The brain pattern of c-fos induction by two doses of amphetamine suggests different brain processing pathways and minor contribution of behavioural traits

Neuroscience

Volumn 168, Issue 3, 2010, Pages 691-705

  Rotllant, D ^a   Marquez C ^a   Nadal, R ^b   Armario, A ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUT DE NEUROCIÈNCIES   (Spain)

Author keywords

Anxiety; Brain circuits; Factorial analysis; Novelty seeking; Tryptophan hydroxylase 2; Tyrosine hydroxylase

Indexed keywords

AMPHETAMINE; PROTEIN C FOS; CENTRAL STIMULANT AGENT; TPH2 PROTEIN, RAT; TRYPTOPHAN HYDROXYLASE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CORPUS STRIATUM; DORSAL RAPHE NUCLEUS; GABAERGIC SYSTEM; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; MALE; NERVE CELL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VENTRAL TEGMENTUM; ANIMAL; BIOSYNTHESIS; BRAIN; DRUG EFFECTS; EXPLORATORY BEHAVIOR; FACTORIAL ANALYSIS; METABOLISM; PSYCHOLOGY; RAPHE NUCLEUS; SPRAGUE DAWLEY RAT;

AMPHETAMINE; ANIMALS; ANXIETY; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; EXPLORATORY BEHAVIOR; FACTOR ANALYSIS, STATISTICAL; MALE; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; TRYPTOPHAN HYDROXYLASE; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA;

EID: 77953120764     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.04.020     Document Type: Article

References (102)

