Neurochemical Research

, Volume 35, Issue 6, pp 851–867 | Cite as

Heterogeneity of Reward Mechanisms

Overview

Abstract

The finding that many drugs that have abuse potential and other natural stimuli such as food or sexual activity cause similar chemical changes in the brain, an increase in extracellular dopamine (DA) in the shell of the nucleus accumbens (NAccS), indicated some time ago that the reward mechanism is at least very similar for all stimuli and that the mechanism is relatively simple. The presently available information shows that the mechanisms involved are more complex and have multiple elements. Multiple brain regions, multiple receptors, multiple distinct neurons, multiple transmitters, multiple transporters, circuits, peptides, proteins, metabolism of transmitters, and phosphorylation, all participate in reward mechanisms. The system is variable, is changed during development, is sex-dependent, and is influenced by genetic differences. Not all of the elements participate in the reward of all stimuli. Different set of mechanisms are involved in the reward of different drugs of abuse, yet different mechanisms in the reward of natural stimuli such as food or sexual activity; thus there are different systems that distinguish different stimuli. Separate functions of the reward system such as anticipation, evaluation, consummation and identification; all contain function-specific elements. The level of the stimulus also influences the participation of the elements of the reward system, there are possible reactions to even below threshold stimuli, and excessive stimuli can change reward to aversion involving parts of the system. Learning and memory of past reward is an important integral element of reward and addictive behavior. Many of the reward elements are altered by repeated or chronic stimuli, and chronic exposure to one drug is likely to alter the response to another stimulus. To evaluate and identify the reward stimulus thus requires heterogeneity of the reward components in the brain.

Keywords

Receptors Developmental changes Stimulus specificity Cognitive components Food reward 

References

  1. 1.
    Koya E, Golden SA, Harvey BK, Guez-Barber DH, Berkow A, Simmons DE, Bossert JM, Nair SG, Uejima JL, Marin MT, Mitchell TB, Farquhar D, Ghosh SC, Mattson BJ, Hope BT (2009) Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nat Neurosci 12:1069–1073PubMedGoogle Scholar
  2. 2.
    Zaborszky L, Alheid GF, Beinfeld MC, Eiden LE, Heimer L, Palkovits M (1985) Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14:427–453PubMedGoogle Scholar
  3. 3.
    Pontieri FE, Tanda G, Di Chiara G (1995) Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the “shell” as compared with the “core” of the rat nucleus accumbens. Proc Natl Acad Sci USA 92:12304–12308PubMedGoogle Scholar
  4. 4.
    Carboni E, Silvagni A, Rolando MT, Di Chiara G (2000) Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs. J Neurosci 20:RC102PubMedGoogle Scholar
  5. 5.
    Nestler EJ (2005) Is there a common molecular pathway for addiction? Nat Neurosci 8:1445–1449PubMedGoogle Scholar
  6. 6.
    Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27:765–776PubMedGoogle Scholar
  7. 7.
    Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5:34–41PubMedGoogle Scholar
  8. 8.
    D’Souza MS, Duvauchelle CL (2008) Certain or uncertain cocaine expectations influence accumbens dopamine responses to self-administered cocaine and non-rewarded operant behavior. Eur Neuropsychopharmacol 18:628–638PubMedGoogle Scholar
  9. 9.
    Wakabayashi KT, Fields HL, Nicola SM (2004) Dissociation of the role of nucleus accumbens dopamine in responding to reward-predictive cues and waiting for reward. Behav Brain Res 154:19–30PubMedCrossRefGoogle Scholar
  10. 10.
    Nisell M, Nomikos GG, Svensson TH (1995) Nicotine dependence, midbrain dopamine systems and psychiatric disorders. Pharmacol Toxicol 76:157–162PubMedGoogle Scholar
  11. 11.
    Schilstrom B, Nomikos GG, Nisell M, Hertel P, Svensson TH (1998) N-methyl-D-aspartate receptor antagonism in the ventral tegmental area diminishes the systemic nicotine-induced dopamine release in the nucleus accumbens. Neuroscience 82:781–789PubMedGoogle Scholar
  12. 12.
    Nisell M, Nomikos GG, Svensson TH (1994) Infusion of nicotine in the ventral tegmental area or the nucleus accumbens of the rat differentially affects accumbal dopamine release. Pharmacol Toxicol 75:348–352PubMedGoogle Scholar
  13. 13.
    Sziraki I, Sershen H, Hashim A, Lajtha A (2002) Receptors in the ventral tegmental area mediating nicotine-induced dopamine release in the nucleus accumbens. Neurochem Res 27:253–261PubMedGoogle Scholar
  14. 14.
    Yun IA, Wakabayashi KT, Fields HL, Nicola SM (2004) The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J Neurosci 24:2923–2933PubMedGoogle Scholar
  15. 15.
    Olds J, Milner P (1954) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 47:419–427PubMedGoogle Scholar
  16. 16.
    Wise RA (2009) Roles for nigrostriatal–not just mesocorticolimbic–dopamine in reward and addiction. Trends Neurosci 32:517–524PubMedGoogle Scholar
  17. 17.
    Singer S, Rossi S, Verzosa S, Hashim A, Lonow R, Cooper T, Sershen H, Lajtha A (2004) Nicotine-induced changes in neurotransmitter levels in brain areas associated with cognitive function. Neurochem Res 29:1779–1792PubMedGoogle Scholar
  18. 18.
    Fallon S, Shearman E, Sershen H, Lajtha A (2007) Food reward-induced neurotransmitter changes in cognitive brain regions. Neurochem Res 32:1772–1782PubMedGoogle Scholar
  19. 19.
