969. Effects of the male's copulatory behavior on successful pregnancy of the female rat. J Comp Physiol Psychol 69: 613–622.PubMedGoogle Scholar
  4. Adler NT. 1974. The behavioral control of reproductive physiology. Adv Behav Biol 11: 259–286.PubMedGoogle Scholar
  5. Adler NT. 1978. On the mechanisms of sexual behavior and their evolutionary constraints. Hutchison JB, (ed) Biological determinants of sexual behavior. New York: Wiley; pp. 657–694.Google Scholar
  6. Akiyama G, Ikeda H, Matsuzaki S, Sato M, Moribe S, et al. 2004. GABAA and GABAB receptors in the nucleus accumbens shell differentially modulate dopamine and acetylcholine receptor-mediated turning behaviour. Neuropharmacology 46: 1082–1088.PubMedGoogle Scholar
  7. Alburges ME, Narang N, Wamsley JK. 1993. Alterations in the dopaminergic receptor system after chronic administration of cocaine. Synapse 14: 314–323.PubMedGoogle Scholar
  8. Almeida OF, Shoaib M, Deicke J, Fischer D, Darwish MH, et al. 1998. Gender differences in ethanol preference and ingestion in rats. The role of the gonadal steroid environment. J Clin Invest 101: 2677–85.PubMedCentralPubMedGoogle Scholar
  9. Anden NE, Dahlstrom A, Fuxe K, Larsson K, Olson L, et al. 1966. Ascending monoamine neurons to the telencephalon and diencephalon. Act Physiol Scand 67: 313–323.Google Scholar
  10. Andrzejewski ME, Sadeghian K, Kelley AE. 2004. Central amygdalar and dorsal striatal NMDA receptor involvement in instrumental learning and spontaneous behavior. Behav Neurosci 118: 715–729.PubMedCentralPubMedGoogle Scholar
  11. Ashby CR Jr, Rohatgi R, Ngosuwan J, Borda T, Gerasimov MR, et al. 1999. Implication of the GABA(B) receptor in gamma vinyl-GABA's inhibition of cocaine-induced increases in nucleus accumbens dopamine. Synapse 31: 151–153.PubMedGoogle Scholar
  12. Backes E, Hemby SE. 2003. Discrete cell gene profiling of ventral tegmental dopamine neurons after acute and chronic cocaine self-administration. J Pharmacol Exp Ther 307: 450–459.PubMedCentralPubMedGoogle Scholar
  13. Barr AM, Fiorino DF, Phillips AG. 1999. Effects of withdrawal from an escalating dose schedule of d-amphetamine on sexual behavior in the male rat. Pharmacol Biochem Behav 64: 597–604.PubMedGoogle Scholar
  14. Bassareo V, De Luca M, Di Chiara G. 2002. Differential expression of motivational stimulus properties by doamine in the nucleus accumbens shell versus core and prefrontal cortex. J Neurosci 22: 4709–4719.PubMedGoogle Scholar
  15. Bates MD, Senogles SE, Bunzow JR, Liggett SB, Civelli O, et al. 1991. Regulation of responsiveness at D2 dopamine receptors by receptor desensitization and adenylyl cyclase sensitization. Mol Pharmacol 39: 55–63.PubMedGoogle Scholar
  16. Battisti JJ, Uretsky NJ, Wallace LJ. 2000. NMDA glutamate receptor role in the development of context-dependent and independent sensitization of the induction of stereotypy by amphetamine or apomorphine. Behav Brain Res 114: 167–174.PubMedGoogle Scholar
  17. Bazzett TJ, Becker JB. 1994. Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding. Brain Res 637: 163-172.Google Scholar
  18. Becker JB. 1999. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64: 803–812.PubMedGoogle Scholar
  19. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, et al. 2005. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146: 1650–1673.PubMedGoogle Scholar
  20. Becker JB, Beer ME. 1986. The influence of estrogen on nigrostriatal dopamine activity: Behavioral and neurochemical evidence for both pre- and postsynaptic components. Behav Brain Res 19: 27–33.PubMedGoogle Scholar
  21. Becker JB, Ramirez VD. 1981. Sex differences in the amphetamine stimulated release of catecholamines from rat striatal tissue in vitro. Brain Res 204: 361–372.PubMedGoogle Scholar
  22. Becker JB, Rudick CN, Jenkins WJ. 2001. The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. J Neurosci 21: 3236–3241.PubMedGoogle Scholar
  23. Beninger RJ, Nakonechny PL, Savina I. 2003. cAMP-dependent protein kinase and reward-related learning: Intra-accumbens Rp-cAMPS blocks amphetamine-produced place conditioning in rats. Psychopharmacology 170: 23–32.PubMedGoogle Scholar
  24. Bermant G. 1961. Response latencies of female rats during sexual intercourse. Science 133: 1771–1773.PubMedGoogle Scholar
  25. Berridge KC.1996. Food reward: Brain substrates of wanting and liking. Neurosci Biobehav Rev 20: 1–25.PubMedGoogle Scholar
  26. Berridge KC. 2003. Pleasures of the brain. Brain Cogn 52: 106–128.PubMedGoogle Scholar
  27. Berridge KC, Robinson TE. 1995. The mind of an addicted brain: Neural sensitization of wanting versus liking. Curr Direct Psychol Sci 4: 71–76.Google Scholar
  28. Berridge KC, Robinson TE. 1998a. What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Res Rev 28: 309-369.Google Scholar
  29. Berridge KC, Robinson TE. 1998b. The role of dopamine in reward: Hedonics, learning and incentive salience after 6-hyproxydopamine lesions. Brain Res Rev 28: 309–369.PubMedGoogle Scholar
  30. Berridge KC, Robinson TE. 2003. Parsing reward. Trends Neurosci 26: 507–515.PubMedGoogle Scholar
  31. Berridge KC, Venier IL, Robinson TE. 1989. Taste reactivity analysis of 6-hydroxydopamine-induced aphagia: Implications for arousal and anhedonia hypotheses of dopamine function. Behav Neurosci 103: 36–45.PubMedGoogle Scholar
  32. Berridge KC, Winkielman P. 2003. What is an unconscious emotion? (The case for unconscious “liking”). Cognition and Emotion 17: 181–211.Google Scholar
  33. Bibb JA. 2003. Role of Cdk5 in neuronal signaling, plasticity, and drug abuse. Neurosignals 12: 191–199.PubMedGoogle Scholar
  34. Bonhomme N, Cador M, Stinus L, Le Moal M, Spampinato U. 1995. Short and long-term changes in dopamine and serotonin receptor binding sites in amphetamine-sensitized rats: A quantitative autoradiographic study. Brain Res 675: 215–223.PubMedGoogle Scholar
  35. Boulay D, Duterte-Boucher D, Leroux-Nicollet I, Naudon L, Costentin J. 1996. Locomotor sensitization and decrease in [3H]mazindol binding to the dopamine transporter in the nucleus accumbens are delayed after chronic treatments by GBR12783 or cocaine. J Pharmacol Exp Ther 278: 330–337.PubMedGoogle Scholar
  36. Bowery NG. 1993. GABAB receptor pharmacology. Annu Rev Pharmacol Toxicol 33: 109–147.PubMedGoogle Scholar
  37. Bradley KC, Meisel RL. 2001. Sexual behavior induction of c-Fos in the nucleus accumbens and amphetamine-stimulated locomotor activity are sensitized by previous sexual experience in female Syrian hamsters. J Neurosci 21: 2123–2130.PubMedGoogle Scholar
  38. Bradley KC, Mullins AJ, Meisel RL, Watts VJ. 2004. Sexual experience alters D1 receptor-mediated cyclic AMP production in the nucleus accumbens of female Syrian hamsters. Synapse 53: 20–27.PubMedGoogle Scholar
  39. Brebner K, Phelan R, Roberts DC. 2000. Intra-VTA baclofen attenuates cocaine self-administration on a progressive ratio schedule of reinforcement. Pharmacol Biochem Behav 66: 857–862.PubMedGoogle Scholar
  40. Breysse N, Baunez C, Spooren W, Gasparini F, Amalric M. 2002. Chronic but not acute treatment with a metabotropic glutamate 5 receptor antagonist reverses the akinetic deficits in a rat model of parkinsonism. J Neurosci 22: 5669–5678.PubMedGoogle Scholar
  41. Brog JS, Salyapongse A, Deutch AY, Zahm DS. 1993. The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338: 255–278.PubMedGoogle Scholar
  42. Brown RW, Gonzalez CL, Kolb B. 2000. Nicotine improves Morris water task performance in rats given medial frontal cortex lesions. Pharmacol Biochem Behav 67: 473–478.PubMedGoogle Scholar
