Pharmacological evidence of functional inhibitory metabotrophic glutamate receptors on mouse arousal-related cholinergic laterodorsal tegmental neurons

Neuropharmacology

Volumn 66, Issue , 2013, Pages 99-113

  Kohlmeier, Kristi A ^a   Christensen, Mark H ^a   Kristensen, Morten P ^a   Kristiansen, Uffe ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Behavioral state; Drug addiction; In vitro; LDT neurons; REM sleep

Indexed keywords

2 CHLORO 5 HYDROXYPHENYLGLYCINE; 3 [(2 METHYL 4 THIAZOLYL)ETHYNYL]PYRIDINE; 4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; CALCIUM ION; CYCLOPIAZONIC ACID; IBERIOTOXIN; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIDROMIC STIMULATION; AROUSAL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; BRAIN SLICE; CALCIUM CELL LEVEL; CALCIUM CONDUCTANCE; CALCIUM CURRENT; CELL MEMBRANE DEPOLARIZATION; CELL STIMULATION; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOUSE; NERVE CELL; NONHUMAN; POTASSIUM CONDUCTANCE; PREDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSITIVITY ANALYSIS; SLEEP; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM; WAKEFULNESS;

AMINO ACIDS; ANIMALS; ANIMALS, OUTBRED STRAINS; AROUSAL; BICYCLO COMPOUNDS, HETEROCYCLIC; CALCIUM; CHOLINERGIC NEURONS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; MESENCEPHALON; MICE; NEURAL INHIBITION; PEPTIDES; PHENYLACETATES; POTASSIUM CHANNEL BLOCKERS; PYRIDINES; RECEPTORS, METABOTROPIC GLUTAMATE; THIAZOLES;

EID: 84872136117     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.02.016     Document Type: Article

References (97)

1. A. Ahnaou, F.M. Dautzenberg, H. Geys, H. Imogai, A. Gibelin, D. Moechars, T. Steckler, and W.H. Drinkenburg Modulation of group II metabotropic glutamate receptor (mGlu2) elicits common changes in rat and mice sleep-wake architecture Eur. J. Pharmacol. 603 2009 62 72
2. A.M. Batchelor, and J. Garthwaite Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway Nature 385 1997 74 77
3. A. Bond, N.M. Jones, C.A. Hicks, G.M. Whiffin, M.A. Ward, M.F. O'Neill, A.E. Kingston, J.A. Monn, P.L. Ornstein, D.D. Schoepp, D. Lodge, and M.J. O'Neill Neuroprotective effects of LY379268, a selective mGlu2/3 receptor agonist: investigations into possible mechanism of action in vivo J. Pharmacol. Exp. Ther. 294 2000 800 809
4. A. Bond, N. Ragumoorthy, J.A. Monn, C.A. Hicks, M.A. Ward, D. Lodge, and M.J. O'Neill LY379268, a potent and selective Group II metabotropic glutamate receptor agonist, is neuroprotective in gerbil global, but not focal, cerebral ischaemia Neurosci. Lett. 273 1999 191 194
5. S. Boucetta, and B.E. Jones Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-Anesthetized rats J. Neurosci. 29 2009 4664 4674
6. S. Burlet, C.J. Tyler, and C.S. Leonard Direct and indirect excitation of laterodorsal tegmental neurons by hypocretin/orexin peptides: implications for wakefulness and narcolepsy J. Neurosci. 22 2002 2862 2872
7. S. Charpak, and B.H. Gahwiler Glutamate mediates a slow synaptic response in hippocampal slice cultures Proc. Biol. Sci. 243 1991 221 226
8. S. Charpak, B.H. Gahwiler, K.Q. Do, and T. Knopfel Potassium conductances in hippocampal neurons blocked by excitatory amino-Acid transmitters Nature 347 1990 765 767
