GABA site agonist gaboxadol induces addiction-predicting persistent changes in ventral tegmental area dopamine neurons but is not rewarding in mice or baboons

Journal of Neuroscience

Volumn 32, Issue 15, 2012, Pages 5310-5320

  Vashchinkina, Elena ^a   Panhelainen, Anne ^a   Vekovischeva, Olga Yu ^a   Aitta Aho, Teemu ^a   Ebert, Bjarke ^b   Ator, Nancy A ^c   Korpi, Esa R ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b H LUNDBECK A S   (Denmark)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AMPA RECEPTOR; GABOXADOL; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADDICTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; LOCOMOTION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PAPIO HAMADRYAS; PLACE PREFERENCE; PRIORITY JOURNAL; REWARD; TRANSGENIC MOUSE; VENTRAL TEGMENTUM;

EID: 84859526586     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4697-11.2012     Document Type: Article

References (87)

1. Argilli E, Sibley DR, Malenka RC, England PM, Bonci A (2008) Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J Neurosci 28:9092-9100.
2. Ator NA (2000) Zaleplon and triazolam: drug discrimination, plasma levels, and self-administration in baboons. Drug Alcohol Depend 61:55-68.
3. Ator NA, Griffiths RR (2003) Principles of drug abuse liability assessment in laboratory animals. Drug Alcohol Depend 70:S55-S72.
4. A/benzodiazepine ligands via selective partialagonist efficacy at α1 and α2/3 subtypes. J Pharmacol Exp Ther 332:4-16.
5. Bagetta V, Picconi B, Marinucci S, Sgobio C, Pendolino V, Ghiglieri V, Fusco FR, Giampà C, Calabresi P (2011) Dopamine-dependent long-term depression is expressed in striatal spiny neurons of both direct and indirect pathways: implications for Parkinson's disease. J Neurosci 31:12513-12522.
6. A receptors: form, pharmacology, and function. J Neurosci 29:12757-12763.
7. Bellone C, Lüscher C (2006) Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat Neurosci 9:636-641.
8. Borgland SL, Malenka RC, Bonci A (2004) Acute and chronic cocaineinduced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats. J Neurosci 24:7482-7490.
9. Bowers MS, Chen BT, Bonci A (2010) AMPA receptor synaptic plasticity induced by psychostimulants: the past, present, and therapeutic future. Neuron 67:11-24.
10. Brischoux F, Chakraborty S, Brierley DI, Ungless MA (2009) Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A 106:4894-4899.
11. Brown MT, Bellone C, Mameli M, Labouèbe G, Bocklisch C, Balland B, Dahan L, Luján R, Deisseroth K, Lüscher C (2010) Drug-driven AMPA receptor redistribution mimicked by selective dopamine neuron stimulation. PLoS One 5:e15870.
12. A receptors. Br J Pharmacol 136:965-974.
13. A receptor α4 subunits mediate extrasynaptic inhibition in thalamus and dentate gyrus and the action of gaboxadol. Proc Natl Acad Sci U S A 103:15230-15235.
14. A receptor agonist muscimol acts preferentially through forebrain high-affinity binding sites. Neuropsychopharmacology 35:999-1007.
15. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18-41.
16. Cremers T, Ebert B (2007) Plasma and CNS concentrations of gaboxadol in rats following subcutaneous administration. Eur J Pharmacol 562:47-52.
17. Criswell HE, Ridings A (1983) Intravenous self-administration of morphine by naive mice. Pharmacol Biochem Behav 18:467-470.
18. Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1:1662-1670.
19. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
20. Dunn JM, Inderwies BR, Licata SC, Pierce RC (2005) Repeated administration of AMPA or a metabotropic glutamate receptor agonist into the rat ventral tegmental area augments the subsequent behavioral hyperactivity induced by cocaine. Psychopharmacology (Berl) 179:172-180.
21. Engblom D, Bilbao A, Sanchis-Segura C, Dahan L, Perreau-Lenz S, Balland B, Parkitna JR, Luján R, Halbout B, Mameli M, Parlato R, Sprengel R, Lüscher C, Schütz G, Spanagel R (2008) Glutamate receptors on dopamine neurons control the persistence of cocaine seeking. Neuron 59:497-508.
22. A receptors. Nat Rev Neurosci 6:215-229.
23. File SE (1986) Aversive and appetitive properties of anxiogenic and anxiolytic agents. Behav Brain Res 21:189-194.
24. Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates, Ed 3. Amsterdam: Elsevier.
25. A receptors: views from outside the synaptic cleft. Neuron 56:763-770.
26. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
27. Gray A, Allison C, Pratt JA (1999) A role for AMPA/kainate receptors in conditioned place preference induced by diazepam in the rat. Neurosci Lett 268:127-130.
28. Gremel CM, Cunningham CL (2007) Role of test activity in ethanolinduced disruption of place preference expression in mice. Psychopharmacology (Berl) 191:195-202.
29. Griffiths RR, Lamb RJ, Sannerud CA, Ator NA, Brady JV (1991) Selfinjection of barbiturates, benzodiazepines, and other sedative anxiolytics in baboons. Psychopharmacology 103:154-161.
30. Hajak G, Hedner J, Eglin M, Loft H, Stórustovu SI, Lütolf S, Lundahl J; Gaboxadol Study 99775 Group (2009) A 2-week efficacy and safety study of gaboxadol and zolpidem using electronic diaries in primary insomnia outpatients. Sleep Med 10:705-712.
31. 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.
32. Heikkinen AE, Möykkynen TP, Korpi ER (2009) Long-lasting modulation of glutamatergic transmission in VTA dopamine neurons after a single dose of benzodiazepine agonists. Neuropsychopharmacology 34:290-298.
33. Hyman SE (2005) Addiction: a disease of learning and memory. Am J Psychiatry 162:1414-1422.
34. Ikemoto S, Witkin BM, Zangen A, Wise RA (2004) Rewarding effects of AMPA administration into the supramammillary or posterior hypothalamic nuclei but not the ventral tegmental area. J Neurosci 24:5758-5765.
35. Imaizumi M, Takeda M, Fushiki T (2000) Effects of oil intake in the conditioned place preference test in mice. Brain Res 870:150-156.
36. Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483-488.
37. Kauer JA, Malenka RC (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8:844-858.
38. A receptor subtypes as targets for neuropsychiatric drug development. Pharmacol Ther 109:12-32.
39. 2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J Neurosci 31:126-132.
40. A agonists and partial agonists: THIP (gaboxadol) as a non-opioid analgesic and a novel type of hypnotic. Biochem Pharmacol 68:1573-1580.
41. Kuzmin AV, Patkina NA, Zvartau EE (1994) Analgesic and reinforcing effects of morphine in mice. Influence of Bay K-8644 and nimodipine. Brain Res 652:1-8.
42. Kuzmin AV, Gerrits MA, Zvartau EE, van Ree JM (2000) Influence of buprenorphine, butorphanol and nalbuphine on the initiation of intravenous cocaine self-administration in drug naive mice. Eur Neuropsychopharmacol 10:447-454.
43. Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773.
44. Lammel S, Ion DI, Roeper J, Malenka RC (2011) Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70:855-862.
45. Lüscher C, Malenka RC (2011) Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69:650-663.
46. Lüscher C, Ungless MA (2006) The mechanistic classification of addictive drugs. PLoS Med 3:e437.
47. Ma QP, Zhou Y, Han JS (1993) Noxious stimulation accelerated the expression of c-fos protooncogene in cholecystokininergic and dopaminergic neurons in the ventral tegmental area. Peptides 14:561-566.
48. Mallart A, Martin AR (1968) The relation between quantum content and facilitation at the neuromuscular junction of the frog. J Physiol 196:593-604.
49. Mameli M, Bellone C, Brown MT, Lüscher C (2011) Cocaine inverts rules for synaptic plasticity of glutamate transmission in the ventral tegmental area. Nat Neurosci 14:414-416.
50. Maren S, Fanselow MS (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 15:7548-7564.
51. 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.
52. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, Mi ZP, Lagenaur C, Tretter V, Sieghart W, Anagnostaras SG, Sage JR, Fanselow MS, Guidotti A, Spigelman I, Li Z, DeLorey TM, Olsen RW, Homanics GE (1999) Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor δ subunit knockout mice. Proc Natl Acad Sci U S A 96:12905-12910.
53. Navarro M, Spray KJ, Cubero I, Thiele TE, Bernstein IL (2000) cFos induction during conditioned taste aversion expression varies with aversion strength. Brain Res 887:450-453.