  43. Brown RW, Gonzalez CL, Whishaw IQ, Kolb B. 2001. Nicotine improvement of Morris water task performance after fimbria-fornix lesion is blocked by mecamylamine. Behav Brain Res 119: 185–192.PubMedGoogle Scholar
  44. Brown RW, Kolb B. 2001. Nicotine sensitization increases dendritic length and spine density in the nucleus accumbens and cingulate cortex. Brain Res 899: 94–100.PubMedGoogle Scholar
  45. Burns LH, Everitt BJ, Kelley AE, Robbins TW. 1994. Glutamate-dopamine interactions in the ventral striatum: Role in locomotor activity and responding with conditioned reinforcement. Psychopharmacology 115: 516–528.PubMedGoogle Scholar
  46. Cador M, Robbins TW, Everitt BJ. 1989. Involvement of the amygdala in stimulus-reward associations: Interaction with the ventral striatum. Neuroscience 30: 77–86.PubMedGoogle Scholar
  47. Camp DM, Robinson TE. 1988a. Susceptibility to sensitization. II. The influence of gonadal hormones on enduring changes in brain monoamines and behavior produced by the repeated administration of D-amphetamine or restraint stress. Behav Brain Res 30: 69–88.PubMedGoogle Scholar
  48. Camp DM, Robinson TE. 1988b. Susceptibility to sensitization. I. Sex differences in the enduring effects of chronic D-amphetamine treatment on locomotion, stereotyped behavior and brain monoamines. Behav Brain Res 30: 55–68.PubMedGoogle Scholar
  49. Cannon CM, Abdallah L, Tecott LH, During MJ, Palmiter RD. 2004. Dysregulation of striatal dopamine signaling by amphetamine inhibits feeding by hungry mice. Neuron 44: 509–520.PubMedGoogle Scholar
  50. Cardinal RN, Everitt BJ. 2004. Neural and psychological mechanisms underlying appetitive learning: Links to drug addiction. Curr Opin Neurobiol 14: 156–162.PubMedGoogle Scholar
  51. Carelli RM. 2004. Nucleus accumbens cell firing and rapid dopamine signaling during goal-directed behaviors in rats. Neuropharmacology 47: 180–189.PubMedGoogle Scholar
  52. Carelli RM, Ijames SG, Crumling AJ. 2000. Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus “natural” (water and food) reward. J Neurosci 20: 4255–4266.PubMedGoogle Scholar
  53. Carelli RM, Williams JG, Hollander JA. 2003. Basolateral amygdala neurons encode cocaine self-administration and cocaine-associated cues. J Neurosci 23: 8204–8211.PubMedGoogle Scholar
  54. Carlezon WA Jr, Nestler EJ. 2002. Elevated levels of GluR1 in the midbrain: A trigger for sensitization to drugs of abuse? Trends Neurosci 25: 610–615.PubMedGoogle Scholar
  55. Carlisle HJ, Kennedy MB. 2005. Spine architecture and synaptic plasticity. Trends Neurosci 28: 182–187.PubMedGoogle Scholar
  56. Carroll ME, Lynch W, Roth M, Morgan A, Cosgrove K. 2004. Sex and estrogen influence drug abuse. Trends Pharmacol Sci 25: 273–279.PubMedGoogle Scholar
  57. Carroll ME, Morgan AD, Lynch WJ, Campbell UC, Dess NK. 2002. Intravenous cocaine and heroin self-administration in rats selectively bred for differential saccharin intake: Phenotype and sex differences. Psychopharmacology 161: 304–313.PubMedGoogle Scholar
  58. Carroll R, Zukin R. 2002. NMDA-receptor trafficking and targeting: Implications for synaptic transmission and plasticity. Trends Neurosci 25: 571–577.PubMedGoogle Scholar
  59. Cartmell J, Monn JA, Schoepp DD. 2000. The mGlu(2/3) receptor agonist LY379268 selectively blocks amphetamine ambulations and rearing. Eur J Pharmacol 400: 221–224.PubMedGoogle Scholar
  60. Cass WA, Gerhardt GA, Gillespie K, Curella P, Mayfield RD et al. 1993. Reduced clearance of exogenous dopamine in rat nucleus accumbens, but not in dorsal striatum, following cocaine challenge in rats withdrawn from repeated cocaine administration. J Neurochem 61: 273–283.PubMedGoogle Scholar
  61. Chen JC, Su HJ, Huang LI, Hsieh MM. 1999. Reductions in binding and functions of D2 dopamine receptors in the rat ventral striatum during amphetamine sensitization. Life Sci 64: 343–354.PubMedGoogle Scholar
  62. Chiang YC, Chen PC, Chen JC. 2003. D(3) dopamine receptors are down-regulated in amphetamine sensitized rats and their putative antagonists modulate the locomotor sensitization to amphetamine. Brain Res 972: 159–167.PubMedGoogle Scholar
  63. Choi KH, Zarandi B, Todd KG, Biondo AM, Greenshaw AJ. 2000. Effects of AMPA/kainate receptor blockade on responses to dopamine receptor agonists in the core and shell of the rat nucleus accumbens. Psychopharmacology 150: 102–111.PubMedGoogle Scholar
  64. Chuhma N, Zhang H, Masson J, Zhuang X, Sulzer D, et al. 2004. Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J Neurosci 24: 972–981.PubMedGoogle Scholar
  65. Churchill L, Swanson CJ, Urbina M, Kalivas PW. 1999. Repeated cocaine alters glutamate receptor subunit levels in the nucleus accumbens and ventral tegmental area of rats that develop behavioral sensitization. J Neurochem 72: 2397–2403.PubMedGoogle Scholar
  66. Colby CR, Whisler K, Steffen C, Nestler EJ, Self DW. 2003. Striatal cell type-specific overexpression of ΔFosB enhances incentive for cocaine. J Neurosci 23: 2488–2493.PubMedGoogle Scholar
  67. Coppola D, O'Connell R. 1988. Are pheromones their own reward? Physiol Behav 44: 811–816.PubMedGoogle Scholar
  68. Cruz HG, Ivanova T, Lunn ML, Stoffel M, Slesinger PA, et al. 2004. Bi-directional effects of GABA(B) receptor agonists on the mesolimbic dopamine system. Nature Neurosci 7: 153–159.PubMedGoogle Scholar
  69. Damsma G, Pfaus JG, Wenkstern D, Phillips AG, Fibiger HC. 1992. Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: Comparison with novelty and locomotion. Behav Neurosci 106: 181–191.PubMedGoogle Scholar
  70. Danysz W, Essmann U, Bresink I, Wilke R. 1994. Glutamate antagonists have different effects on spontaneous locomotor activity in rats. Pharmacol Biochem Behav 48: 111–118.PubMedGoogle Scholar
  71. Darracq L, Drouin C, Blanc G, Glowinski J, Tassin JP. 2001. Stimulation of metabotropic but not ionotropic glutamatergic receptors in the nucleus accumbens is required for the D-amphetamine-induced release of functional dopamine. Neuroscience 103: 395–403.PubMedGoogle Scholar
  72. David HN, Abraini JH. 2003. Blockade of the locomotor stimulant effects of amphetamine by group I, group II, and group III metabotropic glutamate receptor ligands in the rat nucleus accumbens: Possible interactions with dopamine receptors. Neuropharmacology 44: 717–727.PubMedGoogle Scholar
  73. David HN, Sissaoui K, Abraini JH. 2004. Modulation of the locomotor responses induced by D1-like and D2-like dopamine receptor agonists and D-amphetamine by NMDA and non-NMDA glutamate receptor agonists and antagonists in the core of the rat nucleus accumbens. Neuropharmacology 46: 179–191.PubMedGoogle Scholar
  74. Davis CM, Moskovitz B, Nguyen MA, Tran BB, Arai A, et al. 1997. A profile of the behavioral changes produced by facilitation of AMPA-type glutamate receptors. Psychopharmacology 133: 161–167.PubMedGoogle Scholar
  75. de Jong JG, Wasilewski M, Vegt van der BJ, Buwalda B, Koolhaas JM. 2005. A single social defeat induces short-lasting behavioral sensitization to amphetamine. Physiol Behav 83: 805–811.PubMedGoogle Scholar
  76. DeMontis MG, Gambarana C, Gessa GL, Meloni D, Tagliamonte A, Stefanini E. 1993. Reduced [3H]SCH 23390 binding and DA-sensitive adenylyl cyclase in the limbic system of ethanol-preferring rats. Alcohol 28: 387–400.Google Scholar
  77. Devaud LL, Alele P. 2004. Differential effects of chronic ethanol administration and withdrawal on gamma-aminobutyric acid type A and NMDA receptor subunit proteins in male and female rat brain. Alcohol Clin Exp Res 28: 957–65.PubMedGoogle Scholar
