Pharmacological recruitment of the GABAergic tail of the ventral tegmental area by acute drug exposure

British Journal of Pharmacology

Volumn 161, Issue 8, 2010, Pages 1677-1691

  Kaufling, Jennifer ^a,b   Waltisperger, Elisabeth ^a   Bourdy, Romain ^a,b   Valera, Antoine ^b   Veinante, Pierre ^a,b   Freund Mercier, Marie José ^a,b   Barrot, Michel ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

DeltaFosB; Dopamine; GABA; Psychostimulant; RMTg; TVTA; VTA

Indexed keywords

1 [2 [BIS (4 FLUOROPHENYL)METHOXY]ETHYL] 4 (3 PHENYLPROPYL)PIPERAZINE DIHYDROCHLORIDE; 3,4 METHYLENEDIOXYMETHAMPHETAMINE; 4 AMINOBUTYRIC ACID RECEPTOR; 4 HYDROXYBUTYRIC ACID; ALCOHOL; CAFFEINE; COCAINE; DELTA9(11) TETRAHYDROCANNABINOL; DEXAMPHETAMINE; DEXFENFLURAMINE; DIAZEPAM; DOPAMINE TRANSPORTER; FLUOXETINE; GABAPENTIN; KETAMINE; METHYLPHENIDATE; MONOAMINE; MORPHINE; NORTRIPTYLINE; PHENCYCLIDINE; PSYCHOSTIMULANT AGENT; REBOXETINE; SEROTONIN TRANSPORTER; TRANSCRIPTION FACTOR DELTA FOSB; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG; VALPROIC ACID; VANOXERINE; VENLAFAXINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EXPOSURE; GABAERGIC SYSTEM; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; VENTRAL TEGMENTUM;

ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GAMMA-AMINOBUTYRIC ACID; MALE; NEURONS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-FOS; PSYCHOTROPIC DRUGS; RATS; RATS, SPRAGUE-DAWLEY; VENTRAL TEGMENTAL AREA;

EID: 78649414840     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00984.x     Document Type: Article

References (65)

