Activation of group II metabotropic glutamate receptors inhibits the discriminative stimulus effects of alcohol via selective activity within the amygdala

Neuropsychopharmacology

Volumn 36, Issue 11, 2011, Pages 2328-2338

  Cannady, Reginald ^a,b   Grondin, Julie J M ^a   Fisher, Kristen R ^a   Hodge, Clyde W ^a,b   Besheer, Joyce ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

amygdala; discriminative stimulus; Drug discrimination; ethanol; glutamate; mGluR2 3

Indexed keywords

4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; ALCOHOL; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR AGONIST; PROTEIN C FOS; WATER;

ALCOHOLISM; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DATA ANALYSIS; DISCRIMINATIVE STIMULUS; IMMUNOREACTIVITY; MALE; MEDICAL RECORD; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

AMINO ACIDS; AMYGDALA; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; DISCRIMINATION LEARNING; ETHANOL; MALE; MOTOR ACTIVITY; RATS; RATS, LONG-EVANS; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 80052766574     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.121     Document Type: Article

References (83)

1. Adewale AS, Platt DM, Spealman RD (2006). Pharmacological stimulation of group ii metabotropic glutamate receptors reduces cocaine self-administration and cocaine-induced reinstatement of drug seeking in squirrel monkeys. J Pharmacol Exp Ther 318: 922-931. (Pubitemid 44061269)
2. Ator NA, Grant KA, Purdy RH, Paul SM, Griffiths RR (1993). Drug discrimination analysis of endogenous neuroactive steroids in rats. Eur J Pharmacol 241: 237-243. (Pubitemid 23272885)
3. Backstrom P, Hyytia P (2005). Suppression of alcohol self-administration and cue-induced reinstatement of alcohol seeking by the mGlu2/3 receptor agonist LY379268 and the mGlu8 receptor agonist (S)-3,4-DCPG. Eur J Pharmacol 528: 110-118. (Pubitemid 41773660)
4. Baptista MA, Martin-Fardon R, Weiss F (2004). Preferential effects of the metabotropic glutamate 2/3 receptor agonist LY379268 on conditioned reinstatement versus primary reinforcement: comparison between cocaine and a potent conventional reinforcer. J Neurosci 24: 4723-4727. (Pubitemid 38668196)
5. Baskys A, Malenka RC (1991). Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J Physiol 444: 687-701.
6. Besheer J, Cox AA, Hodge CW (2003). Coregulation of ethanol discrimination by the nucleus accumbens and amygdala. Alcohol Clin Exp Res 27: 450-456. (Pubitemid 36343289)
7. Besheer J, Grondin JJ, Cannady R, Sharko AC, Faccidomo S, Hodge CW (2010). Metabotropic glutamate receptor 5 activity in the nucleus accumbens is required for the maintenance of ethanol self-administration in a rat genetic model of high alcohol intake. Biol Psychiatry 67: 812-822.
8. Besheer J, Grondin JJ, Salling MC, Spanos M, Stevenson RA, Hodge CW (2009). Interoceptive effects of alcohol require mGlu5 receptor activity in the nucleus accumbens. J Neurosci 29: 9582-9591.
9. Besheer J, Hodge CW (2005). Pharmacological and anatomical evidence for an interaction between mGluR5-and GABA(A) alpha1-containing receptors in the discriminative stimulus effects of ethanol. Neuropsychopharmacology 30: 747-757. (Pubitemid 40397081)
10. Besheer J, Schroeder JP, Stevenson RA, Hodge CW (2008). Ethanol-induced alterations of c-Fos immunoreactivity in specific limbic brain regions following ethanol discrimination training. Brain Res 1232: 124-131.
11. Bienkowski P, Iwinska K, Stefanski R, Kostowski W (1997). Discriminative stimulus properties of ethanol in the rat: differential effects of selective and nonselective benzodia-zepine receptor agonists. Pharmacol Biochem Behav 58: 969-973. (Pubitemid 28108204)