    See RE, Elliott JC, Feltenstein MW (2007) The role of dorsal vs. ventral striatal pathways in cocaine-seeking behavior after prolonged abstinence in rats. Psychopharmacology (Berl) 194:321–331Google Scholar
  20. 20.
    Liu X, Powell DK, Wang H, Gold BT, Corbly CR, Joseph JE (2007) Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J Neurosci 27:4587–4597PubMedGoogle Scholar
  21. 21.
    Shearman E, Rossi S, Sershen H, Hashim A, Lajtha A (2005) Locally administered low nicotine-induced neurotransmitter changes in areas of cognitive function. Neurochem Res 30:1055–1066PubMedGoogle Scholar
  22. 22.
    Fallon S, Shearman E, Sershen H, Lajtha A (2007) The effects of glutamate and GABA receptor antagonists on nicotine-induced neurotransmitter changes in cognitive areas. Neurochem Res 32:535–553PubMedGoogle Scholar
  23. 23.
    Horvitz JC (2002) Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum. Behav Brain Res 137:65–74PubMedGoogle Scholar
  24. 24.
    Rossi S, Singer S, Shearman E, Sershen H, Lajtha A (2005) Regional heterogeneity of nicotine effects on neurotransmitters in rat brains in vivo at low doses. Neurochem Res 30:91–103PubMedGoogle Scholar
  25. 25.
    Asyyed A, Storm D, Diamond I (2006) Ethanol activates cAMP response element-mediated gene expression in select regions of the mouse brain. Brain Res 1106:63–71PubMedGoogle Scholar
  26. 26.
    Kash TL, Matthews RT, Winder DG (2008) Alcohol inhibits NR2B-containing NMDA receptors in the ventral bed nucleus of the stria terminalis. Neuropsychopharmacology 33:1379–1390PubMedGoogle Scholar
  27. 27.
    Volkow ND, Fowler JS (2000) Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex 10:318–325PubMedGoogle Scholar
  28. 28.
    Batterham RL, ffytche DH, Rosenthal JM, Zelaya FO, Barker GJ, Withers DJ, Williams SC (2007) PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature 450:106–109PubMedGoogle Scholar
  29. 29.
    Lee D, Rushworth MF, Walton ME, Watanabe M, Sakagami M (2007) Functional specialization of the primate frontal cortex during decision making. J Neurosci 27:8170–8173PubMedGoogle Scholar
  30. 30.
    Wallis JD (2007) Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 30:31–56PubMedGoogle Scholar
  31. 31.
    Roesch MR, Olson CR (2007) Neuronal activity related to anticipated reward in frontal cortex: does it represent value or reflect motivation? Ann N Y Acad Sci 1121:431–446PubMedGoogle Scholar
  32. 32.
    Ichihara-Takeda S, Funahashi S (2006) Reward-period activity in primate dorsolateral prefrontal and orbitofrontal neurons is affected by reward schedules. J Cogn Neurosci 18:212–226PubMedGoogle Scholar
  33. 33.
    Eshel N, Nelson EE, Blair RJ, Pine DS, Ernst M (2007) Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 45:1270–1279PubMedGoogle Scholar
  34. 34.
    Rossi S, Singer S, Shearman E, Sershen H, Lajtha A (2005) The effects of cholinergic and dopaminergic antagonists on nicotine-induced cerebral neurotransmitter changes. Neurochem Res 30:541–558PubMedGoogle Scholar
  35. 35.
    Sziraki I, Sershen H, Benuck M, Hashim A, Lajtha A (1998) Receptor systems participating in nicotine-specific effects. Neurochem Int 33:445–457PubMedGoogle Scholar
  36. 36.
    Tarazi FI, Baldessarini RJ (2000) Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 18:29–37PubMedGoogle Scholar
  37. 37.
    Eyny YS, Horvitz JC (2003) Opposing roles of D1 and D2 receptors in appetitive conditioning. J Neurosci 23:1584–1587PubMedGoogle Scholar
  38. 38.
    Adriani W, Granstrem O, Macri S, Izykenova G, Dambinova S, Laviola G (2004) Behavioral and neurochemical vulnerability during adolescence in mice: studies with nicotine. Neuropsychopharmacology 29:869–878PubMedGoogle Scholar
  39. 39.
    Balla A, Nattini ME, Sershen H, Lajtha A, Dunlop DS, Javitt C (2009) GABAB/NMDA receptor interaction in the regulation of extracellular dopamine levels in rodent prefrontal cortex and striatum. Neuropharmacology 56:915–921PubMedGoogle Scholar
  40. 40.
    Knackstedt LA, Kalivas PW (2009) Glutamate and reinstatement. Curr Opin Pharmacol 9:59–64PubMedGoogle Scholar
  41. 41.
    O’Dell LE, Parsons LH (2004) Serotonin1B receptors in the ventral tegmental area modulate cocaine-induced increases in nucleus accumbens dopamine levels. J Pharmacol Exp Ther 311:711–719PubMedGoogle Scholar
  42. 42.
    Hnasko TS, Sotak BN, Palmiter RD (2007) Cocaine-conditioned place preference by dopamine-deficient mice is mediated by serotonin. J Neurosci 27:12484–12488PubMedGoogle Scholar
  43. 43.
    You ZB, Wang B, Zitzman D, Wise RA (2008) Acetylcholine release in the mesocorticolimbic dopamine system during cocaine seeking: conditioned and unconditioned contributions to reward and motivation. J Neurosci 28:9021–9029PubMedGoogle Scholar
  44. 44.
