Long-lasting modulation of glutamatergic transmission in VTA dopamine neurons after a single dose of benzodiazepine agonists

Neuropsychopharmacology

Volumn 34, Issue 2, 2009, Pages 290-298

  Heikkinen, Anne E ^a   Möykkynen, Tommi P ^a   Korpi, Esa R ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

AMPA receptors; Benzodiazepine dependence; Diazepam; Midbrain dopamine neurons; Plasticity; Zolpidem

Indexed keywords

AMPA RECEPTOR; DIAZEPAM; DIZOCILPINE; FLUMAZENIL; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; ZOLPIDEM;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG DEPENDENCE; FEMALE; LIMBIC CORTEX; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BENZODIAZEPINES; DIAZEPAM; DIZOCILPINE MALEATE; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; FLUMAZENIL; GLUTAMIC ACID; MALE; MICE; MICE, INBRED C57BL; MORPHINE; NEURONS; PATCH-CLAMP TECHNIQUES; PYRIDINES; RECEPTORS, AMPA; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTAL AREA;

EID: 57849098746     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2008.89     Document Type: Article

References (71)

1. Allison C, Pratt JA (2006). Differential effects of two chronic diazepam treatment regimes on withdrawal anxiety and AMPA receptor characteristics. Neuropsychopharmacology 31: 602-619.
2. 3H]zolpidem binding in the rat brain: an imidazopyridine with agonist properties at central benzodiazepine receptors. Eur J Pharmacol 130: 257-263.
3. Ashton H (2005). The diagnosis and management of benzodiazepine dependence. Curr Opin Psychiatry 18: 249-255.
4. A receptors. Neuropsychopharmacology 20: 255-262.
5. 1) subtype. J Pharmacol Exp Ther 245: 1033-1041.
6. Bonci A, Malenka RC (1999). Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J Neurosci 19: 3723-3730.
7. Cameron DL, Wessendorf MW, Williams JT (1997). A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids. Neuroscience 77: 155-166.
8. Carlezon Jr WA, Nestler EJ (2002). Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci 25: 610-615.
9. Carlezon Jr WA, Boundy VA, Haile CN, Lane SB, Kalb RG, Neve RL et al (1997). Sensitization to morphine induced by viral-mediated gene transfer. Science 277: 812-814.
10. Coutinho CB, Cheripko JA, Carbone JJ (1969). Relationship between the duration of anticonvulsant activity of chlordiazepoxide and systemic levels of the parent compound and its major metabolites in mice. Biochem Pharmacol 18: 303-316.
11. Crestani F, Martin JR, Möhler H, Rudolph U (2000). Mechanism of action of the hypnotic zolpidem in vivo. Br J Pharmacol 131: 1251-1254.
12. Darcourt G, Pringuey D, Salliere D, Lavoisy J (1999). The safety and tolerability of zolpidem - an update. J Psychopharmacol 13: 81-93.
13. Di Chiara G, Imperato A (1988). Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85: 5274-5278.
14. Dobrunz LE, Stevens CF (1997). Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
15. A receptors. Eur J Pharmacol 244: 29-35.
16. Faleiro LJ, Jones S, Kauer JA (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.
17. A receptor. Eur J Pharmacol 246: 283-287.
18. Finlay JM, Damsma G, Fibiger HC (1992). Benzodiazepine-induced decreases in extracellular concentrations of dopamine in the nucleus accumbens after acute and repeated administration. Psychopharmacology (Berl) 106: 202-208.
19. Fitzgerald LW, Ortiz J, Hamedani AG, Nestler EJ (1996). Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents. J Neurosci 16: 274-282.
20. Frey HH, Löscher W (1982). Anticonvulsant potency of unmetabolized diazepam. Pharmacology 25: 154-159.