9. J.R. Clements, D.D. Toth, D.A. Highfield, and S.J. Grant Glutamate-like immunoreactivity is present within cholinergic neurons of the laterodorsal tegmental and pedunculopontine nuclei Adv. Exp. Med. Biol. 295 1991 127 142
10. I. Collado, C. Pedregal, A. Mazon, J.F. Espinosa, J. Blanco-Urgoiti, D.D. Schoepp, R.A. Wright, B.G. Johnson, and A.E. Kingston (2S,1'S,2'S,3'R)-2-(2'- carboxy-3'-methylcyclopropyl) glycine is a potent and selective metabotropic group 2 receptor agonist with anxiolytic properties J. Med. Chem. 45 2002 3619 3629
11. P.J. Conn, C.W. Lindsley, and C.K. Jones Activation of metabotropic glutamate receptors as a novel approach for the treatment of schizophrenia Trends Pharmacol. Sci. 30 2009 25 31
12. P.J. Conn, and J.P. Pin Pharmacology and functions of metabotropic glutamate receptors Annu. Rev. Pharmacol. Toxicol. 37 1997 205 237
13. P. Conti, M. De Amici, H. Brauner-Osborne, U. Madsen, L. Toma, and C. De Micheli Synthesis and pharmacology of 3-hydroxy-delta2-isoxazoline-cyclopentane analogues of glutamic acid Farmaco 57 2002 889 895
14. A. Czarnecki, B. Birtoli, and D. Ulrich Cellular mechanisms of burst firing-mediated long-term depression in rat neocortical pyramidal cells J. Physiol. 578 2007 471 479
15. C.H. Davies, V.R. Clarke, D.E. Jane, and G.L. Collingridge Pharmacology of postsynaptic metabotropic glutamate receptors in rat hippocampal CA1 pyramidal neurons Br. J. Pharmacol. 116 1995 1859 1869
16. A.J. Doherty, M.J. Palmer, J.M. Henley, G.L. Collingridge, and D.E. Jane (RS)-2-chloro-5-hydroxyphenylglycine (CHPG) activates mGlu5, but no mGlu1, receptors expressed in CHO cells and potentiates NMDA responses in the hippocampus Neuropharmacology 36 1997 265 267
17. P. Dutar, and R.A. Nicoll A physiological role for GABAB receptors in the central nervous system Nature 332 1988 156 158
18. P. Dutar, H.M. Vu, and D.J. Perkel Pharmacological characterization of an unusual mGluR-evoked neuronal hyperpolarization mediated by activation of GIRK channels Neuropharmacology 38 1999 467 475
19. S.A. Eaton, D.E. Jane, P.L. Jones, R.H. Porter, P.C. Pook, D.C. Sunter, P.M. Udvarhelyi, P.J. Roberts, T.E. Salt, and J.C. Watkins Competitive antagonism at metabotropic glutamate receptors by (S)-4-carboxyphenylglycine and (RS)-Alpha-methyl-4-carboxyphenylglycine Eur. J. Pharmacol. 244 1993 195 197
20. A.C. Engblom, B.X. Carlson, R.W. Olsen, A. Schousboe, and U. Kristiansen Point mutation in the first transmembrane region of the beta 2 subunit of the gamma-Aminobutyric acid type A receptor alters desensitization kinetics of gamma-Aminobutyric acid- and anesthetic-induced channel gating J. Biol. Chem. 277 2002 17438 17447
21. L. Fagni, J.L. Bossu, and J. Bockaert Activation of a large-conductance Ca2+-dependent K+ channel by stimulation of glutamate phosphoinositide-coupled receptors in cultured cerebellar granule cells Eur. J. Neurosci. 3 1991 778 789
22. I. Feinberg, I.G. Campbell, D.D. Schoepp, and K. Anderson The selective group mGlu2/3 receptor agonist LY379268 suppresses REM sleep and fast EEG in the rat Pharmacol. Biochem. Behav. 73 2002 467 474
23. I. Feinberg, D.D. Schoepp, K.C. Hsieh, N. Darchia, and I.G. Campbell The metabotropic glutamate (mGLU)2/3 receptor antagonist LY341495 [2S-2-Amino-2-(1S,2S-2-carboxycyclopropyl-1-yl)-3-(xanth-9-yl)propanoic acid] stimulates waking and fast electroencephalogram power and blocks the effects of the mGLU2/3 receptor agonist ly379268 [(-)-2-oxa-4-Aminobicyclo[3.1.0]hexane-4, 6-dicarboxylate] in rats J. Pharmacol. Exp. Ther. 312 2005 826 833