    Sofuoglu M, Sewell RA (2009) Norepinephrine and stimulant addiction. Addict Biol 14:119–129PubMedGoogle Scholar
  45. 45.
    Wang L, Liu J, Harvey-White J, Zimmer A, Kunos G (2003) Endocannabinoid signaling via cannabinoid receptor 1 is involved in ethanol preference and its age-dependent decline in mice. Proc Natl Acad Sci U S A 100:1393–1398PubMedGoogle Scholar
  46. 46.
    Soderman AR, Unterwald EM (2008) Cocaine reward and hyperactivity in the rat: sites of mu opioid receptor modulation. Neuroscience 154:1506–1516PubMedGoogle Scholar
  47. 47.
    Sun WL, Zhou L, Hazim R, Quinones-Jenab V, Jenab S (2008) Effects of dopamine and NMDA receptors on cocaine-induced Fos expression in the striatum of Fischer rats. Brain Res 1243:1–9PubMedGoogle Scholar
  48. 48.
    Kash TL, Nobis WP, Matthews RT, Winder DG (2008) Dopamine enhances fast excitatory synaptic transmission in the extended amygdala by a CRF-R1-dependent process. J Neurosci 28:13856–13865PubMedGoogle Scholar
  49. 49.
    Slotkin TA (2002) Nicotine and the adolescent brain: insights from an animal model. Neurotoxicol Teratol 24:369–384PubMedGoogle Scholar
  50. 50.
    Vastola BJ, Douglas LA, Varlinskaya EI, Spear LP (2002) Nicotine-induced conditioned place preference in adolescent and adult rats. Physiol Behav 77:107–114PubMedGoogle Scholar
  51. 51.
    Schochet TL, Kelley AE, Landry CF (2004) Differential behavioral effects of nicotine exposure in adolescent and adult rats. Psychopharmacology (Berl) 175:265–273Google Scholar
  52. 52.
    Adriani W, Macri S, Pacifici R, Laviola G (2002) Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology 27:212–224PubMedGoogle Scholar
  53. 53.
    Belluzzi JD, Lee AG, Oliff HS, Leslie FM (2004) Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl) 174:389–395Google Scholar
  54. 54.
    Shram MJ, Funk D, Li Z, Le AD (2007) Acute nicotine enhances c-fos mRNA expression differentially in reward-related substrates of adolescent and adult rat brain. Neurosci Lett 418:286–291PubMedGoogle Scholar
  55. 55.
    Kota D, Martin BR, Robinson SE, Damaj MI (2007) Nicotine dependence and reward differ between adolescent and adult male mice. J Pharmacol Exp Ther 322:399–407PubMedGoogle Scholar
  56. 56.
    Brielmaier JM, McDonald CG, Smith RF (2007) Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats. Neurotoxicol Teratol 29:74–80PubMedGoogle Scholar
  57. 57.
    Philpot R, Kirstein C (2007) Developmental differences in the accumbal dopaminergic response to repeated ethanol exposure. Ann N Y Acad Sci 1021:422–426Google Scholar
  58. 58.
    Shram MJ, Funk D, Li Z, Le AD (2007) Nicotine self-administration, extinction responding and reinstatement in adolescent and adult male rats: evidence against a biological vulnerability to nicotine addiction during adolescence. Neuropsychopharmacology 33:739–748PubMedGoogle Scholar
  59. 59.
    Torrella TA, Badanich KA, Philpot RM, Kirstein CL, Wecker L (2004) Developmental differences in nicotine place conditioning. Ann N Y Acad Sci 1021:399–403PubMedGoogle Scholar
  60. 60.
    O’Dell LE, Bruijnzeel AW, Smith RT, Parsons LH, Merves ML, Goldberger BA, Richardson HN, Koob GF, Markou A (2006) Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction. Psychopharmacology (Berl) 186:612–619Google Scholar
  61. 61.
    Shram MJ, Funk D, Li Z, Le AD (2006) Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology (Berl) 186:201–208Google Scholar
  62. 62.
    O’Dell LE, Torres OV, Natividad LA, Tejeda HA (2007) Adolescent nicotine exposure produces less affective measures of withdrawal relative to adult nicotine exposure in male rats. Neurotoxicol Teratol 29:17–22PubMedGoogle Scholar
  63. 63.
    Wilmouth CE, Spear LP (2006) Withdrawal from chronic nicotine in adolescent and adult rats. Pharmacol Biochem Behav 85:648–657PubMedGoogle Scholar
  64. 64.
    Badanich KA, Kirsteina CL (2004) Nicotine administration significantly alters accumbal dopamine in the adult but not in the adolescent rat. Ann N Y Acad Sci 1021:410–417PubMedGoogle Scholar
  65. 65.
    Shearman E, Fallon S, Sershen H, Lajtha A (2008) Nicotine-induced monoamine neurotransmitter changes in the brain of young rats. Brain Res Bull 76:626–639PubMedGoogle Scholar
  66. 66.
    Badanich KA, Adler KJ, Kirstein CL (2006) Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 550:95–106PubMedGoogle Scholar
  67. 67.
    Azam L, Chen Y, Leslie FM (2007) Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons. Neuroscience 144:1347–1360PubMedGoogle Scholar
  68. 68.
    Sershen H, Shearman E, Fallon S, Chakraborty G, Smiley J, Lajtha A (2009) The effects of acetaldehyde on nicotine-induced transmitter levels in young and adult brain areas. Brain Res Bull 79:458–462PubMedGoogle Scholar
  69. 69.
    Becker JB (1999) Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64:803–812PubMedGoogle Scholar
  70. 70.