1. Armario A. The contribution of immediate early genes to the understanding of brain processing of stressors. Immediate early genes in sensory processing, cognitive performance and neurological disorders 2006, 199-221. Springer Science, New York. R. Pinaud, L. Tremere (Eds.).
2. Armario A. The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors?. CNS Neurol Disord Drug Targets 2006, 5:485-501.
3. Aznar S., Qian Z.X., Knudsen G.M. Non-serotonergic dorsal and median raphe projection onto parvalbumin- and calbindin-containing neurons in hippocampus and septum. Neuroscience 2004, 124:573-581.
4. Babai P., Anokhin K.V., Dolgov N., Sudakov K.V. Characteristics of c-fos gene expression in the brains of rats with different investigative and defensive behaviors. Neurosci Behav Physiol 2001, 31:583-588.
5. Badiani A., Oates M.M., Day H.E., Watson S.J., Akil H., Robinson T.E. Amphetamine-induced behavior, dopamine release, and c-fos mRNA expression: modulation by environmental novelty. J Neurosci 1998, 18:10579-10593.
6. Belin D., Mar A.C., Dalley J.W., Robbins T.W., Everitt B.J. High impulsivity predicts the switch to compulsive cocaine-taking. Science 2008, 320:1352-1355.
7. Bernardini G.L., Gu X., Viscardi E., German D.C. Amphetamine-induced and spontaneous release of dopamine from A9 and A10 cell dendrites: an in vitro electrophysiological study in the mouse. J Neural Transm Gen Sect 1991, 84:183-193.
8. Byrnes J.J., Wallace L.J. Amphetamine-induced sensitization and release of dopamine in slices from the ventral tegmental area of rats is enhanced following administration of cholera toxin into the ventral tegmental area. Neurosci Lett 1997, 223:45-48.
9. Carr K.D., Kutchukhidze N. Chronic food restriction increases fos-like immunoreactivity (FLI) induced in rat forebrain by intraventricular amphetamine. Brain Res 2000, 861:88-96.
10. Chefer V.I., Zakharova I., Shippenberg T.S. Enhanced responsiveness to novelty and cocaine is associated with decreased basal dopamine uptake and release in the nucleus accumbens: quantitative microdialysis in rats under transient conditions. J Neurosci 2003, 23:3076-3084.
11. Colussi-Mas J., Geisler S., Zimmer L., Zahm D.S., Berod A. Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double-labelling study. Eur J Neurosci 2007, 26:1011-1025.
12. Dalia A., Wallace L.J. Amphetamine induction of c-fos in the nucleus accumbens is not inhibited by glutamate antagonists. Brain Res 1995, 694:299-307.
13. Datiche F., Luppi P.H., Cattarelli M. Serotonergic and non-serotonergic projections from the raphe nuclei to the piriform cortex in the rat: a cholera toxin B subunit (CTb) and 5-HT immunohistochemical study. Brain Res 1995, 671:27-37.
14. Day H.E., Badiani A., Uslaner J.M., Oates M.M., Vittoz N.M., Robinson T.E., Watson S.J., Akil H. Environmental novelty differentially affects c-fos mRNA expression induced by amphetamine or cocaine in subregions of the bed nucleus of the stria terminalis and amygdala. J Neurosci 2001, 21:732-740.
15. Day H.E., Nebel S., Sasse S., Campeau S. Inhibition of the central extended amygdala by loud noise and restraint stress. Eur J Neurosci 2005, 21:441-454.
16. Dellu F., Piazza P.V., Mayo W., Le Moal M., Simon H. Novelty-seeking in rats-biobehavioral characteristics and possible relationship with the sensation-seeking trait in man. Neuropsychobiology 1996, 34:136-145.
17. Deminiere J.M., Piazza P.V., Le Moal M., Simon H. Experimental approach to individual vulnerability to psychostimulant addiction. Neurosci Biobehav Rev 1989, 13:141-147.
18. Descarries L., Watkins K.C., Garcia S., Beaudet A. The serotonin neurons in nucleus raphe dorsalis of adult rat: a light and electron microscope radioautographic study. J Comp Neurol 1982, 207:239-254.
19. Descarries L., Lemay B., Doucet G., Berger B. Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 1987, 21:807-824.
20. Deutch A.Y., Bubser M., Young C.D. Psychostimulant-induced Fos protein expression in the thalamic paraventricular nucleus. J Neurosci 1998, 18:10680-10687.
21. Dietz D.M., Tapocik J., Gaval-Cruz M., Kabbaj M. Dopamine transporter, but not tyrosine hydroxylase, may be implicated in determining individual differences in behavioral sensitization to amphetamine. Physiol Behav 2005, 86:347-355.
22. Engber T.M., Koury E.J., Dennis S.A., Miller M.S., Contreras P.C., Bhat R.V. Differential patterns of regional c-Fos induction in the rat brain by amphetamine and the novel wakefulness-promoting agent modafinil. Neurosci Lett 1998, 241:95-98.
23. Fallon J.H., Koziell D.A., Moore R.Y. Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol 1978, 180:509-532.