24. C.D. Fiorillo, and J.T. Williams Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons Nature 394 1998 78 82
25. B. Ford, C.J. Holmes, L. Mainville, and B.E. Jones GABAergic neurons in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus J. Comp. Neurol. 363 1995 177 196
26. G.L. Forster, and C.D. Blaha Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area Eur. J. Neurosci. 12 2000 3596 3604
27. G.L. Forster, A.J. Falcon, A.D. Miller, G.A. Heruc, and C.D. Blaha Effects of laterodorsal tegmentum excitotoxic lesions on behavioral and dopamine responses evoked by morphine and d-Amphetamine Neuroscience 114 2002 817 823
28. G.L. Forster, J.S. Yeomans, J. Takeuchi, and C.D. Blaha M5 muscarinic receptors are required for prolonged accumbal dopamine release after electrical stimulation of the pons in mice J. Neurosci. 22 2002 RC190
29. S.R. Glaum, and R.J. Miller Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract J. Neurosci. 12 1992 2251 2258
30. A.A. Grace, S.B. Floresco, Y. Goto, and D.J. Lodge Regulation of firing of dopaminergic neurons and control of goal-directed behaviors Trends Neurosci. 30 2007 220 227
31. V.S. Hambrecht-Wiedbusch, E.A. Gauthier, H.A. Baghdoyan, and R. Lydic Benzodiazepine receptor agonists cause drug-specific and state-specific alterations in EEG power and acetylcholine release in rat pontine reticular formation Sleep 33 2010 909 918
32. N. Harata, J. Katayama, Y. Takeshita, Y. Murai, and N. Akaike Two components of metabotropic glutamate responses in acutely dissociated CA3 pyramidal neurons of the rat Brain Res. 711 1996 223 233
33. D.A. Highfield, and S.J. Grant Electrophysiological evidence for an excitatory pathway from medial prefrontal cortex to laterodorsal tegmental nucleus and rostral local coeruleus Soc. Neurosci. Abstr. 15 1989 644
34. A.A. Hirano, and P.R. MacLeish Glutamate and 2-Amino-4-phosphonobutyrate evoke an increase in potassium conductance in retinal bipolar cells Proc. Natl. Acad. Sci. U S A 88 1991 805 809
35. K.H. Holmes, N.B. Keele, V.L. Arvanov, and P. Shinnick-Gallagher Metabotropic glutamate receptor agonist-induced hyperpolarizations in rat basolateral amygdala neurons: receptor characterization and ion channels J. Neurophysiol. 76 1996 3059 3069
36. T. Honda, and K. Semba An ultrastructural study of cholinergic and non-cholinergic neurons in the laterodorsal and pedunculopontine tegmental nuclei in the rat Neuroscience 68 1995 837 853
37. K.B. Hubbard, and J.R. Hepler Cell signalling diversity of the Gqalpha family of heterotrimeric G proteins Cell Signal. 18 2006 135 150
38. H. Imon, K. Ito, L. Dauphin, and R.W. McCarley Electrical stimulation of the cholinergic laterodorsal tegmental nucleus elicits scopolamine-sensitive excitatory postsynaptic potentials in medial pontine reticular formation neurons Neuroscience 74 1996 393 401
39. W.L. Inglis, and K. Semba Colocalization of ionotropic glutamate receptor subunits with NADPH-diaphorase-containing neurons in the rat mesopontine tegmentum J. Comp. Neurol. 368 1996 17 32