    Levin ED, Lawrence SS, Petro A, Horton K, Rezvani AH, Seidler FJ, Slotkin TA (2007) Adolescent vs. adult-onset nicotine self-administration in male rats: duration of effect and differential nicotinic receptor correlates. Neurotoxicol Teratol 29:458–465PubMedGoogle Scholar
  71. 71.
    Collins SL, Montano R, Izenwasser S (2004) Nicotine treatment produces persistent increases in amphetamine-stimulated locomotor activity in periadolescent male but not female or adult male rats. Brain Res Dev Brain Res 153:175–187PubMedGoogle Scholar
  72. 72.
    Quinones-Jenab V, Ho A, Schlussman SD, Franck J, Kreek MJ (1999) Estrous cycle differences in cocaine-induced stereotypic and locomotor behaviors in Fischer rats. Behav Brain Res 101:15–20PubMedGoogle Scholar
  73. 73.
    Devaud LL, Risinger FO, Selvage D (2006) Impact of the hormonal milieu on the neurobiology of alcohol dependence and withdrawal. J Gen Psychol 133:337–356PubMedGoogle Scholar
  74. 74.
    Sziraki I, Lipovac MN, Hashim A, Sershen H, Allen D, Cooper T, Czobor P, Lajtha A (2001) Differences in nicotine-induced dopamine release and nicotine pharmacokinetics between Lewis and Fischer 344 rats. Neurochem Res 26:609–617PubMedGoogle Scholar
  75. 75.
    Kosten TA, Ambrosio E (2002) HPA axis function and drug addictive behaviors: insights from studies with Lewis and Fischer 344 inbred rats. Psychoneuroendocrinology 27:35–69PubMedGoogle Scholar
  76. 76.
    Alttoa A, Seeman P, Koiv K, Eller M, Harro J (2009) Rats with persistently high exploratory activity have both higher extracellular dopamine levels and higher proportion of D(2) (High) receptors in the striatum. Synapse 63:443–446PubMedGoogle Scholar
  77. 77.
    Sustkova-Fiserova M, Vavrova J, Krsiak M (2009) Brain levels of GABA, glutamate and aspartate in sociable, aggressive and timid mice: an in vivo microdialysis study. Neuro Endocrinol Lett 30:79–84PubMedGoogle Scholar
  78. 78.
    Meyer PJ, Meshul CK, Phillips TJ (2009) Ethanol- and cocaine-induced locomotion are genetically related to increases in accumbal dopamine. Genes Brain Behav 8:346–355PubMedGoogle Scholar
  79. 79.
    Abreu-Villaca Y, Queiroz-Gomes FE, Dal Monte AP, Filgueiras CC, Manhaes AC (2006) Individual differences in novelty-seeking behavior but not in anxiety response to a new environment can predict nicotine consumption in adolescent C57BL/6 mice. Behav Brain Res 167:175–182PubMedGoogle Scholar
  80. 80.
    Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley JW, Robbins TW (2008) Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci 363:3125–3135PubMedGoogle Scholar
  81. 81.
    Crews FT, Boettiger CA (2009) Impulsivity, frontal lobes and risk for addiction. Pharmacol Biochem Behav 93:237–247PubMedGoogle Scholar
  82. 82.
    Sershen H, Hashim A, Lajtha A (2009) Differences between nicotine and cocaine-induced conditioned place preferences. Brain Res Bull. doi:10.1016/j.brainresbull.2009.07.015
  83. 83.
    Vizi ES, Palkovits M, Lendvai B, Baranyi M, Kovacs KJ, Zelles T (2004) Distinct temperature-dependent dopamine-releasing effect of drugs of abuse in the olfactory bulb. Neurochem Int 45:63–71PubMedGoogle Scholar
  84. 84.
    Nelson CL, Milovanovic M, Wetter JB, Ford KA, Wolf ME (2009) Behavioral sensitization to amphetamine is not accompanied by changes in glutamate receptor surface expression in the rat nucleus accumbens. J Neurochem 109:35–51PubMedGoogle Scholar
  85. 85.
    Le Foll B, Goldberg SR, Sokoloff P (2005) The dopamine D3 receptor and drug dependence: effects on reward or beyond? Neuropharmacology 49:525–541PubMedGoogle Scholar
  86. 86.
    Bassareo V, Di Chiara G (1999) Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89:637–641PubMedGoogle Scholar
  87. 87.
    Cheng JJ, de Bruin JP, Feenstra MG (2003) Dopamine efflux in nucleus accumbens shell and core in response to appetitive classical conditioning. Eur J Neurosci 18:1306–1314PubMedGoogle Scholar
  88. 88.
    Li X, Li J, Peng XQ, Spiller K, Gardner EL, Xi ZX (2009) Metabotropic glutamate receptor 7 modulates the rewarding effects of cocaine in rats: involvement of a ventral pallidal GABAergic mechanism. Neuropsychopharmacology 34:1783–1796PubMedGoogle Scholar
  89. 89.
    Romieu P, Host L, Gobaille S, Sandner G, Aunis D, Zwiller J (2008) Histone deacetylase inhibitors decrease cocaine but not sucrose self-administration in rats. J Neurosci 28:9342–9348PubMedGoogle Scholar
  90. 90.
    Roth-Deri I, Green-Sadan T, Yadid G (2008) Beta-endorphin and drug-induced reward and reinforcement. Prog Neurobiol 86:1–21PubMedGoogle Scholar
  91. 91.
    Davis TJ, de Fiebre CM (2006) Alcohol’s actions on neuronal nicotinic acetylcholine receptors. Alcohol Res Health 29:179–185PubMedGoogle Scholar
  92. 92.