  78. Devaud LL, Alele P, Ritu C. 2003. Sex differences in the central nervous system actions of ethanol. Crit Rev Neurobiol 15: 41–59.PubMedGoogle Scholar
  79. Devaud LL, Chadda R. 2001. Sex differences in rats in the development of and recovery from ethanol dependence assessed by changes in seizure susceptibility. Alcohol Clin Exp Res 25: 1689–96.PubMedGoogle Scholar
  80. Dewey SL, Morgan AE, Ashby CR Jr, Horan B, Kushner SA, et al. 1998. A novel strategy for the treatment of cocaine addiction. Synapse 30: 119–129.PubMedGoogle Scholar
  81. Di Chiara G. 1998. A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J Psychopharmacol 12: 54–67.PubMedGoogle Scholar
  82. Di Chiara G. 2002. Nucleus accumbens shell and core dopamine: Differential role in behavior and addiction. Behav Brain Res 137: 75–114.PubMedGoogle Scholar
  83. Di Paolo T, Levesque D, Daigle M. 1986. A physiological dose of progesterone affects rat striatum biogenic amine metabolism. Eur J Pharmacol 125: 11–16.PubMedGoogle Scholar
  84. Di Paolo T, Poyet P, Labrie F. 1981. Effect of chronic estradiol and haloperidol treatment on striatal dopamine receptors. Eur J Pharmacol 73: 105–106.PubMedGoogle Scholar
  85. Dluzen DE, Ramirez VD. 1984. Bimodal effect of progesterone on in vitro dopamine function of the rat corpus striatum. Neuroendocrinol 39: 149–155.Google Scholar
  86. Dluzen DE, Ramirez VD. 1990. In vitro progesterone modulation of amphetamine-stimulated dopamine release from the corpus striatum of ovariectomized estrogen-treated female rats: Response characteristics. Brain Res 517: 117–122.PubMedGoogle Scholar
  87. Erskine MS. 1989. Solicitation behavior in the estrous female rat: A review. Horm Behav 23: 473–502.PubMedGoogle Scholar
  88. Erskine MS. 1995. Prolactin release after mating and genitosensory stimulation in females. Endocr Rev 16: 508–528.PubMedGoogle Scholar
  89. Erskine MS, Kornberg E, Cherry JA. 1989. Paced copulation in rats: Effects of intromission frequency and duration on luteal activation and estrus length. Physiol Behav 45: 33–39.PubMedGoogle Scholar
  90. Everitt BJ. 1990. Sexual motivation: A neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev 14: 217–232.PubMedGoogle Scholar
  91. Everitt BJ, Cador M, Robbins TW. 1989. Interactions between the amygdala and ventral striatum in stimulus-reward associations: Studies using a second-order schedule of sexual reinforcement. Neuroscience 30: 63–75.PubMedGoogle Scholar
  92. Everitt BJ, Stacey P. 1987. Studies of instrumental behaviour with sexual reinforcement in male rats (Rattus norvegicus): II Effects of preoptic area lesions, castration and testosterone. J Comp Psychol 101: 407–419.PubMedGoogle Scholar
  93. Fadda P, Scherma M, Fresu A, Collu M, Fratta W. 2003. Baclofen antagonizes nicotine-, cocaine-, and morphine-induced dopamine release in the nucleus accumbens of rat. Synapse 50: 1–6.PubMedGoogle Scholar
  94. Faleiro L, Jones S, Kauer J. 2004. Rapid synaptic plasticity of glutamatergic synapses on dopamine neurons in the ventral tegmental area in response to acute amphetamine injection. Neuropsychopharmacology 29: 2115–2125.PubMedGoogle Scholar
  95. Fiorillo C, Tobler P, Schultz W. 2003. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299: 1898–1902.PubMedGoogle Scholar
  96. Fiorino DF, Kolb BS. 2003. Sexual experience leads to long-lasting morphological changes in male rat prefrontal cortex, pareital cortex, and nucleus accumbens neurons. Society for neuroscience. New Orleans, LA: 2003 Abstract Viewer and Itinerary Planner. Washington, DC.Google Scholar
  97. Fiorino DF, Phillips AG. 1999a. Facilitation of sexual behavior in male rats following d-amphetamine-induced behavioral sensitization. Psychopharmacology 142: 200–208.PubMedGoogle Scholar
  98. Fiorino DF, Phillips AG. 1999b. Facilitation of sexual behavior and enhanced dopamine efflux in the nucleus accumbens of male rats after D-amphetamine-induced behavioral sensitization. J Neurosci 19: 456–463.PubMedGoogle Scholar
  99. Fischer JF, Cho AK. 1976. Properties of dopamine efflux from rat striatal tissue caused by amphetamine and p-hydroxyamphetamine. Proc West Pharmacol Soc 19: 179–182.PubMedGoogle Scholar
  100. Flanagan LM, Pfaus JG, Pfaff DW, McEwen BS. 1993. Induction of FOS immunoreactivity in oxytocin neurons after sexual activity in female rats. Neuroendocrinology 58: 352–358.PubMedGoogle Scholar
  101. Floresco SB, West AR, Ash B, Moore H, Grace AA. 2003. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6: 968–973.PubMedGoogle Scholar
  102. Forgie ML, Stewart J. 1994. Sex differenc in amphetamine-induced locomotor activity in adult rats: Role of tetosterone exposure in the neonatal period. Pharmacol Biochem Behav 46: 637–645.Google Scholar
  103. Freeman WM, Brebner K, Lynch WJ, Robertson DJ, Roberts DC, et al. 2001. Cocaine-responsive gene expression changes in rat hippocampus. Neuroscience 108: 371–380.PubMedGoogle Scholar
  104. Galef BJ, Whiskin E. 2003. Socially transmitted food preferences can be used to study long-term memory in rats. Learn Behav 31: 160–164.PubMedGoogle Scholar
  105. Garcia-Horsman P, Paredes RG. 2004. Dopamine antagonists do not block conditioned place preference induced by paced mating behavior in female rats. Behav Neurosci 118: 356–364.PubMedGoogle Scholar
  106. Gerdjikov TV, Ross GM, Beninger RJ. 2004. Place preference induced by nucleus accumbens amphetamine is impaired by antagonists of ERK or p38 MAP kinases in rats. Behav Neurosci 118: 740–750.PubMedGoogle Scholar
  107. Ghasemzadeh MB, Nelson LC, Lu XY, Kalivas PW. 1999. Neuroadaptations in ionotropic and metabotropic glutamate receptor mRNA produced by cocaine treatment. J Neurochem 72: 157–165.PubMedGoogle Scholar
  108. Giertler C, Bohn I, Hauber W. 2005. Involvement of NMDA and AMPA/KA receptors in the nucleus accumbens core in instrumental learning guided by reward-predictive cues. Eur J Neurosci 21: 1689–1702.PubMedGoogle Scholar
  109. Gilman DP, Mercer LF, Hitt JC. 1979. Influence of female copulatory behavor on the induction of pseudopregnancy in the female rat. Physiol Behav 22: 675–678.PubMedGoogle Scholar
  110. Giorgetti M, Hotsenpiller G, Froestl W, Wolf ME. 2002. In vivo modulation of ventral tegmental area dopamine and glutamate efflux by local GABA(B) receptors is altered after repeated amphetamine treatment. Neuroscience 109: 585–595.PubMedGoogle Scholar
  111. Giorgetti M, Hotsenpiller G, Ward P, Teppen T, Wolf ME. 2001. Amphetamine-induced plasticity of AMPA receptors in the ventral tegmental area: Effects on extracellular levels of dopamine and glutamate in freely moving rats. J Neurosci 21: 6362–6369.PubMedGoogle Scholar
  112. Gonzalez-Nicolini V, McGinty JF. 2002. Gene expression profile from the striatum of amphetamine-treated rats: A cDNA array and in situ hybridization histochemical study. Brain Res Gene Expr Patterns 1: 193–198.PubMedGoogle Scholar
  113. Gordon JH. 1980. Modulation of apomorphine-induced stereotypy by estrogen: Time course and dose response. Brain Res Bull 5: 679–682.PubMedGoogle Scholar
  114. Griffin ML, Weiss RD, Lange U. 1989. A comparison of male and female cocaine abuse. Arch Gen Psychiatry 46: 122–126.PubMedGoogle Scholar
  115. 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.PubMedGoogle Scholar
  116. Harris GC, Aston-Jones G. 2003. Critical role for ventral tegmental glutamate in preference for a cocaine-conditioned environment. Neuropsychopharmacology 28: 73–76.PubMedGoogle Scholar
