mGluRs induce a long-term depression in the ventral tegmental area that involves a switch of the subunit composition of AMPA receptors

European Journal of Neuroscience

Volumn 21, Issue 5, 2005, Pages 1280-1288

  Bellone, Camilla ^a   Lüscher, Christian ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Addiction; Drug abuse; Glutamate receptors; Mesolimbic dopamine system; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 2; JORO SPIDER TOXIN; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; SPIDER VENOM; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN SLICE; DOPAMINERGIC NERVE CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM;

ANIMALS; ANIMALS, NEWBORN; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; INDOLES; LONG-TERM DEPRESSION (PHYSIOLOGY); MALEIMIDES; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PROTEIN SUBUNITS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SPIDER VENOMS; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTAL AREA;

EID: 17144388567     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03979.x     Document Type: Article

References (68)

1. Anwyl, R. (1999) Metabotropic glutamate receptors: electrophysiologicul properties and role in plasticity. Brain Res. Brain Res. Rev., 29, 83-120.
2. Bengtson, O.P., Tozzi, A., Bernardi, G. & Mercuri, N. (2004) Transient receptor potential-like channels mediate metabotropic glutamate receptor EPSCs in rat dopamine neurons. J. Physiol. (Lond.), 555, 323-330.
3. Bowie, D. & Mayer, M.L. (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron, 15, 453-462.
4. Cameron, D.L., Wessendorf M.W. & Williams, J.T. (1997) A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids. Neuroscience, 77, 155-166.
5. Carlezon, W.A. Jr, Boundy, V.A., Hailc, C.N., Lane, S.B., Kalb, R.G., Neve, R.L. & Nestler, E.J. (1997) Sensitization to morphine induced by viral-mediated gene transfer. Science, 277, 812-814.
6. Carlezon, W.A. Jr & Nestler, E.J. (2002) Elevated levels of GluR1 in the midbrain: a trigger for sensilization to drugs of abuse? TINS, 25, 610-615.
7. Chevaleyre, V. & Castillo, P.E. (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocatinabinoids in regulating excitability. Neuron, 38, 461-472.
8. Chiamulera, C., Epping-Jordan, M.P., Zocchi, A., Marcon, C., Colliny, C., Tacconi, S., Corsi, M., Orzi, F. & Conquet, F. (2001) Reinforcing and locomotor stimulant effects of cocaine are absent in mGluR5 null mutant mice. Nature Neurosci., 4, 873-874.
9. Chung, H.J., Steinberg, J.P., Huganir, R.L. & Linden, D.J. (2003) Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science, 300, 1751-1755.
10. Cruz, H.G., Ivanova, T., Lunn, M.L., Stoffel, M., Slesinger, P.A. & Lüscher, C. (2004) Bi-directional effects of GABA(B) receptor agonists on the mesolimbic dopamine system. Nature Neurosci., 7, 153-159.
11. Engelman, H.S., Allen, T.B. & MacDermott, A.B. (1999) The distribution of neurons expressing calcium-permeable AMPA receptors in the superficial laminae of the spinal cord dorsal horn. J. Neurosci., 19, 2081-2089.
12. Faleiro, L.J., Jones, S. & Kauer, J.A. (2004) Rapid synaptic plasticity of glutamatergic synapses on dopamine neurons in the ventral tegmental area in response to acute amphetamine injection. Neuropsychopharm., 29, 2115-2125.
13. Feldmeyer, D., Kask, K., Brusa, R., Kornau, H.C., Kolhekar, R., Rozov, A., Burnashev, N., Jensen, V., Hvalby, O., Sprengel, R. & Seeburg, P.H. (1999) Neurological dysfunctions in mice expressing different levels of the Q/R. site-unedited AMPAR subunit GluR-B. Nature Neurosci., 2, 57-64.
14. Fiorillo, C.D. & Williams, J.T. (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature, 394, 78-82.
15. Fitzgerald, L.W., Ortiz, J., Hamedani, A.C. & Nestler, E.J. (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.
16. Gee, C.E., Benquet, P. & Gerber, U. (2003) Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J. Physiol. (Lond.), 546, 655-664.
17. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron, 15, 193-204.
18. Gerdeman, G.L., Ronesi, J. & Lovinger, D.M. (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nature Neurosci., 5, 446-451.
19. Ghasemzadeh, M.B., Permenter, L.K., Lake, R., Worley, P.F. & Kalivas, P.W. (2003) Homer1 proteins and AMPA receptors modulate cocaine-induced behavioural plasticity. Eur. J. Neurosci., 18, 1645-1651.
20. Gutlerner, J.L., Penick, E.C., Snyder, E.M. & Kauer, J.A. (2002) Novel protein kinase A-dependent long-term depression of excitatory synapses. Neuron, 36, 921-931.
21. Hyman, S.E. & Malenka, R.C. (2001) Addiction and the brain: the neurobiology of compulsion and its persistence. Nature Rev. Neurosci., 2, 695-703.
22. Jia, Z., Agopyan, N., Miu, P., Xiong, Z., Henderson, J., Gerlai, R., Taverna, F.A., Velumian, A., MacDonald, J., Carlen, P., Abramow-Newerly, W. & Roder, J. (1996) Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron, 17, 945-956.
23. Johnson, S.W. & North, R.A. (1992) Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J. Physiol. (Lond.), 450, 455-468.
24. Jones, S., Kornblum, J.L. & Kauer, J.A. (2000) Amphetamine blocks long-term synaptic depression in the ventral tegmental area. J. Neurosci., 20, 5575-5580.
25. 2+-impermeable AMPARs at the maturing parallel fiber-stellate cell synapse. Soc. Neurosci. Abstr., Program no. 276.3
26. Kalivas, P.W., McFarland, K., Bowers, S., Szumlinski, K., Xi, Z.X. & Baker, D. (2003) Glutamate transmission and addiction to cocaine. Ann. N. Y. Acad. Sci., 1003, 169-175.
27. Kalivas, P.W. & Stewart, J. (1991) Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Brain Res. Rev., 16, 223-244.
28. Kamboj, S.K., Swanson, G.T. & Cull-Candy, S.G. (1995) Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J. Physiol. (Lond.), 486, 297-303.
29. Karler, R., Calder, L.D., Chaudhry, I.A. & Turkanis, S.A. (1989) Blockade of 'reverse tolerance' to cocaine and amphetamine by MK-801. Life Sci., 45, 599-606.
30. Kauer, J.A. (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.
31. Kim, S.J., Kim, Y.S., Yuan, J.P., Petralia, R.S., Worley, P.F. & Linden, D.J. (2003) Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature, 426, 285-291.
32. Kim, J.H. & Vezina, P. (1998) Metabotropic glutamate receptors are necessary for sensitization by amphetamine. Neuroreport, 9, 403-406.
33. Koh, D.S., Burnashev, N. & Jonas, P. (1995) Block of native Ca(2+) -permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J. Physiol. (Lond.), 486, 305-312.
34. Laezza, F., Doherty, J.J. & Dingledine, R. (1999) Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science, 285, 1411-1414.
35. Liu, S.Q. & Cull-Candy, S.G. (2000) Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature, 405, 454-458.
36. Lu, W., Monteggia, L.M. & Wolf, M.E. (2002) Repeated administration of amphetamine or cocaine does not alter AMPA receptor subunit expression in the rat midbrain. Neuropsychopharmacology, 26, 1-13.
37. Lüscher, C. & Frerking, M. (2001) Restless AMPA receptors: implications for synaptic transmission and plasticity. TINS, 24, 665-670.
38. Lüscher, C., Nicoll, R.A., Malenka, R.C. & Muller, D. (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nature Neurosci., 3, 545-550.
39. Lüscher, C., Xia, H., Beattie, E.C., Carroll, R.C., von Zastrow, M., Malenka, R.C. & Nicoll, R.A. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron, 24, 649-658.
40. Lüthi, A., Chittajallu, R., Duprat, F., Palmer, M.J., Benke, T.A., Kidd, F.L., Henley, J.M., Isaac, J.T. & Collingridge, G.L. (1999) Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron, 24, 389-399.
41. Magazanik, L.G., Tikhonov, D.B., Bolshakov, K.V., Gmiro, V.E., Buldakova, S.L. & Samoilova, M. V. (2003) Studies of the structure of glutamate receptor ion channels and the mechanisms of their blockade by organic cations. Neurosci. Behav. Physiol., 33, 237-246.
42. Mahanty, N.K. & Sah, P. (1998) Calcium-permeable AMPA receptors mediate long-term potentiation in intemeurons in the amygdala. Nature, 394, 683-687.