1. Alexander SPH, Mathie A, Peters JA (2009). Guide to receptors and channels (GRAC), 4th edn. Br J Pharmacol 158 (Suppl. 1): S1-S254.
2. Arnt J, Scheel-Krüger J (1979). GABA in the ventral tegmental area: differential regional effects on locomotion, aggression and food intake after microinjection of GABA agonists and antagonists. Life Sci 25: 1351-1360.
3. Beck CH (1995). Acute treatment with antidepressant drugs selectively increases the expression of c-fos in the rat brain. J Psychiatry Neurosci 20: 25-32.
4. Berton O, Covington HE 3rd, Ebner K, Tsankova NM, Carle TL, Ulery P et al. (2007). Induction of DeltaFosB in the periaqueductal gray by stress promotes active coping responses. Neuron 55: 289-300.
5. Berton O, Guigoni C, Li Q, Bioulac BH, Aubert I, Gross CE et al. (2009). Striatal overexpression of DeltaJunD resets L-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 66: 554-561.
6. Bolanos CA, Perrotti LI, Edwards S, Eisch AJ, Barrot M, Olson VG et al. (2003). Phospholipase Cγ in distinct regions of the ventral tegmental area differentially modulates mood-related behaviors. J Neurosci 23: 7569-7576.
7. Brinschwitz K, Dittgen A, Madai VI, Lommel R, Geisler S, Veh RW (2010). Glutamatergic axons from the leteral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168: 463-476.
8. Carlezon WA Jr, Haile CN, Coppersmith R, Hayashi Y, Malinow R, Neve RL et al. (2000). Distinct sites of opiate reward and aversion within the midbrain identified using a herpes simplex virus vector expressing GluR1. J Neurosci 20: RC62.
9. Carter LP, Loel W, France CP (2009). Behavioral analyses of GHB: receptor mechanisms. Pharmacol Ther 121: 100-114.
10. Castellani S, Adams PM (1981). Acute and chronic phencyclidine effects on locomotor activity, stereotypy and ataxia in rats. Eur J Pharmacol 73: 143-154.
11. Chaouloff F, Durand M, Mormède P (1997). Anxiety- and activity-related effects of diazepam and chlordiazepoxide in the rat light/dark and dark/light tests. Behav Brain Res 85: 27-35.
12. Cryan JF, Valentino RJ, Lucki I (2005). Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 29: 547-569.
13. Deurveilher S, Lo H, Murphy JA, Burns J, Semba K (2006). Differential c-Fos immunoreactivity in arousal-promoting cell groups following systemic administration of caffeine in rats. J Comp Neurol 498: 667-689.
14. Ferré S (2008). An update on the mechanisms of the psychostimulant effects of caffeine. J Neurochem 105: 1067-1079.
15. Ferreira JG, Del-Fava F, Hasue RH, Shammah-Lagnado SJ (2008). Organization of ventral tegmental area projections to the ventral tegmental area-nigral complex in the rat. Neuroscience 153: 196-213.
16. Geisler S, Marinelli M, Degarmo B, Becker ML, Freiman AJ, Beales M et al. (2008). Prominent activation of brainstem and pallidal afferents of the ventral tegmental area by cocaine. Neuropsychopharmacology 33: 2688-2700.
17. Grace AA, Floresco SB, Goto Y, Lodge DJ (2007). Regulation of firing of dopamineegic neurons and control of goal-directed behaviors. Trends Neurosci 30: 220-227.
18. Gruner JA, Marcy VR, Yin-Guo L, Bozyczko-Coyne D, Marino MJ, Gasior M (2009). The roles of dopamine transport inhibition and dopamine release facilitation in wake enhancement and rebound hypersomnolence induced by dopaminergic agents. Sleep 32: 1425-1438.
19. Hiroi N, Graybiel AM (1996). Atypical and typical neuroleptic treatments induce distinct programs of transcription factor expression in the striatum. J Comp Neurol 374: 70-83.
20. Hope BT, Nye HE, Kelz MB, Self DW, Iadarola MJ, Nakabeppu Y et al. (1994a). Induction of a long-lasting AP-1 complex composed of altered Fos-like proteins in brain by chronic cocaine and other chronic treatments. Neuron 13: 1235-1244.
21. Hope BT, Kelz MB, Duman RS, Nestler EJ (1994b). Chronic electroconvulsive seizure (ECS) treatment results in expression of a longlasting AP-1 complex in brain with altered composition and characteristics. J Neurosci 14: 4318-4328.
22. Ikemoto S (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56: 27-78.
23. Ikemoto S, Qin M, Liu ZH (2006). Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area. J Neurosci 26: 723-730.
24. Iversen SD, Iversen LL (2007). Dopamine: 50 years in perspective. Trends Neurosci 30: 188-193.
25. Jhou TC, Geisler S, Marinelli M, Degarmo BA, Zahm DS (2009a). The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol 513: 566-596.
26. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC (2009b). The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61: 786-800.
27. Kalivas PW, Duffy P (1988). Effects of daily cocaine and morphine treatment on somatodendritic and terminal field dopamine release. J Neurochem 50: 1498-1504.
28. Kaufling J, Veinante P, Pawlowski SA, Freund-Mercier MJ, Barrot M (2009). Afferents to the GABAergic tail of the ventral tegmental area in the rat. J Comp Neurol 513: 597-621.
29. Kaufling J, Veinante P, Pawlowski SA, Freund-Mercier MJ, Barrot M (2010). Gamma-aminobutyric acid cells with cocaine-induced DeltaFosB in the ventral tegmental area innervate mesolimbic neurons. Biol Psychiatry 67: 88-92.
30. Le Moal M, Simon H (1991). Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiol Rev 71: 155-234.
31. Lepore M, Vorel SR, Lowinson J, Gardner EL (1995). Conditioned place preference induced by delat-9-tetrahydrocannabinol: comparison with cocaine, morphine, and food reward. Life Sci 56: 2073-2080.
32. Luis-Delgado OE, Barrot M, Rodeau JL, Ulery PG, Freund-Mercier MJ, Lasbennes F (2006). The transcription factor DeltaFosB is recruited by inflammatory pain. J Neurochem 98: 1423-1431.
33. McClung CA, Ulery PG, Perrotti LI, Zachariou V, Berton O, Nestler EJ (2004). DeltaFosB: a molecular switch for long-term adaptation in the brain. Mol Brain Res 132: 146-154.
34. McDaid J, Graham MP, Napier TC (2006). Methamphetamine-induced sensitization differentially alters pCREB and Δ-FosB throughout the limbic circuit of the mammalian brain. Mol Pharmacol 70: 2064-2074.