  117. Harris GC, Wimmer M, Byrne R, Aston-Jones G. 2004. Glutamate-associated plasticity in the ventral tegmental area is necessary for conditioning environmental stimuli with morphine. Neuroscience 129: 841–847.PubMedGoogle Scholar
  118. Hecht GS, Spear NE, Spear LP. 1999. Changes in progressive ratio responding for intravenous cocaine throughout the reproductive process in female rats. Dev Psychobiol 35: 136–145.PubMedGoogle Scholar
  119. Heikkila RE, Orlansky H, Mytilineou C, Cohen G. 1975. Amphetamine: Evaluation of d- and l-isomers as releasing agents and uptake inhibitors for 3H-dopamine and 3H-norepinephrine in slices of rat neostriatum and cerebral cortex. J Pharmacol Exp Ther 194: 47–56.PubMedGoogle Scholar
  120. Henry DJ, White FJ. 1991. Repeated cocaine administration causes persistent enhancement of D1 dopamine receptor sensitivity within the rat nucleus accumbens. J Pharmacol Exp Ther 258: 882–890.PubMedGoogle Scholar
  121. Henry SA, Lehmann-Masten V, Gasparini F, Geyer MA, Markou A. 2002. The mGluR5 antagonist MPEP, but not the mGluR2/3 agonist LY314582, augments PCP effects on prepulse inhibition and locomotor activity. Neuropharmacology 43: 1199–1209.PubMedGoogle Scholar
  122. Herzig V, Schmidt WJ. 2004. Effects of MPEP on locomotion, sensitization and conditioned reward induced by cocaine or morphine. Neuropharmacology 47: 973–984.PubMedGoogle Scholar
  123. Hitry A Little KY, Ellenwood EH Jr. 1996. Effect of cocaine on dopamine transporter receptors depends on routes of chronic cocaine administration. Neuropsychopharmacology 14: 205–210.Google Scholar
  124. Horger BA, Iyasere CA, Berhow MT, Messer CJ, Nestler EJ, et al. 1999. Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotropic factor. J Neurosci 19: 4110–4122.PubMedGoogle Scholar
  125. Hotenspiller G, Wolf ME. 2003. Baclofen attenuates conditioned locomotion to cues associated with cocaine administration and stabilizes extracellular glutamate levels in rat nucleus accumbens. Neuroscience 118: 123–134.Google Scholar
  126. Hruska RE. 1988. 17βEstradiol regulation of DA receptor interactions with G-proteins. Soc Neurosci Abstr 14: 454.Google Scholar
  127. Hruska RE, Silbergeld EK. 1980. Increased dopamine receptor sensitivity after estrogen treatment using the rat rotation model. Science 208: 1466–1468.PubMedGoogle Scholar
  128. Hu JH, Yang N, Ma YH, Zhou XG, Zhang XY, et al. 2003. Decrease of morphine-induced reward effects and withdrawal symptoms in mice overexpressing gamma-aminobutyric acid transporter I. J Neurosci Res 74: 614–621.PubMedGoogle Scholar
  129. Hu M, Crombag HS, Robinson TE, Becker JB. 2004. Biological basis of sex differences in the propensity to self-administer cocaine. Neuropsychopharmacology 29: 81–85.PubMedGoogle Scholar
  130. Hummel M, Unterwald EM. 2003. Intra-accumbens pertussis toxin sensitizes rats to the locomotor activating effects of a single cocaine challenge. Brain Res 965: 100–107.PubMedGoogle Scholar
  131. Ikemoto S, Wise RA. 2004. Mapping of chemical trigger zones for reward. Neuropharmacology 1: 190–201.Google Scholar
  132. Ito R, Dalley JW, Howes SR, Robbins TW, Everitt BJ. 2000. Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cures and during cocaine-seeking behavior in rats. J Neurosci 20: 7489–7495.PubMedGoogle Scholar
  133. Ito R, Dalley JW, Robbins TW, Everitt BJ. 2002. Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J Neurosci 22: 6247–6253.PubMedGoogle Scholar
  134. Ito R, Robbins TW, Everitt BJ. 2004. Differential control over coaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7: 389–397.PubMedGoogle Scholar
  135. Jackson LR, Robinson TE, Becker JB. 2005. Sex differences and hormonal influences on acquisition of cocaine self-administration in rats. Neuropsychopharmacology 31: 129–138.Google Scholar
  136. Jacobs E, Wardeh G, Smit A, Schoffelmeer A. 2005. Morphine causes a delayed increase in glutamate receptor functioning in the nucleus accumbens core. Eur J Pharmacol 511: 27–30.PubMedGoogle Scholar
  137. Jayaram P, Steketee JD. 2004. Effects of repeated cocaine on medial prefrontal cortical GABAB receptor modulation of neurotransmission in the mesocorticolimbic dopamine system. J Neurochem 90: 839–847.PubMedGoogle Scholar
  138. Jenkins WJ, Becker JB. 2003a. Dynamic increases in dopamine during paced copulation in the female rat. Eur J Neurosci 18: 1997–2001.PubMedGoogle Scholar
  139. Jenkins WJ, Becker JB. 2003b. Female rats develop conditioned place preferences for sex at their preferred interval. Horm Behav 43: 503–507.PubMedGoogle Scholar
  140. Jones SR, Lee TH, Wightman RM, Ellinwood EH. 1996. Effects of intermittent and continuous cocaine administration on dopamine release and uptake regulation in the striatum: In vitro voltammetric assessment. Psychopharmacology (Berl) 126: 331–338.Google Scholar
  141. Joyce JN, Smith RL, Van Hartesveldt C. 1982. Estradiol suppresses then enhances intracaudate dopamine-induced contralateral deviation. Eur J Pharmacol 81: 117–122.PubMedGoogle Scholar
  142. Jung BJ, Dawson R Jr, Sealey SA Peris J. 1999. Endogenous GABA release is reduced in the striatum of cocaine-sensitized rats. Synapse 34: 103–110.PubMedGoogle Scholar
  143. Kalivas PW, Duffy P. 1998. Repeated cocaine administration alters extracellular glutamate in the ventral tegmental area. J Neurochem 70: 1497–1502.PubMedGoogle Scholar
  144. Kandel DB, Warner MPP, Kessler RC. 1995. The epidemiology of substance abuse and dependence among women. Drug addiction research and the health of women. Wetherington CL, Roman AR, editors. Rockville, MD: US Department of Health and Human Services; pp. 105–130.Google Scholar
  145. Kanner BI. 1983. Bioenergetics of neurotransmitter transport. Biochim Biophys Acta 726: 293–316.PubMedGoogle Scholar
  146. Kaplan GB, Leite-Morris KA, Joshi M, Shoeb MH, Carey RJ. 2003. Baclofen inhibits opiate-induced conditioned place preference and associated induction of Fos in cortical and limbic regions. Brain Res 987: 122–125.PubMedGoogle Scholar
  147. Kelley AE. 2004. Ventral striatal control of appetitive motivation: Role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27: 765–776.PubMedGoogle Scholar
  148. Kelley AE, Bakshi VP, Haber SN, Steininger TL, Will MJ, et al. 2002. Opioid modulation of taste hedonics within the ventral striatum. Physiol Behav 76: 365–377.PubMedGoogle Scholar
  149. Kelley AE, Berridge KC. 2002. The neuroscience of natural rewards: Relevance to addictive drugs. J Neurosci 22: 3306–3311.PubMedGoogle Scholar
  150. Kelley AE, Throne LC. 1992. NMDA receptors mediate the behavioral effects of amphetamine infused into the nucleus accumbens. Brain Res Bull 29: 247–254.PubMedGoogle Scholar
  151. Kelz MB, Chen J, Carlezon WA Jr, Whisler K, Gilden L, et al. 1999. Expression of the transcription factor ΔFosB in the brain controls sensitivity to cocaine. Nature 401: 272–276.PubMedGoogle Scholar
  152. Kim JH, Austin JD, Tanabe L, Creekmore E, Vezina P. 2005. Activation of group II mGlu receptors blocks the enhanced drug taking induced by previous exposure to amphetamine. Eur J Neurosci 21: 295–300.PubMedGoogle Scholar
  153. Kim JH, Beeler JA, Vezina P. 2000. Group II, but not group I, metabotropic glutamate receptors in the rat nucleus accumbens contribute to amphetamine-induced locomotion. Neuropharmacology 39: 1692–1699.PubMedGoogle Scholar
  154. King GR, Ellinwood EH Jr, Silvia C, Joyner CM, Xue Z, et al. 1994. Withdrawal from continuous or intermittent cocaine administration: Changes in D2 receptor function. J Pharmacol Exp Ther 269: 743–749.PubMedGoogle Scholar