40. C. Joly, J. Gomeza, I. Brabet, K. Curry, J. Bockaert, and J.P. Pin Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1 J. Neurosci. 15 1995 3970 3981
41. J. Katayama, N. Akaike, and J. Nabekura Characterization of pre- and post-synaptic metabotropic glutamate receptor-mediated inhibitory responses in substantia nigra dopamine neurons Neurosci. Res. 45 2003 101 115
42. K. Kaupmann, K. Huggel, J. Heid, P.J. Flor, S. Bischoff, S.J. Mickel, G. McMaster, C. Angst, H. Bittiger, W. Froestl, and B. Bettler Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors Nature 386 1997 239 246
43. Y. Kayama, M. Ohta, and E. Jodo Firing of Possibly cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness Brain Res. 569 1992 210 220
44. J.C. Keifer, H.A. Baghdoyan, and R. Lydic Pontine cholinergic mechanisms modulate the cortical electroencephalographic spindles of halothane anesthesia Anesthesiology 84 1996 945 954
45. F. Knoflach, and J.A. Kemp Metabotropic glutamate group II receptors activate a G protein-coupled inwardly rectifying K+ current in neurons of the rat cerebellum J. Physiol. 509 Pt 2 1998 347 354
46. T. Knopfel, R. Kuhn, and H. Allgeier Metabotropic glutamate receptors: novel targets for drug development J. Med. Chem. 38 1995 1417 1426
47. K.A. Kohlmeier, and U. Kristiansen GABAergic actions on cholinergic laterodorsal tegmental neurons: implications for control of behavioral state Neuroscience 171 2010 812 829
48. K.A. Kohlmeier, and C.S. Leonard Transmitter modulation of spike-evoked calcium transients in arousal related neurons: muscarinic inhibition of SNX-482-sensitive calcium influx Eur. J. Neurosci. 23 2006 1151 1162
49. K.A. Kohlmeier, S. Watanabe, C.J. Tyler, S. Burlet, and C.S. Leonard Dual orexin actions on dorsal raphe and laterodorsal tegmentum neurons: noisy cation current activation and selective enhancement of Ca2+ transients mediated by L-type calcium channels J. Neurophysiol. 100 2008 2265 2281
50. K.A. Kohlmeier, J. Wess, M. Bickford, and C.S. Leonard Multiple inhibitory actions mediated by muscarinic M2 and M4 receptors in mesopontine cholinergic neurons Soc. Neurosci. Abstr. 32 2007
51. B. Lancaster, and R.A. Nicoll Properties of two calcium-Activated hyperpolarizations in rat hippocampal neurons J. Physiol. 389 1987 187 203
52. PMt Lea, and A.I. Faden Metabotropic glutamate receptor subtype 5 antagonists MPEP and MTEP CNS Drug Rev. 12 2006 149 166
53. C.S. Leonard, and R. Llinas Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study Neuroscience 59 1994 309 330
54. D.B. Lester, T.D. Rogers, and C.D. Blaha Acetylcholine-dopamine interactions in the pathophysiology and treatment of CNS disorders CNS Neurosci. Ther. 16 2010 137 162
55. L. Littman, L.A. Chase, M. Renzi, A.B. Garlin, J.F. Koerner, R.L. Johnson, and M.B. Robinson Effects of quisqualic acid analogs on metabotropic glutamate receptors coupled to phosphoinositide hydrolysis in rat hippocampus Neuropharmacology 34 1995 829 841
56. D.J. Lodge, and A.A. Grace The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons Proc. Natl. Acad. Sci. U S A 103 2006 5167 5172
57. J.I. Luebke, R.W. Greene, K. Semba, A. Kamondi, R.W. McCarley, and P.B. Reiner Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro Proc. Natl. Acad. Sci. U S A 89 1992 743 747