54. Nestler EJ (2005) Is there a common molecular pathway for addiction? Nat Neurosci 8:1445-1449.
55. Nugent FS, Penick EC, Kauer JA (2007) Opioids block long-term potentiation of inhibitory synapses. Nature 446:1086-1090.
56. Nuutinen S, Karlstedt K, Aitta-Aho T, Korpi ER, Panula P (2010) Histamine and H3 receptor-dependent mechanisms regulate ethanol stimulation and conditioned place preference in mice. Psychopharmacology (Berl) 208:75-86.
57. O'Brien CP (2005) Benzodiazepine use, abuse, and dependence. J Clin Psychiatry 66 [Suppl 2]:28-33.
58. A receptor subunit variants in midbrain dopaminergic neurons. J Neurochem 89:7-14.
59. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ, Hughes T, Self DW, Neve RL, Nestler EJ (2005) Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area. J Neurosci 25:5553-5562.
60. Panhelainen AE, Vekovischeva OY, Aitta-Aho T, Rasanen I, Ojanperä I, Korpi ER (2011) Diazepam-induced neuronal plasticity attenuates locomotor responses to morphine and amphetamine challenges in mice. Neuroscience 192:312-321.
61. Parker LA, Limebeer CL, Simpson GR (1998) Chlordiazepoxide-induced conditioned place and taste aversion learning in rats. Pharmacol Biochem Behav 59:33-37.
62. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141-1144.
63. A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
64. Roth T, Lines C, Vandormael K, Ceesay P, Anderson D, Snavely D (2010) Effect of gaboxadol on patient-reported measures of sleep and waking function in patients with primary insomnia: results from two randomized, controlled, 3-month studies. J Clin Sleep Med 6:30-39.
65. 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.
66. A receptors. J Neurochem 105:338-350.
67. 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.
68. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593-1599.
69. A receptor subunits in the basal ganglia and associated limbic brain areas of the adult rat. J Comp Neurol 433:526-549.
70. Spyraki C, Kazandjian A, Varonos D (1985) Diazepam-induced place preference conditioning: appetitive and antiaversive properties. Psychopharmacology (Berl) 87:225-232.
71. A receptors: functional selectivity for extrasynaptic receptors is dependent on the absence of γ2. J Pharmacol Exp Ther 316:1351-1359.
72. Stuber GD, Klanker M, de Ridder B, Bowers MS, Joosten RN, Feenstra MG, Bonci A (2008) Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 321:1690-1692.
73. Tan KR, Brown M, Labouèbe G, Yvon C, Creton C, Fritschy JM, Rudolph U, Lüscher C (2010) Neural bases for addictive properties of benzodiazepines. Nature 463:769-774.
74. Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L, Deisseroth K (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324:1080-1084.
75. 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.
76. Valenti O, Lodge DJ, Grace AA (2011) Aversive stimuli alter ventral tegmental area dopamine neuron activity via a common action in the ventral hippocampus. J Neurosci 31:4280-4289.
77. Vekovischeva OY, Semenova SG, Verbitskaya EV, Zvartau EE (2004) Effects of morphine and cocaine in mice with stable high aggressive and nonaggressive behavioral strategy. Pharmacol Biochem Behav 77:235-243.
78. A agonist, gaboxadol, in a model of transient insomnia: a randomized, controlled clinical trial. Sleep Med 9:393-402.
79. Waszczak BL, Walters JR (1980) Intravenous GABA agonist administration stimulates firing of A10 dopaminergic neurons. Eur J Pharmacol 66:141-144.
80. A receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 23:10650-10661.
81. White FJ (1996) Synaptic regulation of mesocorticolimbic dopamine neurons. Annu Rev Neurosci 19:405-436.
82. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.
83. Wise RA (2008) Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox Res 14:169-183.
84. Wise RA, Bozarth MA (1987) Apsychomotor stimulant theory of addiction. Psychol Med 94:469-492.
85. Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679-720.
86. A receptors facilitate GABAergic transmission to dopaminergic neurons in the ventral tegmental area of young rats. J Physiol 580:731-743.
87. A receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J Neurosci 27:7520-7531.