    McQuown SC, Belluzzi JD, Leslie FM (2007) Low dose nicotine treatment during early adolescence increases subsequent cocaine reward. Neurotoxicol Teratol 29:66–73PubMedGoogle Scholar
  93. 93.
    de WH (2009) Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 14:22–31Google Scholar
  94. 94.
    Sarviharju M, Hyytia P, Hervonen A, Jaatinen P, Kiianmaa K, Korpi ER (2006) Lifelong ethanol consumption and brain regional GABAA receptor subunit mRNA expression in alcohol-preferring rats. Alcohol 40:159–166PubMedGoogle Scholar
  95. 95.
    Gulick D, Gould TJ (2008) Interactive effects of ethanol and nicotine on learning in C57BL/6J mice depend on both dose and duration of treatment. Psychopharmacology (Berl) 196:483–495Google Scholar
  96. 96.
    Schoedel KA, Tyndale RF (2003) Induction of nicotine-metabolizing CYP2B1 by ethanol and ethanol-metabolizing CYP2E1 by nicotine: summary and implications. Biochim Biophys Acta 1619:283–290PubMedGoogle Scholar
  97. 97.
    Burch JB, de Fiebre CM, Marks MJ, Collins AC (1988) Chronic ethanol or nicotine treatment results in partial cross-tolerance between these agents. Psychopharmacology (Berl) 95:452–458Google Scholar
  98. 98.
    Izenwasser S, Cox BM (1992) Inhibition of dopamine uptake by cocaine and nicotine: tolerance to chronic treatments. Brain Res 573:119–125PubMedGoogle Scholar
  99. 99.
    Lessov CN, Phillips TJ (2003) Cross-sensitization between the locomotor stimulant effects of ethanol and those of morphine and cocaine in mice. Alcohol Clin Exp Res 27:616–627PubMedGoogle Scholar
  100. 100.
    Corringer PJ, Sallette J, Changeux JP (2006) Nicotine enhances intracellular nicotinic receptor maturation: a novel mechanism of neural plasticity? J Physiol Paris 99:162–171PubMedGoogle Scholar
  101. 101.
    Sallette J, Pons S, villers-Thiery A, Soudant M, Prado de CL, Changeux JP, Corringer PJ (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46:595–607PubMedGoogle Scholar
  102. 102.
    Moroni M, Zwart R, Sher E, Cassels BK, Bermudez I (2006) Alpha4beta2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol Pharmacol 70:755–768PubMedGoogle Scholar
  103. 103.
    Barik J, Wonnacott S (2009) Molecular and cellular mechanisms of action of nicotine in the CNS. Handb Exp Pharmacol 173–207Google Scholar
  104. 104.
    Sanderson EM, Drasdo AL, McCrea K, Wonnacott S (1993) Upregulation of nicotinic receptors following continuous infusion of nicotine is brain-region-specific. Brain Res 617:349–352PubMedGoogle Scholar
  105. 105.
    Nashmi R, Lester H (2007) Cell autonomy, receptor autonomy, and thermodynamics in nicotine receptor up-regulation. Biochem Pharmacol 74:1145–1154PubMedGoogle Scholar
  106. 106.
    Mansvelder HD, De RM, McGehee DS, Brussaard AB (2003) Cholinergic modulation of dopaminergic reward areas: upstream and downstream targets of nicotine addiction. Eur J Pharmacol 480:117–123PubMedGoogle Scholar
  107. 107.
    Fu Y, Matta SG, Kane VB, Sharp BM (2003) Norepinephrine release in amygdala of rats during chronic nicotine self-administration: an in vivo microdialysis study. Neuropharmacology 45:514–523PubMedGoogle Scholar
  108. 108.
    Briand LA, Flagel SB, Seeman P, Robinson TE (2008) Cocaine self-administration produces a persistent increase in dopamine D2 High receptors. Eur Neuropsychopharmacol 18:551–556PubMedGoogle Scholar
  109. 109.
    Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679–720PubMedGoogle Scholar
  110. 110.
    Liu Y, Matsumoto RR (2008) Alterations in fos-related antigen 2 and sigma1 receptor gene and protein expression are associated with the development of cocaine-induced behavioral sensitization: time course and regional distribution studies. J Pharmacol Exp Ther 327:187–195PubMedGoogle Scholar
  111. 111.
    Nisell M, Nomikos GG, Chergui K, Grillner P, Svensson TH (1997) Chronic nicotine enhances basal and nicotine-induced Fos immunoreactivity preferentially in the medial prefrontal cortex of the rat. Neuropsychopharmacology 17:151–161PubMedGoogle Scholar
  112. 112.
    Brunzell DH, Russell DS, Picciotto MR (2003) In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signaling in C57Bl/6J mice. J Neurochem 84:1431–1441PubMedGoogle Scholar
  113. 113.
    Li MD, Kane JK, Wang J, Ma JZ (2004) Time-dependent changes in transcriptional profiles within five rat brain regions in response to nicotine treatment. Brain Res Mol Brain Res 132:168–180PubMedGoogle Scholar
  114. 114.
    Rezvani K, Teng Y, Shim D, De BM (2007) Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J Neurosci 27:10508–10519PubMedGoogle Scholar
  115. 115.
    Picciotto MR, Brunzell DH, Caldarone BJ (2002) Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport 13:1097–1106PubMedGoogle Scholar
  116. 116.
    O’Neill MJ, Murray TK, Lakics V, Visanji NP, Duty S (2002) The role of neuronal nicotinic acetylcholine receptors in acute and chronic neurodegeneration. Curr Drug Targets CNS Neurol Disord 1:399–411PubMedGoogle Scholar
  117. 117.
    Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598PubMedGoogle Scholar
  118. 118.
    Gould TJ (2006) Nicotine and hippocampus-dependent learning: implications for addiction. Mol Neurobiol 34:93–107PubMedGoogle Scholar
  119. 119.
    Belin D, Jonkman S, Dickinson A, Robbins TW, Everitt BJ (2009) Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav Brain Res 199:89–102PubMedGoogle Scholar
  120. 120.
    Boning J (2009) Addiction memory as a specific, individually learned memory imprint. Pharmacopsychiatry 42(Suppl 1):S66–S68PubMedGoogle Scholar
  121. 121.
    Koob GF (2009) Dynamics of neuronal circuits in addiction: reward, antireward, and emotional memory. Pharmacopsychiatry 42(Suppl 1):S32–S41PubMedGoogle Scholar
  122. 122.
    Rezvani AH, Levin ED (2001) Cognitive effects of nicotine. Biol Psychiatry 49:258–267PubMedGoogle Scholar
  123. 123.
    Lajtha A (2008) Interrelated mechanisms in reward and learning. Neurochem Int 52:73–79PubMedGoogle Scholar
  124. 124.
    Chen HI, Kuo YM, Liao CH, Jen CJ, Huang AM, Cherng CG, Su SW, Yu L (2008) Long-term compulsive exercise reduces the rewarding efficacy of 3, 4-methylenedioxymethamphetamine. Behav Brain Res 187:185–189PubMedGoogle Scholar
  125. 125.
    Meeusen R (2005) Exercise and the brain: insight in new therapeutic modalities. Ann Transplant 10:49–51PubMedGoogle Scholar
  126. 126.
    Sutoo D, Akiyama K (2003) Regulation of brain function by exercise. Neurobiol Dis 13:1–14PubMedGoogle Scholar
  127. 127.
    Volkow ND, Wang GJ, Fowler JS, Telang F (2008) Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci 363:3191–3200PubMedGoogle Scholar
  128. 128.
    Koizumi M, Cagniard B, Murphy NP (2009) Endogenous nociceptin modulates diet preference independent of motivation and reward. Physiol Behav 97:1–13PubMedGoogle Scholar
  129. 129.
    Schienle A, Schafer A, Hermann A, Vaitl D (2009) Binge-eating disorder: reward sensitivity and brain activation to images of food. Biol Psychiatry 65:654–661PubMedGoogle Scholar
  130. 130.
    Adan RA, Vanderschuren LJ, El Fleur (2008) Anti-obesity drugs and neural circuits of feeding. Trends Pharmacol Sci 29:208–217PubMedGoogle Scholar
  131. 131.
    Le FB, Chefer SI, Kimes AS, Shumway D, Stein EA, Mukhin AG, Goldberg SR (2009) Baseline expression of alpha4beta2* nicotinic acetylcholine receptors predicts motivation to self-administer nicotine. Biol Psychiatry 65:714–716Google Scholar
  132. 132.
    Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86:773–795PubMedGoogle Scholar
  133. 133.
    Costentin J (2004) Physiological and neurobiological elements of food intake. Ann Pharm Fr 62:92–102PubMedGoogle Scholar
  134. 134.
    Jerlhag E, Egecioglu E, Dickson SL, Douhan A, Svensson L, Engel JA (2007) Ghrelin administration into tegmental areas stimulates locomotor activity and increases extracellular concentration of dopamine in the nucleus accumbens. Addict Biol 12:6–16PubMedGoogle Scholar
  135. 135.
    Quarta D, Di FC, Melotto S, Mangiarini L, Heidbreder C, Hedou G (2009) Systemic administration of ghrelin increases extracellular dopamine in the shell but not the core subdivision of the nucleus accumbens. Neurochem Int 54:89–94PubMedGoogle Scholar
  136. 136.
    Geiger BM, Behr GG, Frank LE, Caldera-Siu AD, Beinfeld MC, Kokkotou EG, Pothos EN (2008) Evidence for defective mesolimbic dopamine exocytosis in obesity-prone rats. FASEB J 22:2740–2746PubMedGoogle Scholar
  137. 137.
    Wang GJ, Volkow ND, Thanos PK, Fowler JS (2004) Similarity between obesity and drug addiction as assessed by neurofunctional imaging: a concept review. J Addict Dis 23:39–53PubMedGoogle Scholar
  138. 138.
    Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705–1712PubMedGoogle Scholar
  139. 139.
    Baldo BA, Sadeghian K, Basso AM, Kelley AE (2002) Effects of selective dopamine D1 or D2 receptor blockade within nucleus accumbens subregions on ingestive behavior and associated motor activity. Behav Brain Res 137:165–177PubMedGoogle Scholar
  140. 140.
    Liu ZH, Shin R, Ikemoto S (2008) Dual role of medial A10 dopamine neurons in affective encoding. Neuropsychopharmacology 33:3010–3020PubMedGoogle Scholar
  141. 141.
    Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651–656PubMedGoogle Scholar
  142. 142.
    Milton AL, Lee JL, Everitt BJ (2008) Reconsolidation of appetitive memories for both natural and drug reinforcement is dependent on {beta}-adrenergic receptors. Learn Mem 15:88–92PubMedGoogle Scholar
  143. 143.
    dos Santos RL, Mansur SS, Steffens SM, Faria MS, Marino-Neto J, Paschoalini MA (2009) Food intake increased after injection of adrenaline into the median raphe nucleus of free-feeding rats. Behav Brain Res 197:411–416PubMedGoogle Scholar
  144. 144.