24. Ferguson S.M., Norton C.S., Watson S.J., Akil H., Robinson T.E. Amphetamine-evoked c-fos mRNA expression in the caudate-putamen: the effects of DA and NMDA receptor antagonists vary as a function of neuronal phenotype and environmental context. J Neurochem 2003, 86:33-44.
25. Fields H.L., Hjelmstad G.O., Margolis E.B., Nicola S.M. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 2007, 30:289-316.
26. Fray P.J., Sahakian B.J., Robbins T.W., Koob G.F., Iversen S.D. An observational method for quantifying the behavioural effects of dopamine agonists: contrasting effects of d-amphetamine and apomorphine. Psychopharmacology 1980, 69:253-259.
27. Gagliano H., Andero R., Armario A., Nadal R. Repeated amphetamine administration in rats revealed consistency across days and a complete dissociation between locomotor and hypothalamic-pituitary-adrenal axis effects of the drug. Psychopharmacology 2009, 207:447-459.
28. Genova L.M., Hyman S.E. 5-HT3 receptor activation is required for induction of striatal c-Fos and phosphorylation of ATF-1 by amphetamine. Synapse 1998, 30:71-78.
29. Graybiel A.M., Moratalla R., Robertson H.A. Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc Natl Acad Sci U S A 1990, 87:6912-6916.
30. Haddjeri N., Lavoie N., Blier P. Electrophysiological evidence for the tonic activation of 5-HT(1A) autoreceptors in the rat dorsal raphe nucleus. Neuropsychopharmacology 2004, 29:1800-1806.
31. Hamamura T., Ichimaru Y. Amphetamine sensitization augments amphetamine-induced Fos expression in the lateral habenula. Brain Res 1997, 767:140-143.
32. Harlan R.E., Garcia M.M. Drugs of abuse and immediate-early genes in the forebrain. Mol Neurobiol 1998, 16:221-267.
33. Heeringa M.J., Abercrombie E.D. Biochemistry of somatodendritic dopamine release in substantia nigra: an in vivo comparison with striatal dopamine release. J Neurochem 1995, 65:192-200.
34. Heidenreich B.A., Basse-Tomusk A.E., Rebec G.V. Serotonergic dorsal raphe neurons: subsensitivity to amphetamine with long-term treatment. Neuropharmacology 1987, 26:719-724.
35. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003, 24:151-180.
36. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog Neurobiol 1996, 50:83-107.
37. Hoffman G.E., Lyo D. Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out'?. J Neuroendocrinol 2002, 14:259-268.
38. Holdefer R.N., Jensen R.A. The effects of peripheral D-amphetamine, 4-OH amphetamine, and epinephrine on maintained discharge in the locus coeruleus with reference to the modulation of learning and memory by these substances. Brain Res 1987, 417:108-117.
39. Hooks M.S., Jones G.H., Smith A.D., Neill D.B., Justice J.B. Individual differences in locomotor activity and sensitization. Pharmacol Biochem Behav 1991, 38:467-470.
40. Hooks M.S., Kalivas P.W. Involvement of dopamine and excitatory amino acid transmission in novelty-induced motor activity. J Pharmacol Exp Ther 1994, 269:976-988.
41. Iversen S.D., Kelly P.H., Miller R.J., Seviour P. Proceedings: amphetamine and apomorphine responses in the rat after lesion of mesolimbic or striatal dopamine neurones. Br J Pharmacol 1975, 54:244P.
42. Jaber M., Cador M., Dumartin B., Normand E., Stinus L., Bloch B. Acute and chronic amphetamine treatments differently regulate neuropeptide messenger RNA levels and Fos immunoreactivity in rat striatal neurons. Neuroscience 1995, 65:1041-1050.
43. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-229.
44. Johansson B., Lindstrom K., Fredholm B.B. Differences in the regional and cellular localization of c-fos messenger RNA induced by amphetamine, cocaine and caffeine in the rat. Neuroscience 1994, 59:837-849.
45. Kabbaj M. Individual differences in vulnerability to drug abuse: the high responders/low responders model. CNS Neurol Disord Drug Targets 2006, 5:513-520.
46. Kabbaj M., Akil H. Individual differences in novelty-seeking behavior in rats: a c-fos study. Neuroscience 2001, 106:535-545.
47. Kelly P.H., Seviour P.W., Iversen S.D. Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res 1975, 94:507-522.
48. Koh T., Nakazawa M., Kani K., Maeda T. Investigations of origins of serotonergic projection to developing rat visual cortex: a combined retrograde tracing and immunohistochemical study. Brain Res Bull 1991, 27:675-684.
49. Köhler C., Chan-Palay V., Steinbusch H. The distribution and origin of serotonin-containing fibers in the septal area: a combined immunohistochemical and fluorescent retrograde tracing study in the rat. J Comp Neurol 1982, 209:91-111.
50. Konradi C., Leveque J.C., Hyman S.E. Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends on postsynaptic NMDA receptors and calcium. J Neurosci 1996, 16:4231-4329.
51. Koob G., Le Moal M. Neurobiology of addiction 2006, Academic Press, London.