  155. Klein S, Hadamitzky M, Koch M, Schwabe K. 2004. Role of glutamate receptors in nucleus accumbens core and shell in spatial behaviour of rats. Neuroscience 128: 229–238.PubMedGoogle Scholar
  156. Kosten TA, Gawin FH, Kosten TR, Rounsaville BJ. 1993. Gender differeces in cocaine use and treatment response. J Subst Abuse Treat 10: 63–66.PubMedGoogle Scholar
  157. Kozell B, Meshul K. 2003. Alterations in nerve terminal glutamate immunoreactivity in the nucleus accumbens and ventral tegmental area following single and repeated doses of cocaine. Psychopharmacology 165: 337–345.PubMedGoogle Scholar
  158. Kozell LB, Meshul CK. 2001. The effects of acute or repeated cocaine administration on nerve terminal glutamate within the rat mesolimbic system. Neuroscience 106: 15–25.PubMedGoogle Scholar
  159. Kozell LB, Meshul CK. 2004. Nerve terminal glutamate immunoreactivity in the rat nucleus accumbens and ventral tegmental area after a short withdrawal from cocaine. Synapse 51: 224–232.PubMedGoogle Scholar
  160. Kuhar MJ, Ritz MC, Sharkey J. 1988. Cocaine receptors on dopamine transporters mediate cocaine-reinforced beahvior. NIDA Res Monogr 88: 14–22.PubMedGoogle Scholar
  161. Kushner SA, Dewey SL, Kornetsky C. 1997. Gamma-vinyl GABA attenuates cocaine-induced lowering of brain stimulation reward thresholds. Psychopharmacology 133: 383–388.PubMedGoogle Scholar
  162. Kushner SA, Dewey SL, Kornetsky C. 1999. The irreversible gamma-aminobutyric acid (GABA) transaminase inhibitor gamma-vinyl-GABA blocks cocaine self-administration in rats. J Pharmacol Exp Ther 290: 797–802.PubMedGoogle Scholar
  163. Laviolette SR, Kooy van der D. 2001. GABA(A) receptors in the ventral tegmental area control bidirectional reward signalling between dopaminergic and non-dopaminergic neural motivational systems. Eur J Neurosci 13: 1009–1015.PubMedGoogle Scholar
  164. Laviolette SR, Kooy van der D. 2004. GABAA receptors signal bidirectional reward transmission from the ventral tegmental area to the tegmental pedunculopontine nucleus as a function of opiate state. Eur J Neurosci 20: 2179–2187.PubMedGoogle Scholar
  165. Le Foll B, Diaz J, Sokoloff P. 2003. Increased dopamine D3 receptor expression accompanying behavioral sensitization to nicotine in rats. Synapse 47: 176–183.PubMedGoogle Scholar
  166. Leite-Morris KA, Fukudome EY, Shoeb MH, Kaplan GB. 2004. GABA(B) receptor activation in the ventral tegmental area inhibits the acquisition and expression of opiate-induced motor sensitization. J Pharmacol Exp Ther 308: 667–678.PubMedGoogle Scholar
  167. Leone P, Popcock D, Wise RA. 1991. Morphine-dopamine interaction: Ventral tegmental morphine increases nucleus accumbens dopamine release. Pharmacol Biochem Behav 39: 469–472.PubMedGoogle Scholar
  168. Leriche L, Schwartz JC, Sokoloff P. 2003. The dopamine D3 receptor mediates locomotor hyperactivity induced by NMDA receptor blockade. Neuropharmacology 45: 174–181.PubMedGoogle Scholar
  169. Letchworth SR, Daunais JB, Hedgecock AA, Porrino LJ. 1997. Effects of chronic cocaine administration on dopamine transporter mRNA and protein in the rat. Brain Res 750: 214–222.PubMedGoogle Scholar
  170. Letchworth SR, Nader MA, Smith HR, Friedman DP, Porrino LJ. 2001. Progression of changes in dopamine transporter binding site density as a result of cocaine self-administration in rhesus monkeys. J Neurosci 21: 2799–2807.PubMedGoogle Scholar
  171. Levitt D, Teitelbaum P. 1975. Somnolence, akinesia, and sensory activation of motivated behavior in the lateral hypothalamic syndrome. Proc Natl Acad Sci USA 72: 2819–2823.PubMedCentralPubMedGoogle Scholar
  172. Li Y, Acerbo MJ, Robinson TE. 2004 The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 20: 1647–1654.PubMedGoogle Scholar
  173. Li Y, Hu XT, Berney TG, Vartanian AJ, Stine CD, et al. 1999. Both glutamate receptor antagonists and prefrontal cortex lesions prevent induction of cocaine sensitization and associated neuroadaptations. Synapse 34: 169–180.PubMedGoogle Scholar
  174. Li Y, Kolb B, Robinson TE. 2003. The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen. Neuropsychopharmacology 28: 1082–1085.PubMedGoogle Scholar
  175. Licata SC, Freeman AY, Pierce-Bancroft AF, Pierce RC. 2000. Repeated stimulation of L-type calcium channesl in the rat ventral tremental area mimics the initiation of behavioral sensitization to cocaine. Psychopharmacology 152: 110–118.PubMedGoogle Scholar
  176. Lu W, Wolf ME. 1999. Repeated amphetamine administration alters AMPA receptor subunit expression in rat nucleus accumbens and medial prefrontal cortex. Synapse 32: 119–131.PubMedGoogle Scholar
  177. Lynch WJ, Carroll ME. 1999. Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology 144: 77–82.PubMedGoogle Scholar
  178. Lynch WJ, Roth ME, Carroll ME. 2002. Biological basis of sex differences in drug abuse: Preclinical and clinical studies. Psychopharmacology 164: 121–137.PubMedGoogle Scholar
  179. Maldonado-Irizarry CS, Kelley AE. 1994. Differential behavioral effects following microinjection of an NMDA antagonist into nucleus accumbens subregions. Psychopharmacology 116: 65–72.PubMedGoogle Scholar
  180. Mao L, Wang JQ. 2001. Differentially altered mGluR1 and mGluR5 mRNA expression in rat caudate nucleus and nucleus accumbens in the development and expression of behavioral sensitization to repeated amphetamine administration. Synapse 41: 230–240.PubMedGoogle Scholar
  181. Marrow LP, Overton PG, Brain PF, Clark D. 1999. Encounters with aggressive conspecifics enhance the locomotor-activating effects of cocaine in the rat. Addiction Biology 4: 437–441.PubMedGoogle Scholar
  182. Martinez I, Paredes RG. 2001. Only self-paced mating is rewarding in rats of both sexes. Horm Behav 40: 510–517.PubMedGoogle Scholar
  183. Masserano JM, Venable D, Wyatt RJ. 1994. Effects of chronic cocaine administration on [3H]dopamine uptake in the nucleus accumbens, striatum and frontal cortex of rats. J Pharmacol Exp Ther 270: 133–141.PubMedGoogle Scholar
  184. Matsumoto RR. 1989. GABA receptors: Are cellular differences reflected in function? Brain Res Brain Res Rev 14: 203–225.PubMedGoogle Scholar
  185. McClintock MK. 1984. Group mating in the domestic rat as context for sexual selection: Consequences for the analysis of sexual behavior and neuroendocrine responses. Adv Study of Behav 14: 1–50.Google Scholar
  186. McClintock MK, Adler NT. 1977. The role of the female during copulation in wild and domestic norway rats. Behav 67: 67–96.Google Scholar
  187. McClung CA, Nestler EJ. 2003. Regulation of gene expression and cocaine reward by CREB and δFosB. Nat Neurosci 6: 1208–1215.PubMedGoogle Scholar
  188. McGeehan AJ, Olive MF. 2003. The mGluR5 antagonist MPEP reduces the conditioned rewarding effects of cocaine but not other drugs of abuse. Synapse 47: 240–242.PubMedGoogle Scholar
  189. Mead AN, Stephens DN. 2003. Involvement of AMPA receptor GluR2 subunits in stimulus-reward learning: Evidence from glutamate receptor gria2 knock-out mice. J Neurosci 23: 9500–9507.PubMedGoogle Scholar
  190. Meisel RL, Camp DM, Robinson TE. 1993. A microdialysis study of ventral striatal dopamine during sexual behaivor in female Syrian hamsters. Behav Brain Res 55: 151–157.PubMedGoogle Scholar
  191. Meisel RL, Joppa MA, Rowe RK. 1996. Dopamine receptor antagonists attenuate conditioned place preference following sexual behavior in female Syrian hamsters. Eur J Pharmacol 309: 21–4.PubMedGoogle Scholar
  192. Mello NK. 1995. Cocaine abuse and reproductive function in women. Drug addiction research and the health of women. Wetherington CL, Roman AR, editors. Rockville, MD: US Department of Health and Human Services.Google Scholar