43. Mainen, Z.F., Jia, Z., Roder, J. & Malinow, R. (1998) Use-dependent AMPA receptor block in mice lacking GluR2 suggests postsynaptic site for LTP expression. Nature Neurosci., 1, 579-586.
44. McFarland, K. & Kalivas, P.W. (2001) The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci., 21, 8655-8663.
45. Melis, M., Pistis, M., Perra, S., Muntoni, A.L., Pillolla, G. & Gessa, G.L. (2004) Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J. Neurosci., 24, 53-62.
46. Meng, Y., Zhang, Y & Jia, Z. (2003) Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron, 39, 163-176.
47. Morikawa, H., Imani, F., Khodakhah, K. & Williams, J.T. (2000) Inositol 1,4,5-triphosphate-evoked responses in midbrain dopamine neurons. J. Neurosci., 20, RC103.
48. 2+ mobilization in dopamine neurons. J. Neurosci., 23, 149-157.
49. Neuhoff, H., Neu, A., Liss, B. & Roeper, J. (2002) 1(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J. Neurosci., 22, 1290-1302.
50. Oliet, S.H., Malenka, R.C. & Nicoll, R.A. (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron, 18, 969-982.
51. Robbe, D., Kopf, M., Remaury, A., Bockaert, J. & Manzoni, O.J. (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl Acad. Sci. USA, 99, 8384-8388.
52. Robbins, T.W. & Everitt, B.J. (1999) Drug addiction: bad habits add up. Nature, 398, 567-570.
53. Rouach, N. & Nicoll, R.A. (2003) Endocannabinoids contribute to short-term but not long-term mGluR-induced depression in the hippocampus. Eur. J. Neurosci., 18, 1017-1020.
54. Saal, D., Dong, Y., Bonci, A. & Malenka, R.C. (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron, 37, 577-582.
55. Schenk, S. & Snow, S. (1994) Sensitization to cocaine's motor activating properties produced by electrical kindling of the medial prefrontal cortex but not of the hippocampus. Brain Res., 659, 17-22.
56. Schultz, W., Dayan, P. & Montague, P.R. (1997) A neural substrate of prediction and reward. Science, 275, 1593-1599.
57. Self, D.W. (2002) Where's the excitement in psychostimulant sensitization? Newopsychophurmacol., 26, 14-17.
58. Swanson, G.T., Kamboj, S.K. & Cull-Candy, S.G. (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci., 17, 58-69.
59. Szumlinski, K.K., Toda, S., Middaugh, L.D., Worley, P.P. & Kalivas, P.W. (2003) Evidence for a relationship between Group 1 mGluR hypofunction and increased cocaine and ethanol sensitivity in Homer2 null mutant mice. Ann. N.Y. Acad. Sci., 1003, 468-471.
60. Terashima, A., Cotton, L., Dev, K.K., Meyer, G., Zaman, S., Duprat, F., Henley, J.M., Collingridge, G.L. & Isaac, J.T. (2004) Regulation of synaptic strength and AMPA receptor subunit composition by PICK1. J. Neurosci., 24, 5381-5390.
61. Thomas, M.J., Malenka, R.C. & Bonci, A. (2000) Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci., 20, 5581-5586.
62. Tikhonov, D.B., Samoilova, M.V., Buldakova, S.L., Gmiro, V.E. & Magazanik, L.G. (2000) Voltage-dependent block of native AMPA receptor channels by dicationic compounds. Br. J. Pharmacol., 129, 265-274.
63. Tozzi, A., Bengtson, C.P., Longone, P., Carignani, C., Fusco, F.R., Bernardi, G. & Mercuri, N.B. (2003) Involvement of transient receptor potential-like channels in response to mGluR-1 activation in midbrain dopamine neurons. Eur. J. Neurosci., 18, 2133-2145.
64. Ungless, M.A., Whistler, J.L., Malenka, R.C. & Bonci, A. (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature, 411, 583-587.
65. Varma, N., Carlson, G.C., Ledent, C. & Alger, B.E. (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J. Neurosci., 21, RC188.
66. Wilson, R.I. & Nicoll, R.A. (2002) Endocannabinoid signaling in the brain. Science, 296, 678-682.
67. Xia, J., Zhang, X., Staudinger, J. & Huganir, R.L. (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron, 22, 179-187.
68. Xiao, M.Y., Zhou, Q. & Nicoll, R.A. (2001) Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors. Neuropharmacology, 41, 664-671.