Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area.
Synaptic plasticity in the ventral tegmental area (VTA) has been implicated in the acquisition of a drug-dependent state. Even a single exposure to cocaine in naive animals is sufficient to trigger sustained changes on VTA glutamatergic synapses that resemble activity-dependent long-term potentiation (LTP) in other brain regions. However, an insight into its time course and mechanisms of action is limited. Here, we show that cocaine acts locally within the VTA to induce an LTP-like enhancement of AMPA receptor-mediated transmission that is not detectable minutes after drug exposure but is fully expressed within 3 h. This cocaine-induced LTP appears to be mediated via dopamine D(5) receptor activation of NMDA receptors and to require protein synthesis. Increased levels of high-conductance GluR1-containing AMPA receptors at synapses are evident at 3 h after cocaine exposure. Furthermore, our data suggest that cocaine-induced LTP might share the same molecular substrates for expression with activity-dependent LTP induced in the VTA by a spike-timing-dependent (STD) protocol, because we observed that STD LTP is significantly reduced or not inducible in VTA neurons previously exposed to cocaine in vivo or in vitro.
Argilli
Emanuela
E
Department of Neurology, Ernest Gallo Clinic and Research Center, University of California, San Francisco, Emeryville, California 94608, USA.
Sibley
David R
DR
Malenka
Robert C
RC
England
Pamela M
PM
Bonci
Antonello
A
D015763:2-Amino-5-phosphonovalerate / Q000494:pharmacology; D000818:Animals; D003042:Cocaine / Q000494:pharmacology*; D003513:Cycloheximide / Q000494:pharmacology; D018492:Dopamine Antagonists / Q000494:pharmacology; D018765:Dopamine Uptake Inhibitors / Q000494:pharmacology*; D004558:Electric Stimulation / Q000379:methods; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D066298:In Vitro Techniques; D017774:Long-Term Potentiation / Q000187:drug effects* / Q000502:physiology; D016202:N-Methylaspartate / Q000494:pharmacology; D009474:Neurons / Q000187:drug effects*; D018408:Patch-Clamp Techniques / Q000379:methods; D011500:Protein Synthesis Inhibitors / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D018091:Receptors, AMPA / Q000502:physiology; D050641:Receptors, Dopamine D5 / Q000502:physiology; D013997:Time Factors; D017557:Ventral Tegmental Area / Q000166:cytology*; D018350:alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid / Q000494:pharmacology
D018492:Dopamine Antagonists; D018765:Dopamine Uptake Inhibitors; D018690:Excitatory Amino Acid Agonists; D018691:Excitatory Amino Acid Antagonists; D011500:Protein Synthesis Inhibitors; D018091:Receptors, AMPA; D050641:Receptors, Dopamine D5; D016202:N-Methylaspartate; D015763:2-Amino-5-phosphonovalerate; D018350:alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid; D003513:Cycloheximide; D003042:Cocaine
Nat Neurosci. 2006 May;9(5):602-4
16582904
Neuron. 2004 Sep 30;44(1):5-21
15450156
J Neurosci. 1984 Dec;4(12):3080-8
6502226
Neurochem Res. 2002 Oct;27(10):1065-77
12462405
Neuron. 2003 Oct 9;40(2):361-79
14556714
Neuron. 2005 Mar 3;45(5):765-79
15748851
J Am Chem Soc. 2007 Apr 25;129(16):4902-3
17391037
Science. 1987 Sep 4;237(4819):1219-23
2820058
Brain Res. 1988 Jun 14;452(1-2):57-65
3401749
J Physiol. 1992 May;450:455-68
1331427
J Pharmacol Toxicol Methods. 1998 Feb;39(1):1-8
9596142
Neuropsychopharmacology. 2004 Dec;29(12):2115-25
15150533
Nat Rev Neurosci. 2007 Oct;8(10):776-89
17848965
Br J Pharmacol. 1990 Apr;99(4):731-5
2361170
Neuron. 2006 Mar 2;49(5):663-70
16504942
Neuron. 2003 Feb 20;37(4):577-82
12597856
J Neurosci. 2002 Dec 15;22(24):10801-10
12486173
J Neurosci. 1995 Jul;15(7 Pt 2):5379-88
7623160
Synapse. 2000 Aug;37(2):125-45
10881034
Science. 1999 Jun 11;284(5421):1811-6
10364548
Neuron. 1995 Nov;15(5):987-90
7576666
J Neurosci. 2007 Apr 25;27(17):4598-602
17460072
Eur J Neurosci. 2004 Aug;20(3):649-57
15255976
Neuroscience. 1995 Apr;65(3):709-30
7609871
J Physiol. 1995 Jul 15;486 ( Pt 2):297-303
7473197
Nat Neurosci. 2005 Nov;8(11):1445-9
16251986
Nat Neurosci. 2006 Apr;9(4):478-80
16531998
Eur J Neurosci. 2007 Aug;26(3):749-56
17686047
Neuron. 2007 Nov 21;56(4):582-92
18031678
J Neurosci. 2004 Aug 25;24(34):7482-90
15329395
Annu Rev Neurosci. 2002;25:103-26
12052905
J Physiol. 2006 Dec 15;577(Pt 3):907-24
16959856
Annu Rev Neurosci. 2001;24:299-325
11283313
Neuroscience. 2004;125(4):879-87
15120849
Science. 2007 Jul 27;317(5837):530-3
17656725
Neuroscience. 2000;100(4):689-99
11036203
Behav Brain Res. 2001 Nov 29;126(1-2):205-9
11704265
Trends Neurosci. 2002 Nov;25(11):578-88
12392933
J Neurosci. 2007 Dec 26;27(52):14275-85
18160635
Curr Opin Pharmacol. 2005 Feb;5(1):20-5
15661621
Cell. 2006 Oct 6;127(1):49-58
17018276
Neuropharmacology. 2007 Jun;52(7):1547-54
17433377
Nature. 2000 May 25;405(6785):454-8
10839540
J Pharmacol Exp Ther. 1996 Jul;278(1):384-92
8764374
J Neurosci. 2007 Dec 12;27(50):13706-18
18077682
Nature. 2005 Oct 13;437(7061):1027-31
16222299
Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2446-50
7708662
J Neurosci. 1996 Apr 1;16(7):2411-20
8601820
Nat Neurosci. 2006 May;9(5):636-41
16582902
Annu Rev Pharmacol Toxicol. 1993;33:639-77
8494354
Nat Rev Neurosci. 2007 Nov;8(11):844-58
17948030
Nature. 2001 May 31;411(6837):583-7
11385572
Synapse. 1997 Feb;25(2):205-14
9021901
J Neurosci. 2006 Aug 16;26(33):8549-58
16914681