12. Bossert JM, Gray SM, Lu L, Shaham Y (2006). Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking. Neuropsychopharmacology 31: 2197-2209. (Pubitemid 44413197)
13. Cartmell J, Monn JA, Schoepp DD (2000). Tolerance to the motor impairment, but not to the reversal of PCP-induced motor activities by oral administration of the mGlu2/3 receptor agonist, LY379268. Naunyn Schmiedebergs Arch Pharmacol 361: 39-46. (Pubitemid 30064652)
14. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340: 474-476. (Pubitemid 19191284)
15. Criswell HE, Ming Z, Griffith BL, Breese GR (2003). Comparison of effect of ethanol on N-methyl-D-aspartate-and GABA-gated currents from acutely dissociated neurons: absence of regional differences in sensitivity to ethanol. J Pharmacol Exp Ther 304: 192-199. (Pubitemid 36008928)
16. Dildy JE, Leslie SW (1989). Ethanol inhibits NMDA-induced increases in free intracellular Ca2+ in dissociated brain cells. Brain Res 499: 383-387. (Pubitemid 19244834)
17. Farazifard R, Wu SH (2010). Metabotropic glutamate receptors modulate glutamatergic and GABAergic synaptic transmission in the central nucleus of the inferior colliculus. Brain Res 1325: 28-40.
18. Fell MJ, Perry KW, Falcone JF, Johnson BG, Barth VN, Rash KS et al (2009). In vitro and in vivo evidence for a lack of interaction with dopamine D2 receptors by the metabotropic glutamate 2/3 receptor agonists 1S,2S,5R,6S-2-aminobicyclo[3.1.0]hexane-2,6-bicaroxylate monohydrate (LY354740) and (-)-2-oxa-4-aminobicyclo[3.1.0] Hexane-4,6-dicarboxylic acid (LY379268). J Pharmacol Exp Ther 331: 1126-1136.
19. Ferraguti F, Shigemoto R (2006). Metabotropic glutamate receptors. Cell Tissue Res 326: 483-504. (Pubitemid 44435821)
20. Gallagher M, Holland PC (1994). The amygdala complex: multiple roles in associative learning and attention. Proc Natl Acad Sci USA 91: 11771-11776. (Pubitemid 24368545)
21. Grant KA (1999). Strategies for understanding the pharmacological effects of ethanol with drug discrimination procedures. Pharmacol Biochem Behav 64: 261-267. (Pubitemid 29438610)
22. Grant KA, Colombo G (1993). Discriminative stimulus effects of ethanol: effect of training dose on the substitution of N-methyl-D-aspartate antagonists. J Pharmacol Exp Ther 264: 1241-1247. (Pubitemid 23318617)
23. Grant KA, Waters CA, Green-Jordan K, Azarov A, Szeliga KT (2000). Characterization of the discriminative stimulus effects of GABA(A) receptor ligands in Macaca fascicularis monkeys under different ethanol training conditions. Psychopharmacology (Berl) 152: 181-188.
24. Hao Y, Martin-Fardon R, Weiss F (2010). Behavioral and functional evidence of metabotropic glutamate receptor 2/3 and metabotropic glutamate receptor 5 dysregulation in cocaine-escalated rats: factor in the transition to dependence. Biol Psychiatry 68: 240-248.
25. Hasin DS, Goodwin RD, Stinson FS, Grant BF (2005). Epidemiology of major depressive disorder: results from the National Epidemiologic Survey on Alcoholism and Related Conditions. Arch Gen Psychiatry 62: 1097-1106. (Pubitemid 41396935)
26. Heidbreder CA, Hagan JJ (2005). Novel pharmacotherapeutic approaches for the treatment of drug addiction and craving. Curr Opin Pharmacol 5: 107-118. (Pubitemid 40124543)
27. Helms CM, Rogers LS, Grant KA (2009). Antagonism of the ethanol-like discriminative stimulus effects of ethanol, pento-barbital, and midazolam in cynomolgus monkeys reveals involvement of specific GABA(A) receptor subtypes. J Pharmacol Exp Ther 331: 142-152.
28. Hiltunen AJ, Jarbe TU (1989). Discriminative stimulus properties of ethanol: effects of cumulative dosing and Ro 15-4513. Behav Pharmacol 1: 133-140.