  193. Mendelson JH, Weiss R, Griffin M, Mirin SM, Teoh SK, et al. 1991. Some special considerations for treatment of drug abuse and dependence in women. NIDA Res Monogr 106: 313–327.PubMedGoogle Scholar
  194. Mermelstein PG, Becker JB. 1995. Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior. Behav Neurosci 109: 354–365.PubMedGoogle Scholar
  195. Meshul CK, Noguchi K, Emre N, Ellison G. 1998. Cocaine-induced changes in glutamate and GABA immunolabeling within rat habenula and nucleus accumbens. Synapse 30: 211–220.PubMedGoogle Scholar
  196. Miczek KA. 2004. Animal models of social stress and drug abuse. Biol Psychiatry 55: 193S–193S.Google Scholar
  197. Miczek KA, Covington HE, Nikulina EA, Hammer RP. 2004. Aggression and defeat: Persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27: 787–802.PubMedGoogle Scholar
  198. Mitchell JB, Stewart J. 1990. Facilitation of sexual behaviors in the male rat associated with intra-VTA injections of opiates. Pharmacol Biochem Behav 35: 643–650.PubMedGoogle Scholar
  199. Morissette M, Di Paolo T. 1993. Effect of chronic estradiol and progesterone treatments of ovariectomized rats on brain dopamine uptake sites. J Neurochem 60: 1876–1883.PubMedGoogle Scholar
  200. Mullins AJ, Sengelaub DR, Meisel RL. 2004. Effects of sexual experience in female hamsters on MAP kinase signaling and dendritic morphology. In: Society for Neuroscience. San Diego: 2004 Abstract Viewer and Itinerary Planner. Washington, DC.Google Scholar
  201. Nakagawa T, Fujio M, Ozawa T, Minami M, Satoh M. 2005. Effect of MS-153, a glutamate transporter activator, on the conditioned rewarding effects of morphine, methamphetamine and cocaine in mice. Behav Brain Res 156: 233–239.PubMedGoogle Scholar
  202. Nakayama K, Kiyosu K, Taguchi T. 2005. Diminished neuronal activity increases neuron-neuron connectivity underlying silent synapse formation and the rapid conversion of silent to functional synapses. J Neurosci 25: 4040–4051.PubMedGoogle Scholar
  203. Narita M, Aoki T, Suzuki T. 2000. Molecular evidence for the involvement of NR2B subunit containing N-methyl-D-aspartate receptors in the development of morphine-induced place preference. Neuroscience 101: 601–606.PubMedGoogle Scholar
  204. Nestby P, Schotte A, Janssen PF, Tjon GH, Vanderschuren LJ, et al. 1997. Striatal dopamine receptors in rats displaying long-term behavioural sensitization to morphine. Synapse 27: 262–265.PubMedGoogle Scholar
  205. Nestler EJ. 2002. Common molecular and cellular substrates of addiction and memory. Neurobiol Learn Mem 78: 637–647.PubMedGoogle Scholar
  206. Norrholm SD, Bobb JA, Nestler EJ, Ouimet CC, Taylor JR, et al. 2003. Cocaine-induced proliferation of dendritic spines in nucleus accumbens is dependent on the activity of cyclin-dependent kinase-5. Neuroscience 116: 19–22.PubMedCentralPubMedGoogle Scholar
  207. Oldenberger WP, Everitt BJ, de Jong FH. 1992. Conditioned place preference induced by sexual interaction in female rats. Horm Behav 26: 214–228.Google Scholar
  208. Olds J, Milner P. 1954. Positive reinforcement produced by electrical stimulationof septal area and other areas of the brain. J Comp Physiol Psychol 47: 419–427.PubMedGoogle Scholar
  209. Olds M, Olds J. 1969. Effects of lesions in the medial forebrain bundle on self-stimulation behavior. Am J Physiol 217: 1253–1264.PubMedGoogle Scholar
  210. Paladini CA, Fiorillo CD, Morikawa H, Williams JT. 2001. Amphetamine selectively blocks inhibitory glutamate transmission in dopamine neurons. Nat Neurosci 4: 275–281.PubMedGoogle Scholar
  211. Paredes RG, Alonso A. 1997. Sexual behavior regulated (paced) by the female induces conditioned place preference. Behav Neurosci 111: 123–128.PubMedGoogle Scholar
  212. Paredes RG, Martinez I. 2001. Naloxone blocks place preference conditioning after paced mating in female rats. Behav Neurosci 115: 1363–1367.PubMedGoogle Scholar
  213. Paredes RG, Vazquez B. 1999. What do female rats like about sex? Paced mating. Behav Brain Res 105: 117–127.PubMedGoogle Scholar
  214. Pecina S, Cagniard B, Berridge K, Aldridge J, Zhuang X. 2003. Hyperdopaminergic mutant mice have a higher “wanting: But not “liking” for sweet rewards. J Neurosci 23: 9395–9402.PubMedGoogle Scholar
  215. Peris J, Decambre N, Coleman-Hardee M, Simpkins J. 1991. Estradiol enhances behavioral sensitization to cocaine and amphetamine-stimulated [3H]dopamine release. Brain Res 566: 255–264.PubMedGoogle Scholar
  216. Perrine SA, Schroeder JA, Unterwald EM. 2005. Behavioral sensitization to binge-pattern cocaine administration is not associated with changes in protein levels of four major G-proteins. Brain Res Mol Brain Res 133: 224–232.PubMedGoogle Scholar
  217. Peters YM, O'Donnell P, Carelli RM. 2003. Prefrontal cortical responses during maintenance vs extinction of goal directed behavior for water reinforcement in rats. Behav Pharmacol 14: S74.Google Scholar
  218. Pfaus JG, Damsma G, Nomikos GG, Wenkstern DG, Blaha CD, et al. 1990. Sexual behavior enhances central dopamine transmission in the male rat. Brain Res 530: 345–348.PubMedGoogle Scholar
  219. Pfaus JG, Damsma G, Wenkstern D, Fibiger HC. 1995. Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats. Brain Res 693: 21–30.PubMedGoogle Scholar
  220. Pfaus JG, Kippin TE, Centeno S. 2001. Conditioning and sexual behavior: A review. Horm Behav 40: 291–321.PubMedGoogle Scholar
  221. Pfaus JG, Phillips AG. 1991. Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behav Neurosci 105: 727–743.PubMedGoogle Scholar
  222. Pierce RC, Duffy P, Kalivas PW. 1995. Sensitization to cocaine and dopamine autoreceptor subsensitivity in the nucleus accumbens. Synapse 20: 33–36.PubMedGoogle Scholar
  223. Pierce RC, Kalivas PW. 1995. Amphetamine produces sensitized increases in locomotion and extracellular dopamine preferentially in the nucleus accumbens shell of rats administered repeated cocaine. J Pharmacol Exp Ther 275: 1019–1029.PubMedGoogle Scholar
  224. Pleim ET, Matochik JA, Barfield RJ, Auerbach SB. 1990. Correlation of dopamine release in the nucleus accumbens with masculine sexual behavior in rats. Brain Res 524: 160–163.PubMedGoogle Scholar
  225. Popik P, Wrobel M. 2002. Morphine conditioned reward is inhibited by MPEP, the mGluR5 antagonist. Neuropharmacology 43: 1210–1217.PubMedGoogle Scholar
  226. Pothos E, Rada P, Mark GP, Hoebel BG. 1991. Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone-precipitated withdrawal and clonidine treatment. Brain Res 566: 348–350.PubMedGoogle Scholar
  227. Pulvirenti L, Berrier R, Kreifeldt M, Koob GF. 1994. Modulation of locomotor activity by NMDA receptors in the nucleus accumbens core and shell regions of the rat. Brain Res 664: 231–236.PubMedGoogle Scholar
  228. Quinones-Jenab V, Perrotti LI, Mc Monagle J, Ho A, Kreek MJ. 2000. Ovarian hormone replacement affects cocaine-induced behaviors in ovariectomized female rats. Pharmacol Biochem Behav 67: 417–422.PubMedGoogle Scholar
  229. Rahman Z, Schwarz J, Gold SJ, Zachariou V, Wein MN, et al. 2003. RGS9 modulates dopamine signaling in the basal ganglia. Neuron 38: 941–952.PubMedGoogle Scholar
  230. Raiteri M, Bertollini A, Angelini F, Levi G. 1975. d-Amphetamine as a releaser or reuptake inhibitor of biogenic amines in synaptosomes. Eur J Pharmacol 34: 189–195.PubMedGoogle Scholar
  231. Ribeiro Do Couto B, Aguilar MA, Manzanedo C, Rodriguez-Arias M, Minarro J. 2005. NMDA glutamate but not dopamine antagonists blocks drug-induced reinstatement of morphine place preference. Brain Res Bull 64: 493–503.PubMedGoogle Scholar