52. Kovacs K.J. c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 1998, 33:287-297.
53. Kreek M.J., Koob G.F. Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend 1998, 51:23-47.
54. LaHoste G.J., Henry B.L., Marshall J.F. Dopamine D1 receptors synergize with D2, but not D3 or D4, receptors in the striatum without the involvement of action potentials. J Neurosci 2000, 20:6666-6671.
55. Lillrank S.M., Lipska B.K., Bachus S.E., Wood G.K., Weinberger D.R. Amphetamine-induced c-fos mRNA expression is altered in rats with neonatal ventral hippocampal damage. Synapse 1996, 23:292-301.
56. Margolis E.B., Lock H., Hjelmstad G.O., Fields H.L. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?. J Physiol 2006, 577:907-924.
57. Marinelli M., White F.J. Enhanced vulnerability to cocaine self-administration is associated with elevated impulse activity of midbrain dopamine neurons. J Neurosci 2000, 20:8876-8885.
58. Mercuri N.B., Calabresi P., Bernardi G. The electrophysiological actions of dopamine and dopaminergic drugs on neurons of the substantia nigra pars compacta and ventral tegmental area. Life Sci 1992, 51:711-718.
59. Miyamoto S., Snouwaert J.N., Koller B.H., Moy S.S., Lieberman J.A., Duncan G.E. Amphetamine-induced Fos is reduced in limbic cortical regions but not in the caudate or accumbens in a genetic model of NMDA receptor hypofunction. Neuropsychopharmacology 2004, 29:2180-2188.
60. Muller C.P., Carey R.J., Huston J.P., De Souza Silva M.A. Serotonin and psychostimulant addiction: focus on 5-HT1A-receptors. Prog Neurobiol 2007, 81:133-178.
61. Muñoz A., Rodriguez-Pallares J., Guerra M.J., Labandeira-Garcia J.L. Host brain regulation of dopaminergic grafts function: role of the serotonergic and noradrenergic systems in amphetamine-induced responses. Synapse 2003, 47:66-76.
62. Nadal R., Rotllant D., Márquez C., Armario A. Perseverance of exploration in novel environments predicts morphine place conditioning in rats. Behav Brain Res 2005, 165:72-79.
63. Nikulina E.M., Covington H.E., Ganschow L., Hammer R.P., Miczek K.A. Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: Fos in the ventral tegmental area and amygdala. Neuroscience 2004, 123:857-865.
64. Ostrander M.M., Badiani A., Day H.E., Norton C.S., Watson S.J., Akil H., Robinson T.E. Environmental context and drug history modulate amphetamine-induced c-fos mRNA expression in the basal ganglia, central extended amygdala, and associated limbic forebrain. Neuroscience 2003, 120:551-571.
65. Pacak K., Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001, 22:502-548.
66. Palkovits M. Interconnections between the neuroendocrine hypothalamus and the central autonomic system. Geoffrey Harris Memorial Lecture, Kitakyushu, Japan, October 1998. Front Neuroendocrinol 1999, 20:270-295.
67. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, Inc, London.
68. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 1986, 24:525-529.
69. Perrotti L.I., Bolanos C.A., Choi K.H., Russo S.J., Edwards S., Ulery P.G., Wallace D.L., Self D.W., Nestler E.J., Barrot M. DeltaFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment. Eur J Neurosci 2005, 21:2817-2824.
70. Phillips G.D., Setzu E., Vugler A., Hitchcott P.K. An immunohistochemical examination of the effects of sensitisation on the mesotelencephalic dopaminergic response to d-amphetamine. Neuroscience 2003, 117:741-753.
71. Piazza P.V., Deminière J.M., Le Moal M., Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989, 245:1511-1513.
72. Piazza P.V., Deminière J.-M., Maccari S., Mormède P., Le Moal M., Simon H. Individual reactivity to novelty predicts probability of amphetamine self-administration. Behav Pharmacol 1990, 1:339-345.
73. Piazza P.V., Le Moal M. Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons. Annu Rev Pharmacol Toxicol 1996, 36:359-378.
74. Piazza P.V., Maccari S., Deminière J.M., Le Moal M., Mormède P., Simon H. Corticosterone levels determine individual vulnerability to amphetamine self-administration. Proc Natl Acad Sci U S A 1991, 88:2088-2092.
75. Ramirez O.A., Wang R.Y. Electrophysiological evidence for locus coeruleus norepinephrine autoreceptor subsensitivity following subchronic administration of D-amphetamine. Brain Res 1986, 385:415-419.
76. Rebec G.V., Curtis S.D., Zimmerman K.S. Dorsal raphe neurons: self-inhibition by an amphetamine-induced release of endogenous serotonin. Brain Res 1982, 251:374-379.
77. Robertson G.S., Damsma G., Fibiger H.C. Characterization of dopamine release in the substantia nigra by in vivo microdialysis in freely moving rats. J Neurosci 1991, 11:2209-2216.
78. Rotllant D., Nadal R., Armario A. Differential effects of stress and amphetamine administration on Fos-like protein expression in corticotropin releasing factor-neurons of the rat brain. Dev Neurobiol 2007, 67:702-714.