29. Hodge CW, Aiken AS (1996). Discriminative stimulus function of ethanol: role of GABAA receptors in the nucleus accumbens. Alcohol Clin Exp Res 20: 1221-1228. (Pubitemid 26357025)
30. Hodge CW, Cox AA (1998). The discriminative stimulus effects of ethanol are mediated by NMDA and GABA(A) receptors in specific limbic brain regions. Psychopharmacology (Berl) 139: 95-107. (Pubitemid 28416887)
31. Hodge CW, Cox AA, Bratt AM, Camarini R, Iller K, Kelley SP et al (2001). The discriminative stimulus properties of self-administered ethanol are mediated by GABA(A) and NMDA receptors in rats. Psychopharmacology (Berl) 154: 13-22. (Pubitemid 32186510)
32. Hundt W, Danysz W, Holter SM, Spanagel R (1998). Ethanol and N-methyl-D-aspartate receptor complex interactions: a detailed drug discrimination study in the rat. Psychopharmacology (Berl) 135: 44-51. (Pubitemid 28055449)
33. Imre G (2007). The preclinical properties of a novel group II metabotropic glutamate receptor agonist LY379268. CNS Drug Rev 13: 444-464. (Pubitemid 350233471)
34. Jarbe TU, McMillan DE (1983). Interaction of the discriminative stimulus properties of diazepam and ethanol in pigeons. Pharmacol Biochem Behav 18: 73-80. (Pubitemid 13224587)
35. Jin X, Semenova S, Yang L, Ardecky R, Sheffler DJ, Dahl R et al (2010). The mGluR2 positive allosteric modulator BINA decreases cocaine self-administration and cue-induced cocaine-seeking and counteracts cocaine-induced enhancement of brain reward function in rats. Neuropsychopharmacology 35: 2021-2036.
36. Kaatz KW, Albin RL (1995). Intrastriatal and intrasubthalamic stimulation of metabotropic glutamate receptors: a behavioral and Fos immunohistochemical study. Neuroscience 66: 55-65.
37. Kearney JA, Frey KA, Albin RL (1997). Metabotropic glutamate agonist-induced rotation: a pharmacological, FOS immunohis-tochemical, and [14C]-2-deoxyglucose autoradiographic study. J Neurosci 17: 4415-4425. (Pubitemid 27220632)
38. Kenny PJ, Markou A (2004). The ups and downs of addiction: role of metabotropic glutamate receptors. Trends Pharmacol Sci 25: 265-272. (Pubitemid 38553829)
39. Kostowski W, Bienkowski P (1999). Discriminative stimulus effects of ethanol: neuropharmacological characterization. Alcohol 17: 63-80. (Pubitemid 29225855)
40. LeDoux J (2003). The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23: 727-738.
41. Liechti ME, Lhuillier L, Kaupmann K, Markou A (2007). Metabotropic glutamate 2/3 receptors in the ventral tegmental area and the nucleus accumbens shell are involved in behaviors relating to nicotine dependence. J Neurosci 27: 9077-9085. (Pubitemid 47312061)
42. Liu YB, Disterhoft JF, Slater NT (1993). Activation of meta-botropic glutamate receptors induces long-term depression of GABAergic inhibition in hippocampus. J Neurophysiol 69: 1000-1004. (Pubitemid 23102969)
43. Lu L, Uejima JL, Gray SM, Bossert JM, Shaham Y (2007). Systemic and central amygdala injections of the mGluR(2/3) agonist LY379268 attenuate the expression of incubation of cocaine craving. Biol Psychiatry 61: 591-598. (Pubitemid 46343539)
44. Macek TA, Winder DG, Gereau RWt, Ladd CO, Conn PJ (1996). Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol 76: 3798-3806. (Pubitemid 27009683)
45. Majewska MD (1988). Interaction of ethanol with the GABAA receptor in the rat brain: possible involvement of endogenous steroids. Alcohol 5: 269-273. (Pubitemid 19263829)
46. Marek GJ, Wright RA, Schoepp DD, Monn JA, Aghajanian GK (2000). Physiological antagonism between 5-hydroxytrypt-amine(2A) and group II metabotropic glutamate receptors in prefrontal cortex. J Pharmacol Exp Ther 292: 76-87. (Pubitemid 30026356)
47. Maren S (2005). Synaptic mechanisms of associative memory in the amygdala. Neuron 47: 783-786. (Pubitemid 41266945)