35. McGahan L, Hakim AM, Nakabeppu Y, Robertson GS (1998). Ischemia-induced CA1 neuronal death is preceded by elevated FosB and Jun expression and reduced NGFI-A and JunB levels. Mol Brain Res 56: 146-161.
36. Maitre M (1997). The γ-hydroxybutyrate signalling system in brain: organization and functional implications. Prog Neurobiol 51: 337-361.
37. Millan MJ, Dekeyne A, Papp M, Drieu La Rochelle C, MacSweeny C, Peglion JL et al. (2001). S33005, a novel ligand at both serotonin and norepinephrine transporters: II. Behavioral profile in comparison with venlafaxine, reboxetine, citalopram, and clomipramine. J Pharmacol Exp Ther 298: 581-591.
38. Nehlig A, Daval JL, Debry G (1992). Caffeine and the central nervous system: mechanisms of action, biochemical, metabolic and psychostimulant effects. Brain Res Rev 17: 139-170.
39. Nestler EJ, Carlezon WA Jr (2006). The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59: 1151-1159.
40. Nestler EJ, Barrot M, Self DW (2001). DeltaFosB: a sustained molecular switch for addiction. Proc Natl Acad Sci USA 98: 11042-11046.
41. De Olmos S, Bender C, De Olmos JS, Lorenzo A (2009). Neurodegeneration and prolonged immediate early gene expression throughout cortical areas of the rat brain following acute administration of dizocilpine. Neuroscience 164: 1347-1359.
42. Olson VG, Nestler EJ (2007). Topographical organization of GABAergic neurons within the ventral tegmental area of the rat. Synapse 61: 87-95.
43. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ et al. (2005). Regulation of drug reward by CREB: evidence for two functionnaly distinct subregions of the ventral tegmental area. J Neurosci 25: 5553-5562.
44. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press: San Diego, CA.
45. Paxinos G, Watson C (2007). The Rat Brain in Stereotaxic Coordinates, 6th edn. Academic Press: San Diego, CA, fig 89-92.
46. Pedersen LH, Blackburn-Munro G (2006). Pharmacological characterisation of place escape/avoidance behaviour in the rat chronic constriction injury model of neuropathic pain. Psychopharmacology 185: 208-217.
47. Perrotti LI, Hadeishi Y, Ulery PG, Barrot M, Monteggia L, Duman RS et al. (2004). Induction of DeltaFosB in reward-related brain structures after chronic stress. J Neurosci 24: 10594-10602.
48. Perrotti LI, Bolanos CA, Choi KH, Russo SJ, Edwards S, Ulery PG et al. (2005). DeltaFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment. Eur J Neurosci 21: 2817-2824.
49. Perrotti LI, Weaver RR, Robison B, Renthal W, Maze I, Yazdani S et al. (2008). Distinct patterns of DeltaFosB induction in brain by drugs of abuse. Synapse 62: 358-369.
50. Pich EM, Pagliusi SR, Tessari M, Talabot-Ayer D, Hooft van Huijsduijnen R, Chiamulera C (1997). Common neural substrates for the addictive properties of nicotine and cocaine. Science 275: 83-86.
51. Rodd ZA, Bell RL, Kuc KA, Zhang Y, Murphy JM, McBride WJ (2005a). Intracranial self-administration of cocaine within the posterior ventral tegmental area of Wistar rats: evidence for involvement of serotonin-3 receptors and dopamine neurons. J Pharmacol Exp Ther 31: 134-145.
52. Rodd ZA, Bell RL, Zhang Y, Murphy JM, Goldstein A, Zaffaroni A et al. (2005b). Regional heterogeneity for the intracranial self-administration of ethanol and acetaldehyde within the ventral tegmental area of alcohol-preferring (P) rats: involvement of dopamine and serotonin. Neuropsychopharmacology 30: 330-338.
53. Rodd-Henricks ZA, McKinzie DL, Crile RS, Murphy JM, McBride WJ (2000). Regional heterogeneity for the intracranial self-administration of ethanol within the ventral tegmental area of female Wistar rats. Psychopharmacology 149: 217-224.
54. 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: 55-64.
55. Scammell TE, Estabrooke IV, McCarthy MT, Chemelli RM, Yanagisawa M, Miller MS et al. (2000). Hypothalamic arousal regions are activated during modafinil-induced wakefulness. J Neurosci 20: 8620-8628.
56. Schultz W (2007). Behavioral dopamine signals. Trends Neurosci 30: 203-210.
57. Stephenson CP, Hunt GE, Topple AN, McGregor IS (1999). The distribution of 3, 4-methylenedioxymethamphetamine 'Ecstasy'-induced c-fos expression in rat brain. Neuroscience 92: 1011-1023.
58. Tose R, Kushikata T, Yoshida H, Kudo M, Furukawa K, Ueno S et al. (2009). Orexin A decreases ketamine-induced anesthesia time in the rat: relevance to brain noradrenergic neuronal activity. Anesth Analg 108: 491-495.
59. Vickers SP, Clifton PG, Dourish CT (1996). Behavioural evidence that d-fenfluramine-induced anorexia in the rat is not mediated by the 5-HT1A receptor subtype. Psychopharmacology 125: 168-175.
60. Vilpoux C, Warmault V, Pierrefiche O, Daoust M, Naassila M (2009). Ethanol-sensitive brain regions in rat and mouse: a cartographic review, using immediate early gene expression. Alcohol Clin Exp Res 33: 945-969.
61. Wallace DL, Vialou V, Rios L, Carle-Florence TL, Chakravarty S, Kumar A et al. (2008). The influence of DeltaFosB in the nucleus accumbens on natural reward-related behavior. J Neurosci 28: 10272-10277.
62. Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ et al. (2002). DeltaFosB regulates wheel running. J Neurosci 22: 8133-8138.
63. Yalcin I, Tessier LH, Petit-Demoulière N, Doridot S, Hein L, Freund-Mercier MJ et al. (2009). Beta2-adrenoceptors are essential for desipramine, venlafaxine or reboxetine action in neuropathic pain. Neurobiol Dis 33: 386-394.
64. Zangen A, Ikemoto S, Zadina JE, Wise RA (2002). Rewarding and psychomotor stimulant effects of endomorphin-1: anteroposterior differences within the ventral tegmental area and lack of effect in nucleus accumbens. J Neurosci 22: 7225-7233.
65. Zangen A, Solinas M, Ikemoto S, Goldberg SR, Wise RA (2006). Two brain sites for cannabinoid reward. J Neurosci 26: 4901-4907.