21. Gobbi M, Barone D, Mennini T, Garattini S (1987). Diazepam and desmethyldiazepam differ in their affinities and efficacies at 'central' and 'peripheral' benzodiazepine receptors. J Pharm Pharmacol 39: 388-391.
22. Greenblatt DJ, Sethy VH (1990). Benzodiazepine concentrations in brain directly reflect receptor occupancy: studies of diazepam, lorazepam, and oxazepam. Psychopharmacology (Berl) 102: 373-378.
23. Griffiths RR, Johnson MW (2005). Relative abuse liability of hypnotic drugs: a conceptual framework and algorithm for differentiating among compounds. J Clin Psychiatry 66(Suppl 9): 31-41.
24. Griffiths RR, Weerts EM (1997). Benzodiazepine self-administration in humans and laboratory animals - implications for problems of long-term use and abuse. Psychopharmacology (Berl) 134: 1-37.
25. Hajak G, Müller WE, Wittchen HU, Pittrow D, Kirch W (2003). Abuse and dependence potential for the non-benzodiazepine hypnotics zolpidem and zopiclone: a review of case reports and epidemiological data. Addiction 98: 1371-1378.
26. Harte M, O'Connor WT (2004). Evidence for a differential medial prefrontal dopamine D1 and D2 receptor regulation of local and ventral tegmental glutamate and GABA release: a dual probe microdialysis study in the awake rat. Brain Res 1017: 120-129.
27. Huang YY, Nguyen PV, Abel T, Kandel ER (1996). Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn Mem 3: 74-85.
28. Hucker HB, Hutt JE, White SD, Arison BH, Zacchei AG (1983). Disposition and metabolism of (+)-5-methyl-10,11-dihydro-5H-dibenzo[ a,d] cyclohepten-5,10-imine in rats, dogs, and monkeys. Drug Metab Dispos 11: 54-58.
29. Hunkeler W, Möhler H, Pieri L, Polc P, Bonetti EP, Cumin R et al (1981). Selective antagonists of benzodiazepines. Nature 290: 514-516.
30. A receptor-specific expression profiling. J Neurochem 88: 1059-1067.
31. Izzo E, Auta J, Impagnatiello F, Pesold C, Guidotti A, Costa E (2001). Glutamic acid decarboxylase and glutamate receptor changes during tolerance and dependence to benzodiazepines. Proc Natl Acad Sci USA 98: 3483-3488.
32. Jones S, Bonci A (2005). Synaptic plasticity and drug addiction. Curr Opin Pharmacol 5: 20-25.
33. Kauer JA (2004). Learning mechanisms in addiction: synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse. Annu Rev Physiol 66: 447-475.
34. Khan GM, Smolders I, Ebinger G, Michotte Y (2000). Flumazenil prevents diazepam-elicited anticonvulsant action and concomitant attenuation of glutamate overflow. Eur J Pharmacol 407: 139-144.
35. Klockowski PM, Levy G (1987). Simultaneous determination of diazepam and its active metabolites in rat serum, brain and cerebrospinal fluid by high-performance liquid chromatography. J Chromatogr 422: 334-339.
36. Koob GF (1992). Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13: 177-184.
37. A receptors. Prog Neurobiol 67: 113-159.
38. Lister RG, Greenblatt DJ, Abernethy DR, File SE (1984). Pharmacokinetic studies on Ro 15-1788, a benzodiazepine receptor ligand, in the brain of the rat. Brain Res 290: 183-186.
39. Liu QS, Pu L, Poo MM (2005). Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437: 1027-1031.
40. A/ benzodiazepine receptor heterogeneity: neurophysiological implications. Neuropharmacology 34: 245-254.
41. Lüscher C, Nicoll RA, Malenka RC, Muller D (2000). Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3: 545-550.
42. Mandema JW, Gubbens-Stibbe JM, Danhof M (1991). Stability and pharmacokinetics of flumazenil in the rat. Psychopharmacology (Berl) 103: 384-387.
43. Margolis EB, Lock H, Hjelmstad GO, Fields HL (2006). The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol 577: 907-924.
44. McClung CA, Nestler EJ (2008). Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 33: 3-17.