    Swiergiel AH, Wieczorek M (2008) Noradrenaline-induced feeding responses in the rat do not depend on food characteristics. Acta Neurobiol Exp (Wars) 68:354–361Google Scholar
  145. 145.
    Huang XF, Huang X, Han M, Chen F, Storlien L, Lawrence AJ (2004) 5-HT2A/2C receptor and 5-HT transporter densities in mice prone or resistant to chronic high-fat diet-induced obesity: a quantitative autoradiography study. Brain Res 1018:227–235PubMedGoogle Scholar
  146. 146.
    Capasso A, Petrella C, Milano W (2009) Pharmacological profile of SSRIs and SNRIs in the treatment of eating disorders. Curr Clin Pharmacol 4:78–83PubMedGoogle Scholar
  147. 147.
    Pratt WE, Kelley AE (2005) Striatal muscarinic receptor antagonism reduces 24-h food intake in association with decreased preproenkephalin gene expression. Eur J Neurosci 22:3229–3240PubMedGoogle Scholar
  148. 148.
    Perry ML, Baldo BA, Andrzejewski ME, Kelley AE (2009) Muscarinic receptor antagonism causes a functional alteration in nucleus accumbens mu-opiate-mediated feeding behavior. Behav Brain Res 197:225–229PubMedGoogle Scholar
  149. 149.
    Kramer PR, Guan G, Wellman PJ, Bellinger LL (2007) Nicotine’s attenuation of body weight involves the perifornical hypothalamus. Life Sci 81:500–508PubMedGoogle Scholar
  150. 150.
    Rada P, Hernandez L, Hoebel BG (2007) Feeding and systemic D-amphetamine increase extracellular acetylcholine in the medial thalamus: a possible reward enabling function. Neurosci Lett 416:184–187PubMedGoogle Scholar
  151. 151.
    Melis T, Succu S, Sanna F, Boi A, Argiolas A, Melis MR (2007) The cannabinoid antagonist SR 141716A (Rimonabant) reduces the increase of extra-cellular dopamine release in the rat nucleus accumbens induced by a novel high palatable food. Neurosci Lett 419:231–235PubMedGoogle Scholar
  152. 152.
    Viveros MP, de Fonseca FR, Bermudez-Silva FJ, McPartland JM (2008) Critical role of the endocannabinoid system in the regulation of food intake and energy metabolism, with phylogenetic, developmental, and pathophysiological implications. Endocr Metab Immune Disord Drug Targets 8:220–230PubMedGoogle Scholar
  153. 153.
    Sperlagh B, Windisch K, Ando RD, Vizi ES (2009) Neurochemical evidence that stimulation of CB1 cannabinoid receptors on GABAergic nerve terminals activates the dopaminergic reward system by increasing dopamine release in the rat nucleus accumbens. Neurochem Int 54:452–457PubMedGoogle Scholar
  154. 154.
    Kirkham TC (2005) Endocannabinoids in the regulation of appetite and body weight. Behav Pharmacol 16:297–313PubMedGoogle Scholar
  155. 155.
    DiPatrizio NV, Simansky KJ (2008) Activating parabrachial cannabinoid CB1 receptors selectively stimulates feeding of palatable foods in rats. J Neurosci 28:9702–9709PubMedGoogle Scholar
  156. 156.
    Kola B, Farkas I, Christ-Crain M, Wittmann G, Lolli F, Amin F, Harvey-White J, Liposits Z, Kunos G, Grossman AB, Fekete C, Korbonits M (2008) The orexigenic effect of ghrelin is mediated through central activation of the endogenous cannabinoid system. PLoS ONE 3:e1797PubMedGoogle Scholar
  157. 157.
    Will MJ, Franzblau EB, Kelley AE (2003) Nucleus accumbens mu-opioids regulate intake of a high-fat diet via activation of a distributed brain network. J Neurosci 23:2882–2888PubMedGoogle Scholar
  158. 158.
    Sahr AE, Sindelar DK, exander-Chacko JT, Eastwood BJ, Mitch CH, Statnick MA (2008) Activation of mesolimbic dopamine neurons during novel and daily limited access to palatable food is blocked by the opioid antagonist LY255582. Am J Physiol Regul Integr Comp Physiol 295:R463–R471PubMedGoogle Scholar
  159. 159.
    Billes SK, Cowley MA (2008) Catecholamine reuptake inhibition causes weight loss by increasing locomotor activity and thermogenesis. Neuropsychopharmacology 33:1287–1297PubMedGoogle Scholar
  160. 160.
    Kaye WH, Bailer UF, Frank GK, Wagner A, Henry SE (2005) Brain imaging of serotonin after recovery from anorexia and bulimia nervosa. Physiol Behav 86:15–17PubMedGoogle Scholar
  161. 161.
    Halford JC, Harrold JA, Boyland EJ, Lawton CL, Blundell JE (2007) Serotonergic drugs: effects on appetite expression and use for the treatment of obesity. Drugs 67:27–55PubMedGoogle Scholar
  162. 162.
    Clifford PS, Davis KW, Elliott AE, Wellman PJ (2007) Effects of ICV administration of the alpha1A-adrenoceptor antagonist 5-methylurapidil on concurrent measures of eating and locomotion after cocaine in the rat. Life Sci 81:1059–1065PubMedGoogle Scholar
  163. 163.
    Herzig V, Capuani EM, Kovar KA, Schmidt WJ (2005) Effects of MPEP on expression of food. Addict Biol 10:243–249PubMedGoogle Scholar
  164. 164.
    Lutter M, Nestler EJ (2009) Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr 139:629–632PubMedGoogle Scholar
  165. 165.