58. J.I. Luebke, R.W. McCarley, and R.W. Greene Inhibitory action of muscarinic agonists on neurons in the rat laterodorsal tegmental nucleus in vitro J. Neurophysiol. 70 1993 2128 2135
59. R. Lydic, and H.A. Baghdoyan Ketamine and MK-801 decrease acetylcholine release in the pontine reticular formation, slow breathing, and disrupt sleep Sleep 25 2002 617 622
60. R. Lydic, and H.A. Baghdoyan Sleep, anesthesiology, and the neurobiology of arousal state control Anesthesiology 103 2005 1268 1295
61. M. Mameli-Engvall, A. Evrard, S. Pons, U. Maskos, T.H. Svensson, J.P. Changeux, and P. Faure Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors Neuron 50 2006 911 921
62. S. Mortazavi, J. Thompson, H.A. Baghdoyan, and R. Lydic Fentanyl and morphine, but not remifentanil, inhibit acetylcholine release in pontine regions modulating arousal Anesthesiology 90 1999 1070 1077
63. S. Nakanishi Molecular diversity of glutamate receptors and implications for brain function Science 258 1992 597 603
64. S. Nakanishi Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity Neuron 13 1994 1031 1037
65. H. Naruo, S. Onizuka, D. Prince, M. Takasaki, and N.I. Syed Sevoflurane blocks cholinergic synaptic transmission postsynaptically but does not affect short-term potentiation Anesthesiology 102 2005 920 928
66. E. Neher Correction for liquid junction potentials in patch clamp experiments Methods Enzymol. 207 1992 123 131
67. N.R. Newberry, and R.A. Nicoll Comparison of the action of baclofen with gamma-Aminobutyric acid on rat hippocampal pyramidal cells in vitro J. Physiol. 360 1985 161 185
68. Z. Nusser Subcellular distribution of neurotransmitter receptors and voltage-gated ion channels G. Stuart, N. Spruston, M. Hausser, Dendrites 1999 Oxford University Press Oxford 85 113
69. N. Omelchenko, and S.R. Sesack Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area J. Comp. Neurol. 483 2005 217 235
70. N. Omelchenko, and S.R. Sesack Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons J. Comp. Neurol. 494 2006 863 875
71. J.P. Pin, and R. Duvoisin The metabotropic glutamate receptors: structure and functions Neuropharmacology 34 1995 1 26
72. R.H. Porter, P.J. Roberts, D.E. Jane, and J.C. Watkins (S)-homoquisqualate: a potent agonist at the glutamate metabotropic receptor Br. J. Pharmacol. 106 1992 509 510
73. D.G. Rainnie, K.H. Holmes, and P. Shinnick-Gallagher Activation of postsynaptic metabotropic glutamate receptors by trans-ACPD hyperpolarizes neurons of the basolateral amygdala J. Neurosci. 14 1994 7208 7220
74. T.E. Salt, and J.P. Turner Reduction of sensory and metabotropic glutamate receptor responses in the thalamus by the novel metabotropic glutamate receptor-1-selective antagonist S-2-methyl-4-carboxy-phenylglycine Neuroscience 85 1998 655 658
75. R. Sanchez, and C.S. Leonard NMDA-receptor-mediated synaptic currents in guinea pig laterodorsal tegmental neurons in vitro J. Neurophysiol. 76 1996 1101 1111
76. R.M. Sanchez, A. Surkis, and C.S. Leonard Voltage-clamp analysis and computer simulation of a novel cesium-resistant A-current in guinea pig laterodorsal tegmental neurons J. Neurophysiol. 79 1998 3111 3126
77. J.A. Saugstad, T.P. Segerson, and G.L. Westbrook Metabotropic glutamate receptors activate G-protein-coupled inwardly rectifying potassium channels in Xenopus oocytes J. Neurosci. 16 1996 5979 5985