  232. Rice M, Cragg J. 2004. Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7: 583–584.PubMedGoogle Scholar
  233. Robbins SJ, Ehrman RN, Childress AR, O'Brien CP. 1999. Comparing levels of cocaine cue reactivity in male and female outpatients. Drug Alcohol Depend 53: 223–230.PubMedGoogle Scholar
  234. Roberts DCS, Bennett SAL, Vickers GJ. 1989. The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats. Psychopharmacology 98: 408–411.PubMedGoogle Scholar
  235. Robinson S, Kunko P, Smith J, Wallace M, Mo Q, et al. 1997. Extracellular aspartate concentration increases in nucleus accumbens after cocaine sensitization. Eur J Pharmacol 319: 31–36.PubMedGoogle Scholar
  236. Robinson TE. 1984. Behavioral sensitization: Characterization of enduring changes in rotational behavior produced by intermittent injections of amphetamine in male and female rats. Psychopharmacology (Berl) 84: 466–475.Google Scholar
  237. Robinson TE, Becker JB, Presty SK. 1982. Long-term facilitation of amphetamine-induced rotational behavior and striatal dopamine release produced by a single exposure to amphetamine: Sex differences. Brain Res 253: 231–241.PubMedGoogle Scholar
  238. Robinson TE, Berridge KC. 1993. The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Rev 18: 247–291.PubMedGoogle Scholar
  239. Robinson TE, Berridge KC. 2000. The psychology and neurobiology of addiction: An incentive-sensitization view. Addiction 95: S91–S117.PubMedGoogle Scholar
  240. Robinson TE, Berridge KC. 2001. Incentive-sensitization and addiction. Addiction 96: 103–114.PubMedGoogle Scholar
  241. Robinson TE, Berridge KC. 2003. Addiction. Annu Rev Psychol 54: 25–53.PubMedGoogle Scholar
  242. Robinson TE, Kolb B. 2004. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47: 33–46.PubMedGoogle Scholar
  243. Robinson TE, Gorny G, Mitton E, Kolb B. 2001. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39: 257–266.PubMedGoogle Scholar
  244. Robinson TE, Gorny G, Savage VR, Kolb B. 2002. Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46: 271–279.PubMedGoogle Scholar
  245. Robinson TE, Kolb B. 1997. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17: 8491–8497.PubMedGoogle Scholar
  246. Robinson TE, Kolb B. 1999. Morphine alters the structure of neurons in the nucleus accumbens and neocortex of rats. Synapse 33: 160–162.PubMedGoogle Scholar
  247. Roitman MF, Na E, Anderson G, Jones TA, Bernstein IL. 2002. Induction of a salt appetite alters dendritic morphology in nucleus accumbens and sensitizes rats to amphetamine. J Neurosci 22: RC225.PubMedGoogle Scholar
  248. Rolls ET. 2004. Smell, taste, texture, and temperature multimodal representations in the brain, and their relevance to the control of appetite. Nutr Rev 62: S193–S204.PubMedGoogle Scholar
  249. Roseboom PH, Hewlett GH, Gnegy ME. 1990. Repeated amphetamine administration alters the interaction between D1-stimulated adenylyl cyclase activity and calmodulin in rat striatum. J Pharmacol Exp Ther 255: 197–203.PubMedGoogle Scholar
  250. Roth M, Cosgrove K, Carroll M. 2004. Sex differences in the vulnerability to drug abuse: A review of preclinical studies. Neurosci Biobehav Rev 28: 533–546.PubMedGoogle Scholar
  251. Salamone JD, Correa M. 2002. Motivational views of reinforcement: Implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav Brain Res 137: 3–25.PubMedGoogle Scholar
  252. Schenk JO. 2002. The functioning neuronal transporter for dopamine: Kinetic mechanisms and effects of amphetamines, cocaine and methylphenidate. Prog Drug Res 59: 111–131.PubMedGoogle Scholar
  253. Schoenbaum G, Setlow B. 2003. Lesions of nucleus accumbens disrupt learning about aversive outcomes. J Neurosci 23: 9833–9841.PubMedGoogle Scholar
  254. Schoepp DD, Jane DE, Monn JA. 1999. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38: 1431–1476.PubMedGoogle Scholar
  255. Schoffelmeer AN, Voorn P, Jonker AJ, Wardeh G, Nestby P, et al. 1996. Morphine-induced increase in D-1 receptor regulated signal transduction in rat striatal neurons and its facilitation by glucocorticoid receptor activation: Possible role in behavioral sensitization. Neurochem Res 21: 1417–1423.PubMedGoogle Scholar
  256. Schroeder JA, Hummel M, Unterwald EM. 2004. Repeated intracerebroventricular forskolin administration enhances behavioral sensitization to cocaine. Behav Brain Res 153: 255–260.PubMedGoogle Scholar
  257. Schultz W. 1992. Activity of dopamine neurons in the behaving primate. Sem Neurosci 4: 129–138.Google Scholar
  258. Schultz W. 1997. Dopamine neurons and their role in reward mechanisms. Curr Opin Neurobiol 7: 191–197.PubMedGoogle Scholar
  259. Schultz W. 2002. Getting formal with dopamine and reward. Neuron 36: 241–263.PubMedGoogle Scholar
  260. Schultz W. 2004. Neural coding of basic reward terms of animal learning theory, game theory, microeconomics andbehavioral ecology. Curr Opin Neurobiol 14: 139–147.PubMedGoogle Scholar
  261. Schultz W, Apicella P, Ljungberg T, Romo R, Scarnati E. 1993. Reward-related activity in the monkey striatum and substantia nigra. Prog Brain Res 99: 227–235.PubMedGoogle Scholar
  262. Schultz W, Apicella P, Scarnati E, Ljungberg T. 1992. Neuronal activity in monkey ventral striatum related to the expectation of reward. J Neurosci 12: 4595–4610.PubMedGoogle Scholar
  263. Schultz W, Romo R. 1990. Dopamine neurons of the monkey midbrain: Contingencies of responses to stimuli eliciting immediate behavioral reactions. J Neurophysiol 63: 607–624.PubMedGoogle Scholar
  264. Sell SL, Thomas ML, Cunningham KA. 2002. Influence of estrous cycle and estradiol on behavioral sensitization to cocaine in female rats. Drug Alcohol Depend 67: 281–290.PubMedGoogle Scholar
  265. Setlow B, Schoenbaum G, Gallagher M. 2003. Neural encoding in ventral striatum during olfactory discrimination learning. Neuron 38: 625–636.PubMedGoogle Scholar
  266. Shippenberg TS, Bals-Kubik R, Herz A. 1993. Examination of the neurochemical substrates mediating the motivational effects of opioids: Role of the mesolimbic dopamine system and D-1 vs. D-2 dopamine receptors. J Pharmacol Exp Ther 265: 53–59.PubMedGoogle Scholar
  267. Shippenberg TS, Herz A. 1987. Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists. Brain Res 436: 169–172.PubMedGoogle Scholar
  268. Shippenberg TS, Herz A. 1988. Motivational effects of opioids: Influence of D-1 versus D-2 receptor antagonists. Eur J Pharmacol 151: 233–242.PubMedGoogle Scholar
  269. Sircar R, Kim D. 1999. Female gonadal hormones differentially modulate cocaine-induced behavioral sensitization in Fischer, Lewis and Sprague-Dawley rats. J Pharmacol Exp Ther 289: 54–65.PubMedGoogle Scholar
  270. Smith GP. 2004. Accumbens dopamine mediates the rewarding effect of orosensory stimulation by sucrose. Appetite 43: 11–13.PubMedGoogle Scholar
  271. Smith-Roe SL, Kelley AE. 2000. Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20: 7737–7742.PubMedGoogle Scholar
  272. Sokolov BP, Polesskaya OO, Uhl GR. 2003. Mouse brain gene expression changes after acute and chronic amphetamine. J Neurochem 84: 244–252.PubMedGoogle Scholar
  273. Sora I, Wichems C, Takahashi N, Li XF, Zeng Z, Revay R, et al. 1998. Cocaine reward models: Conditioned place preference can be established in dopamine- and serotonin-transporter knockout mice. Proc Natl Acad Sci USA 95: 7699–7704.PubMedCentralPubMedGoogle Scholar
  274. Sulzer D, Chen T, Lau Y, Kristensen H, Rayport S, et al. 1995. Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci 15: 4102–4108.PubMedGoogle Scholar