48. Mogenson GJ, Swanson LW, Wu M (1983). Neural projections from nucleus accumbens to globus pallidus, substantia innomi-nata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat. J Neurosci 3: 189-202. (Pubitemid 13193402)
49. Morgan JI, Cohen DR, Hempstead JL, Curran T (1987). Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237: 192-197.
50. Molinaro G, Traficante A, Riozzi B, Di Menna L, Curto M, Pallottino S et al (2009). Activation of mGlu2/3 metabotropic glutamate receptors negatively regulates the stimulation of inositol phospholipid hydrolysis mediated by 5-hydroxytrypta-mine2A serotonin receptors in the frontal cortex of living mice. Mol Pharmacol 76: 379-387.
51. Monn JA, Valli MJ, Massey SM, Hansen MM, Kress TJ, Wepsiec JP et al (1999). Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related to (+)-2-aminobicyclo[3.1.0] hexane-2,6-dicarboxylic acid (LY354740): identification of two new potent, selective, and systemically active agonists for group II metabotropic glutamate receptors. J Med Chem 42: 1027-1040.
52. Ohishi H, Neki A, Mizuno N (1998). Distribution of a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat and mouse: an immunohistochemical study with a monoclonal antibody. Neurosci Res 30: 65-82. (Pubitemid 28119150)
53. Olive MF, Mehmert KK, Nannini MA, Camarini R, Messing RO, Hodge CW (2001). Reduced ethanol withdrawal severity and altered withdrawal-induced c-fos expression in various brain regions of mice lacking protein kinase C-epsilon. Neuroscience 103: 171-179. (Pubitemid 32304357)
54. Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV et al (2007). Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat Med 13: 1102-1107. (Pubitemid 47517511)
55. Paxinos G, Waton C (eds) (1998). The Rat Brain in Stereotaxic Coordinates. Academic Press: London.
56. Perez de la Mora M, Lara-Garcia D, Jacobsen KX, Vazquez-Garcia M, Crespo-Ramirez M, Flores-Gracia C et al (2006). Anxiolytic-like effects of the selective metabotropic glutamate receptor 5 antagonist MPEP after its intra-amygdaloid microinjection in three different non-conditioned rat models of anxiety. Eur J Neurosci 23: 2749-2759. (Pubitemid 43801467)
57. Peters J, Kalivas PW (2006). The group II metabotropic glutamate receptor agonist, LY379268, inhibits both cocaine-and food-seeking behavior in rats. Psychopharmacology (Berl) 186: 143-149. (Pubitemid 43727330)
58. Petralia RS, Wang YX, Niedzielski AS, Wenthold RJ (1996). The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neu-roscience 71: 949-976. (Pubitemid 26090013)
59. Pinheiro PS, Mulle C (2008). Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9: 423-436.
60. Rodd ZA, McKinzie DL, Bell RL, McQueen VK, Murphy JM, Schoepp DD et al (2006). The metabotropic glutamate 2/3 receptor agonist LY404039 reduces alcohol-seeking but not alcohol self-administration in alcohol-preferring (P) rats. Behav Brain Res 171: 207-215. (Pubitemid 43946492)
61. Sapp DW, Yeh HH (1998). Ethanol-GABAA receptor interactions: a comparison between cell lines and cerebellar Purkinje cells. J Pharmacol Exp Ther 284: 768-776. (Pubitemid 28086670)
62. Schechter MD, Meehan SM, Gordon TL, McBurney DM (1993). The NMDA receptor antagonist MK-801 produces ethanol-like discrimination in the rat. Alcohol 10: 197-201. (Pubitemid 23145454)
63. Schoepp DD (2001). Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J Pharmacol Exp Ther 299: 12-20. (Pubitemid 32905113)
64. Schroeder JP, Spanos M, Stevenson JR, Besheer J, Salling M, Hodge CW (2008). Cue-induced reinstatement of alcohol-seeking behavior is associated with increased ERK1/2 phosphor-ylation in specific limbic brain regions: blockade by the mGluR5 antagonist MPEP. Neuropharmacology 55: 546-554.