79. Rotllant D., Ons S., Carrasco J., Armario A. Evidence that metyrapone can act as a stressor: effect on pituitary-adrenal hormones, plasma glucose and brain c-fos induction. Eur J Neurosci 2002, 16:693-700.
80. Ruskin D.N., Marshall J.F. Amphetamine- and cocaine-induced fos in the rat striatum depends on D2 dopamine receptor activation. Synapse 1994, 18:233-240.
81. Sahakian B.J., Robbins T.W., Morgan M.J., Iversen S.D. The effects of psychomotor stimulants on stereotypy and locomotor activity in socially-deprived and control rats. Brain Res 1975, 84:195-205.
82. Shaham Y., Shalev U., Lu L., De Wit H., Stewart J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 2003, 168:3-20.
83. Shilling P.D., Kuczenski R., Segal D.S., Barrett T.B., Kelsoe J.R. Differential regulation of immediate-early gene expression in the prefrontal cortex of rats with a high vs low behavioral response to methamphetamine. Neuropsychopharmacology 2006, 31:2359-2367.
84. Snyder-Keller A.M. Striatal c-fos induction by drugs and stress in neonatally dopamine-depleted rats given nigral transplants: importance of NMDA activation and relevance to sensitization phenomena. Exp Neurol 1991, 113:155-165.
85. Stephenson C.P., Hunt G.E., Topple A.N., McGregor I.S. The distribution of 3,4-methylenedioxymethamphetamine "Ecstasy"-induced c-fos expression in rat brain. Neuroscience 1999, 92:1011-1023.
86. Sulzer D., Sonders M.S., Poulsen N.W., Galli A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 2005, 75:406-433.
87. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 1982, 9:321-353.
88. Swerdlow N.R., Koob G.F., Cador M., Lorang M., Hauger R.L. Pituitary-adrenal axis responses to acute amphetamine in the rat. Pharmacol Biochem Behav 1993, 45:629-637.
89. Thompson B. Exploratory and confirmatory factor analysis: understanding concepts and applications 2004, American Psychological Association, Washington, DC.
90. Timmerman W., Abercrombie E.D. Amphetamine-induced release of dendritic dopamine in substantia nigra pars reticulata: D1-mediated behavioral and electrophysiological effects. Synapse 1996, 23:280-291.
91. Todtenkopf M.S., Stellar J.R. Assessment of tyrosine hydroxylase immunoreactive innervation in five subregions of the nucleus accumbens shell in rats treated with repeated cocaine. Synapse 2000, 38:261-270.
92. Tong Z.Y., Overton P.G., Martinez-Cue C., Clark D. Do non-dopaminergic neurons in the ventral tegmental area play a role in the responses elicited in A10 dopaminergic neurons by electrical stimulation of the prefrontal cortex?. Exp Brain Res 1998, 118:466-476.
93. Trinh J.V., Nehrenberg D.L., Jacobsen J.P., Caron M.G., Wetsel W.C. Differential psychostimulant-induced activation of neural circuits in dopamine transporter knockout and wild type mice. Neuroscience 2003, 118:297-310.
94. Turgeon S.M., Pollack A.E., Schusheim L., Fink J.S. Effects of selective adenosine A1 and A2a agonists on amphetamine-induced locomotion and c-Fos in striatum and nucleus accumbens. Brain Res 1996, 707:75-80.
95. Turgeon S.M., Roche J.K. The delayed effects of phencyclidine enhance amphetamine-induced behavior and striatal C-Fos expression in the rat. Neuroscience 1999, 91:1265-1275.
96. Uslaner J., Badiani A., Day H.E., Watson S.J., Akil H., Robinson T.E. Environmental context modulates the ability of cocaine and amphetamine to induce c-fos mRNA expression in the neocortex, caudate nucleus, and nucleus accumbens. Brain Res 2001, 920:106-116.
97. Uslaner J., Badiani A., Norton C.S., Day H.E., Watson S.J., Akil H., Robinson T.E. Amphetamine and cocaine induce different patterns of c-fos mRNA expression in the striatum and subthalamic nucleus depending on environmental context. Eur J Neurosci 2001, 13:1977-1983.
98. Uslaner J., Norton C.S., Watson S.J., Akil H., Robinson T.E. Amphetamine-induced c-fos mRNA expression in the caudate-putamen and subthalamic nucleus: interactions between dose, environment, and neuronal phenotype. J Neurochem 2003, 85:105-114.
99. Valjent E., Pages C., Herve D., Girault J.A., Caboche J. Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 2004, 19:1826-1836.
100. Van der Werf Y.D., Witter M.P., Groenewegen H.J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 2002, 39:107-140.
101. Vanderschuren L.J., Schoffelmeer A.N., Van Leeuwen S.D., Hof L., Jonker A.J., Voorn P. Compartment-specific changes in striatal neuronal activity during expression of amphetamine sensitization are the result of drug hypersensitivity. Eur J Neurosci 2002, 16:2462-2468.
102. Voorn P., Vanderschuren L.J., Groenewegen H.J., Robbins T.W., Pennartz C.M. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 2004, 27:468-474.