  275. Sulzer D, Maidment NT, Rayport S. 1993. Amphetamine and other weak bases act to promote reverse transport of dopamine in ventral midbrain neurons. J Neurochem 60: 527–535.PubMedGoogle Scholar
  276. Teitelbaum P, Epstein AN. 1962. The lateral hypothalamic syndrome: Recovery of feeding and drinking after lateral hypothalamic lesions. Psych Rev 69: 74–90.Google Scholar
  277. Thompson TL, Moss RL. 1994. Estrogen regulation of dopamine release in the nucleus accumbens: Genomic- and nongenomic-mediated effects. J Neurochem 62: 1750–1756.PubMedGoogle Scholar
  278. Tobler P, Dickinson A, Schultz W. 2003. Coding of predicted reward omission by dopamine neurons in a conditioned inhibition paradigm. J Neurosci 23: 10402–10410.PubMedGoogle Scholar
  279. Turner TJ. 2004. Nicotine enhancement of dopamine release by a calcium-dependent increase in the size of the readily releasable pool of synaptic vesicles. J Neurosci 24: 11328–11326.PubMedGoogle Scholar
  280. Tzschentke TM, Schmidt WJ. 1998. Blockade of morphine- and amphetamine-induced conditioned place preference in the rat by riluzole. Neurosci Lett 242: 114–116.PubMedGoogle Scholar
  281. Uhl GR, Hall FS, Sora I. 2002. Cocaine, reward, movement and monoamine transporters. Mol Psychiatry 7: 21–26.PubMedGoogle Scholar
  282. Ungerstedt U. 1971. Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol Scand Suppl 367: 95–122.PubMedGoogle Scholar
  283. Unterwald EM, Fillmore J, Kreek MJ. 1996. Chronic repeated cocaine administration increases dopamine D1 receptor-mediated signal transduction. Eur J Pharmacol 318: 31–35.PubMedGoogle Scholar
  284. Unterwald EM, Ho A, Rubenfeld JM, Kreek MJ. 1994. Time course of the development of behavioral sensitization and dopamine receptor up-regulation during binge cocaine administration. J Pharmacol Exp Ther 270: 1387–1396.PubMedGoogle Scholar
  285. Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, et al. 2005. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci USA 102: 491–496.PubMedCentralPubMedGoogle Scholar
  286. Van Bockstaele EJ, Pickel VM. 1995. GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res 682: 215–221.PubMedGoogle Scholar
  287. van Haaren F, Meyer M. 1991. Sex differences in the locomotor activity after acute and chronic cocaine administration. Pharmacol Biochem Behav 39: 923–927.PubMedGoogle Scholar
  288. Van Hartesveldt C, Cottrell GA, Meyer ME. 1989. Effects of intrastriatal hormones on the dorsal immobility response in male rats. Pharmacol Biochem Behav 35: 307–310.Google Scholar
  289. Van Vliet BJ, Van Rijswijk AL, Wardeh G, Mulder AH, Schoffelmeer AN. 1993. Adaptive changes in the number of Gs- and Gi-proteins underlie adenylyl cyclase sensitization in morphine-treated rat striatal neurons. Eur J Pharmacol 245: 23–29.PubMedGoogle Scholar
  290. Vanover KE. 1998. Effects of AMPA receptor antagonists on dopamine-mediated behaviors in mice. Psychopharmacology 136: 123–131.PubMedGoogle Scholar
  291. Verimer T, Arneric SP, Long JP, Walsh BJ, Abou Zeit-Har MS 1981. Effects of ovariectomy, castration, and chronic lithium chloride treatment on stereotyped behavior in rats. Psychopharmacology 75: 273–276.PubMedGoogle Scholar
  292. Volkow ND, Fowler JS, Wang GJ, Goldstein RZ. 2002. Role of dopamine, the frontal cortex and memory circuits in drug addiction: Insight from imaging studies. Neurobiol Learn Mem 78: 610–624.PubMedGoogle Scholar
  293. Wei FY, Tomizawa K, Ohshima T, Asada A, Saito T, et al. 2005. Control of cyclin-dependent kinase 5 (Cdk5) activity by glutamatergic regualtion of p35 stability. J Neurochem 93: 502–512.PubMedGoogle Scholar
  294. Westberry J, Meredith M. 2003. The influence of chemosensory input and gonadotropin releasing hormone on mating behavior circuits in male hamsters. Brain Res 974: 1–16.PubMedGoogle Scholar
  295. Wetherington CL, Roman AR, editors. 1995. Drug addiction research and the health of women. Rockville, MD: US Department of Health and Human Services.Google Scholar
  296. White FJ. 2002. A behavioral/systems approach to the neuroscience of drug addiction. J Neurosci 22: 3303–3305.PubMedGoogle Scholar
  297. White NM. 1996. Addictive drugs as reinforcers: Multiple partial actions on memory systems. Addiction 91: 921–949.PubMedGoogle Scholar
  298. Wise RA. 1978. Catecholamine theories of reward: A critical review. Brain Res 152: 215–247.PubMedGoogle Scholar
  299. Wise RA. 1984. Neural mechanisms of the reinforcing action of cocaine. NIDA Res Monogr 50: 15–33.PubMedGoogle Scholar
  300. Wise RA. 2004. Dopamine, learning and motivation. Nat Rev Neurosci. 5: 483–494.PubMedGoogle Scholar
  301. Wise RA, Rompre P. 1989. Brain dopamine and reward. Annu Rev Psychol 40: 191–225.PubMedGoogle Scholar
  302. Wolf ME. 1998. The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54: 679–720.PubMedGoogle Scholar
  303. Wolf ME, Xue CJ, Li Y, Wavak D. 2000. Amphetamine increases glutamate efflux in the rat ventral tegmental area by a mechanism involving glutamate transporters and reactive oxygen species. J Neurochem 75: 1634–1644.PubMedGoogle Scholar
  304. Wright C, Beijer A, Groenewegen HJ. 1996. Basal amygdaloid complex afferent to the rat nucleus accumbens are compartmentally organized. J Neurosci 16: 1877–1893.PubMedGoogle Scholar
  305. Wyvell CL, Berridge KC. 2001. Incentive sensitization by previous amphetamine exposure: Increased cue-triggered “wanting” for sucrose reward. J Neurosci 21: 7831–7840.PubMedGoogle Scholar
  306. Xi ZX, Stein EA. 1998a. Nucleus accumbens dopamine release modulation by mesolimbic GABA(A) receptors – an in vivo electrochemical study. Brain Res 798: 156–165.PubMedGoogle Scholar
  307. Xi ZX, Stein EA. 1998b. Nucleus accumbens dopamine release modulation by mesolimbic GABAA receptors – an in vivo electrochemical study. Brain Res 798: 156–165.PubMedGoogle Scholar
  308. Xi ZX, Stein EA. 2002. GABAergic mechanisms of opiate reinforcement. Alcohol Alcohol 37: 485–494.PubMedGoogle Scholar
  309. Xi ZX, Ramamoorthy S, Shen H, Lake R, Samuvel DJ, et al. 2003. GABA transmission in the nucleus accumbens is altered after withdrawal from repeated cocaine. J Neurosci 23: 3498–3505.PubMedGoogle Scholar
  310. Xue CJ, Ng JP, Li Y, Wolf ME. 1996. Acute and repeated systemic amphetamine administration: Effects on extracellular glutamate, aspartate, and serine levels in rat ventral tegmental area and nucleus accumbens. J Neurochem 67: 352–363.PubMedGoogle Scholar
  311. Yamaguchi M, Suzuki T, Abe S, Hori T, Kurita H, et al. 2002. Repeated cocaine administration differentially affects NMDA receptor subunit (NR1, NR2A-C) mRNAs in rat brain. Synapse 46: 157–169.PubMedGoogle Scholar
  312. Yuferov V, Kroslak T, Laforge KS, Zhou Y, Ho A, et al. 2003. Differential gene expression in the rat caudate putamen after “binge” cocaine administration: Advantage of triplicate microarray analysis. Synapse 48: 157–169.PubMedGoogle Scholar
  313. Zachariou V, Benoit-Marand M, Allen PB, Ingrassia P, Feinberg AA, et al. 2002. Reduction of cocaine place preference in mice lacking the protein phosphatase 1 inhibitors DARPP 32 or Inhibitor 1. Biol Psychiatry 51: 612–620.PubMedGoogle Scholar
  314. Zhang H, Sulzer D. 2004. Frequency-dependent modulation of dopamine release by nicotine. Nat Neurosci 7: 581–582.PubMedGoogle Scholar
  315. Zhang K, Tarazi FI, Campbell A, Baldessarini RJ. 2000. GABA(B) receptors: Altered coupling to G-proteins in rats sensitized to amphetamine. Neuroscience 101: 5–10.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • J. B. Becker
  • R. L. Meisel

There are no affiliations available

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