    Oldfield BJ, Allen AM, Davern P, Giles ME, Owens NC (2007) Lateral hypothalamic ‘command neurons’ with axonal projections to regions involved in both feeding and thermogenesis. Eur J Neurosci 25:2404–2412PubMedGoogle Scholar
  166. 166.
    Malik S, McGlone F, Bedrossian D, Dagher A (2008) Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 7:400–409PubMedGoogle Scholar
  167. 167.
    Morales T, Aguilar L, Ramos E, Mena F, Morgan C (2008) Fos expression induced by milk ingestion in the caudal brainstem of neonatal rats. Brain Res 1241:76–83PubMedGoogle Scholar
  168. 168.
    Zaidi FN, Todd K, Enquist L, Whitehead MC (2008) Types of taste circuits synaptically linked to a few geniculate ganglion neurons. J Comp Neurol 511:753–772PubMedGoogle Scholar
  169. 169.
    Marsh R, Steinglass JE, Gerber AJ, Graziano OK, Wang Z, Murphy D, Walsh BT, Peterson BS (2009) Deficient activity in the neural systems that mediate self-regulatory control in bulimia nervosa. Arch Gen Psychiatry 66:51–63PubMedGoogle Scholar
  170. 170.
    Stice E, Spoor S, Bohon C, Small DM (2008) Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322:449–452PubMedGoogle Scholar
  171. 171.
    Meister B (2007) Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav 92:263–271PubMedGoogle Scholar
  172. 172.
    Leibowitz SF (2007) Overconsumption of dietary fat and alcohol: mechanisms involving lipids and hypothalamic peptides. Physiol Behav 91:513–521PubMedGoogle Scholar
  173. 173.
    Hillebrand JJ, Kas MJ, Adan RA (2006) To eat or not to eat; regulation by the melanocortin system. Physiol Behav 89:97–102PubMedGoogle Scholar
  174. 174.
    Park SM, Gaykema RP, Goehler LE (2008) How does immune challenge inhibit ingestion of palatable food? Evidence that systemic lipopolysaccharide treatment modulates key nodal points of feeding neurocircuitry. Brain Behav Immun 22:1160–1172PubMedGoogle Scholar
  175. 175.
    Davis JF, Tracy AL, Schurdak JD, Tschop MH, Lipton JW, Clegg DJ, Benoit SC (2008) Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav Neurosci 122:1257–1263PubMedGoogle Scholar
  176. 176.
    Baldwin AE, Sadeghian K, Kelley AE (2002) Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J Neurosci 22:1063–1071PubMedGoogle Scholar
  177. 177.
    Baldwin AE, Holahan MR, Sadeghian K, Kelley AE (2000) N-methyl-D-aspartate receptor-dependent plasticity within a distributed corticostriatal network mediates appetitive instrumental learning. Behav Neurosci 114:84–98PubMedGoogle Scholar
  178. 178.
    Holahan MR (2005) Complementary roles for the amygdala and hippocampus during different phases of appetitive information processing. Neurobiol Learn Mem 84:124–131PubMedGoogle Scholar
  179. 179.
    Verwey M, Khoja Z, Stewart J, Amir S (2007) Differential regulation of the expression of Period2 protein in the limbic forebrain and dorsomedial hypothalamus by daily limited access to highly palatable food in food-deprived and free-fed rats. Neuroscience 147:277–285PubMedGoogle Scholar
  180. 180.
    Rodd-Henricks ZA, Melendez RI, Zaffaroni A, Goldstein A, McBride WJ, Li TK (2002) The reinforcing effects of acetaldehyde in the posterior ventral tegmental area of alcohol-preferring rats. Pharmacol Biochem Behav 72:55–64PubMedGoogle Scholar
  181. 181.
    Quintanilla ME, Tampier L (2003) Acetaldehyde-reinforcing effects: differences in low-alcohol-drinking (UChA) and high-alcohol-drinking (UChB) rats. Alcohol 31:63–69PubMedGoogle Scholar
  182. 182.
    Belluzzi JD, Wang R, Leslie FM (2005) Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 30:705–712PubMedGoogle Scholar
  183. 183.
    Quertemont E, Tambour S, Tirelli E (2005) The role of acetaldehyde in the neurobehavioral effects of ethanol: a comprehensive review of animal studies. Prog Neurobiol 75:247–274PubMedGoogle Scholar
  184. 184.
    Quertemont E, Tambour S, Bernaerts P, Zimatkin SM, Tirelli E (2004) Behavioral characterization of acetaldehyde in C57BL/6J mice: locomotor, hypnotic, anxiolytic and amnesic effects. Psychopharmacology (Berl) 177:84–92Google Scholar
  185. 185.
    Ward RJ, Colantuoni C, Dahchour A, Quertemont E, De Witte P (1997) Acetaldehyde-induced changes in monoamine and amino acid extracellular microdialysate content of the nucleus accumbens. Neuropharmacology 36:225–232PubMedGoogle Scholar
  186. 186.
    Hasler G, Luckenbaugh DA, Snow J, Meyers N, Waldeck T, Geraci M, Roiser J, Knutson B, Charney DS, Drevets WC (2009) Reward processing after catecholamine depletion in unmedicated, remitted subjects with major depressive disorder. Biol Psychiatry 66:201–205PubMedGoogle Scholar
  187. 187.
    Koob GF (2006) The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 101(Suppl 1):23–30PubMedGoogle Scholar
  188. 188.
    Wolters EC, Van Der Werf YD, van den Heuvel OA (2008) Parkinson’s disease-related disorders in the impulsive-compulsive spectrum. J Neurol 255(Suppl 5):48–56PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Nathan Kline InstituteOrangeburgUSA

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