78. D.D. Schoepp, and P.J. Conn Metabotropic glutamate receptors in brain function and pathology Trends Pharmacol. Sci. 14 1993 13 20
79. D.D. Schoepp, J. Goldsworthy, B.G. Johnson, C.R. Salhoff, and S.R. Baker 3,5-dihydroxyphenylglycine is a highly selective agonist for phosphoinositide-linked metabotropic glutamate receptors in the rat hippocampus J. Neurochem. 63 1994 769 772
80. M.K. Schulte, R.J. Roon, D.J. Chalmers, D.C. Sunter, and J.F. Koerner Utilization of the resolved L-isomer of 2-Amino-6-phosphonohexanoic acid (L-AP6) as a selective agonist for a quisqualate-sensitized site in hippocampal CA1 pyramidal neurons Brain Res. 649 1994 203 207
81. W. Schultz Getting formal with dopamine and reward Neuron 36 2002 241 263
82. N. Sekiyama, Y. Hayashi, S. Nakanishi, D.E. Jane, H.W. Tse, E.F. Birse, and J.C. Watkins Structure-Activity relationships of new agonists and antagonists of different metabotropic glutamate receptor subtypes Br. J. Pharmacol. 117 1996 1493 1503
83. K. Semba, and H.C. Fibiger Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study J. Comp. Neurol. 323 1992 387 410
84. S.R. Sesack, A.Y. Deutch, R.H. Roth, and B.S. Bunney Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J. Comp. Neurol. 290 1989 213 242
85. D. Sharon, D. Vorobiov, and N. Dascal Positive and negative coupling of the metabotropic glutamate receptors to a G protein-Activated K+ channel, GIRK, in Xenopus oocytes J. Gen. Physiol. 109 1997 477 490
86. T. Shirasaki, N. Harata, and N. Akaike Metabotropic glutamate response in acutely dissociated hippocampal CA1 pyramidal neurons of the rat J. Physiol. 475 1994 439 453
87. M.M. Slaughter, and R.F. Miller 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research Science 211 1981 182 185
88. C. Staub, I. Vranesic, and T. Knopfel Responses to metabotropic glutamate receptor activation in cerebellar Purkinje cells: induction of an inward current Eur. J. Neurosci. 4 1992 832 839
89. A. Stefani, A. Pisani, N.B. Mercuri, and P. Calabresi The modulation of calcium currents by the activation of mGluRs. Functional implications Mol. Neurobiol. 13 1996 81 95
90. M. Steriade, and R. McCarley Brainstem Control of Wakefulness and Sleep 2005 Plenum Plenum
91. D.R. Stevens, R.W. McCarley, and R.W. Greene Excitatory amino acid-mediated responses and synaptic potentials in medial pontine reticular formation neurons of the rat in vitro J. Neurosci. 12 1992 4188 4194
92. S.R. Vincent, K. Satoh, D.M. Armstrong, and H.C. Fibiger NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation Neurosci. Lett. 43 1983 31 36
93. I. Vranesic, C. Staub, and T. Knopfel Activation of metabotropic glutamate receptors induces an outward current which is potentiated by methylxanthines in rat cerebellar Purkinje cells Neurosci. Res. 16 1993 209 215
94. H.L. Wang, and M. Morales Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat Eur. J. Neurosci. 29 2009 340 358
95. J. Watkins, and G. Collingridge Phenylglycine derivatives as antagonists of metabotropic glutamate receptors Trends Pharmacol. Sci. 15 1994 333 342
96. K. Wisniewski, and H. Car (S)-3,5-DHPG: a review CNS Drug Rev. 8 2002 101 116
97. J. Yeomans, G. Forster, and C. Blaha M5 muscarinic receptors are needed for slow activation of dopamine neurons and for rewarding brain stimulation Life Sci. 68 2001 2449 2456