45. Neuhoff H, Neu A, Liss B, Roeper J (2002). I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22: 1290-1302.
46. O'Brien DP, White FJ (1987). Inhibition of non-dopamine cells in the ventral tegmental area by benzodiazepines: relationship to A10 dopamine cell activity. Eur J Pharmacol 142: 343-354.
47. A receptor subunit variants in midbrain dopaminergic neurons. J Neurochem 89: 7-14.
48. Pan B, Hillard CJ, Liu QS (2008). Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci 28: 1385-1397.
49. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004). Recycling endosomes supply AMPA receptors for LTP. Science 305: 1972-1975.
50. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM et al (2006). Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52: 817-830.
51. Petursson H (1994). The benzodiazepine withdrawal syndrome. Addiction 89: 1455-1459.
52. A receptor subunit for benzodiazepine pharmacology. Nature 338: 582-585.
53. A receptor subtypes mediate the anxiolytic, abuse-related, and motor effects of benzodiazepine-like drugs in primates. Proc Natl Acad Sci USA 102: 915-920.
54. Saal D, Dong Y, Bonci A, Malenka RC (2003). Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37: 577-582.
55. Sarti F, Borgland SL, Kharazia VN, Bonci A (2007). Acute cocaine exposure alters spine density and long-term potentiation in the ventral tegmental area. Eur J Neurosci 26: 749-756.
56. A receptors mediating glutamate release in an alcohol-sensitive rat line. Neuropharmacology 38: 1273-1279.
57. Schultz W (1998). Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27.
58. A receptor subtypes. Pharmacol Rev 47: 181-234.
59. Song J, Shen G, Greenfield Jr LJ, Tietz EI (2007). Benzodiazepine withdrawal-induced glutamatergic plasticity involves upregulation of GluR1-containing α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in hippocampal CA1 neurons. J Pharmacol Exp Ther 322: 569-581.
60. Spyraki C, Fibiger HC (1988). A role for the mesolimbic dopamine system in the reinforcing properties of diazepam. Psychopharmacology (Berl) 94: 133-137.
61. Stephens DN (1995). A glutamatergic hypothesis of drug dependence: extrapolations from benzodiazepine receptor ligands. Behav Pharmacol 6: 425-446.
62. Steppuhn KG, Turski L (1993). Diazepam dependence prevented by glutamate antagonists. Proc Natl Acad Sci USA 90: 6889-6893.
63. Sutton MA, Schuman EM (2006). Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127: 49-58.
64. Thomas MJ, Beurrier C, Bonci A, Malenka RC (2001). Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat Neurosci 4: 1217-1223.
65. Ungless MA, Whistler JL, Malenka RC, Bonci A (2001). Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411: 583-587.
66. Van Sickle BJ, Cox AS, Schak K, Greenfield Jr LJ, Tietz EI (2002). Chronic benzodiazepine administration alters hippocampal CA1 neuron excitability: NMDA receptor function and expression. Neuropharmacology 43: 595-606.
67. Waelti P, Dickinson A, Schultz W (2001). Dopamine responses comply with basic assumptions of formal learning theory. Nature 412: 43-48.
68. Wanat MJ, Hopf FW, Stuber GD, Phillips PE, Bonci A (2008). Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586: 2157-2170.
69. A receptor. J Med Chem 37: 4576-4580.
70. Wise RA (1996). Neurobiology of addiction. Curr Opin Neurobiol 6: 243-251.
71. Xiang K, Tietz EI (2007). Benzodiazepine-induced hippocampal CA1 neuron α-amino-3-hydroxy-5-methylisoxasole-4-propionic acid (AMPA) receptor plasticity linked to severity of withdrawal anxiety: differential role of voltage-gated calcium channels and N-methyl-D-aspartic acid receptors. Behav Pharmacol 18: 447-460.