65. Schuckit MA, Hesselbrock V (1994). Alcohol dependence and anxiety disorders: what is the relationship? Am J Psychiatry 151: 1723-1734. (Pubitemid 24370891)
66. See RE, Fuchs RA, Ledford CC, McLaughlin J (2003). Drug addiction, relapse, and the amygdala. Ann NY Acad Sci 985: 294-307. (Pubitemid 36521122)
67. Seeman P, Guan HC (2008). Phencyclidine and glutamate agonist LY379268 stimulate dopamine D2High receptors: D2 basis for schizophrenia. Synapse 62: 819-828.
68. Shelton KL (2004). Substitution profiles of N-methyl-D-aspartate antagonists in ethanol-discriminating inbred mice. Alcohol 34: 165-175. (Pubitemid 40292774)
69. Shelton KL, Grant KA (2002). Discriminative stimulus effects of ethanol in C57BL/6J and DBA/2J inbred mice. Alcohol Clin Exp Res 26: 747-757. (Pubitemid 34666132)
70. Sidhpura N, Weiss F, Martin-Fardon R (2010). Effects of the mGlu2/3 agonist LY379268 and the mGlu5 antagonist MTEP on ethanol seeking and reinforcement are differentially altered in rats with a history of ethanol dependence. Biol Psychiatry 67: 804-811.
71. Stolerman I (1992). Drugs of abuse: behavioural principles, methods and terms. Trends Pharmacol Sci 13: 170-176.
72. Swanson CJ, Bures M, Johnson MP, Linden AM, Monn JA, Schoepp DD (2005). Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nat Rev Drug Discov 4: 131-144. (Pubitemid 40277494)
73. Theberge FR, Milton AL, Belin D, Lee JL, Everitt BJ (2010). The basolateral amygdala and nucleus accumbens core mediate dissociable aspects of drug memory reconsolidation. Learn Mem 17: 444-453.
74. Uejima JL, Bossert JM, Poles GC, Lu L (2007). Systemic and central amygdala injections of the mGluR2/3 agonist LY379268 attenuate the expression of incubation of sucrose craving in rats. Behav Brain Res 181: 292-296. (Pubitemid 46908754)
75. Vengeliene V, Bilbao A, Molander A, Spanagel R (2008). Neuro-pharmacology of alcohol addiction. Br J Pharmacol 154: 299-315.
76. Vivian JA, Waters CA, Szeliga KT, Jordan K, Grant KA (2002). Characterization of the discriminative stimulus effects of N-methyl-D-aspartate ligands under different ethanol training conditions in the cynomolgus monkey (Macaca fascicularis). Psychopharmacology (Berl) 162: 273-281. (Pubitemid 34762286)
77. Weight FF, Lovinger DM, White G (1991). Alcohol inhibition of NMDA channel function. Alcohol Alcohol Suppl 1: 163-169.
78. Winter JC, Eckler JR, Rabin RA (2004). Serotonergic/glutamatergic interactions: the effects of mGlu2/3 receptor ligands in rats trained with LSD and PCP as discriminative stimuli. Psycho-pharmacology (Berl) 172: 233-240. (Pubitemid 38388775)
79. Wise RA, Wang B, You ZB (2008). Cocaine serves as a peripheral interoceptive conditioned stimulus for central glutamate and dopamine release. PLoS ONE 3: e2846.
80. Yasuhara A, Chaki S (2010). Metabotropic glutamate receptors: potential drug targets for psychiatric disorders. Open Med Chem J 4: 20-36.
81. Zhao Y, Dayas CV, Aujla H, Baptista MA, Martin-Fardon R, Weiss F (2006). Activation of group II metabotropic glutamate receptors attenuates both stress and cue-induced ethanol-seeking and modulates c-fos expression in the hippocampus and amygdala. J Neurosci 26: 9967-9974. (Pubitemid 44477158)
82. Zimmerman JM, Rabinak CA, McLachlan IG, Maren S (2007). The central nucleus of the amygdala is essential for acquiring and expressing conditional fear after overtraining. Learn Mem 14: 634-644. (Pubitemid 47481697)
83. Zysk JR, Widzowski D, Sygowski LA, Knappenberger KS, Spear N, Elmore CS et al (2011). Absence of direct effects on the dopamine D2 receptor by mGluR2/3-selective receptor agonists LY 354 740 and LY 379 268. Synapse 65: 64-68.