A silent synapse-based mechanism for cocaine-induced locomotor sensitization

Journal of Neuroscience

Volumn 31, Issue 22, 2011, Pages 8163-8174

  Brown, Travis E ^a   Lee, Brian R ^a   Mu, Ping ^a   Ferguson, Deveroux ^b   Dietz, David ^b   Ohnishi, Yoshinori N ^b   Lin, Ying ^c   Suska, Anna ^d,e   Ishikawa, Masago ^a   Huang, Yanhua H ^a   Shen, Haowei ^f   Kalivas, Peter W ^f   Sorg, Barbara A ^a   Suzanne Zukin, R ^c   Nestler, Eric J ^b   Dong, Yan ^a   Schlüüter, Oliver M ^d,e  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

^f MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PROTEIN; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; RO 256981; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DRUG EXPOSURE; DRUG MECHANISM; ENZYME INHIBITION; GENETIC MANIPULATION; GENETIC TRANSCRIPTION; IN VIVO STUDY; LOCOMOTION; MALE; MOLECULAR DYNAMICS; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SENSITIZATION; SILENT SYNAPSE; SYNAPSE; SYNAPTIC POTENTIAL; TRANSCRIPTION INITIATION;

ANIMALS; COCAINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DENDRITIC SPINES; GENE EXPRESSION REGULATION; GENETIC VECTORS; MALE; MICROINJECTIONS; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; PATCH-CLAMP TECHNIQUES; PHENOLS; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SINDBIS VIRUS; SYNAPSES;

EID: 79958056044     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0016-11.2011     Document Type: Article

References (81)

1. Andersen SL, Arvanitogiannis A, Pliakas AM, LeBlanc C, Carlezon WA Jr (2002) Altered responsiveness to cocaine in rats exposed to methylphenidate during development. Nat Neurosci 5:13-14.
2. Anderson SM, Famous KR, Sadri-Vakili G, Kumaresan V, Schmidt HD, Bass CE, Terwilliger EF, Cha JH, Pierce RC (2008) CaMKII: a biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking. Nat Neurosci 11:344-353.
3. Apicella P, Scarnati E, Ljungberg T, Schultz W (1992) Neuronal activity in monkey striatum related to the expectation of predictable environmental events. J Neurophysiol 68:945-960.
4. Barria A, Malinow R (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48:289-301.
5. Brami-Cherrier K, Valjent E, Hervé D, Darragh J, Corvol JC, Pages C, Arthur SJ, Simon AJ, Girault JA, Caboche J (2005) Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J Neurosci 25:11444-11454.
6. Burns LH, Everitt BJ, Kelley AE, Robbins TW (1994) Glutamate-dopamine interactions in the ventral striatum: role in locomotor activity and responding with conditioned reinforcement. Psychopharmacology (Berl) 115:516-528.
7. Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436-445.
8. Cull-Candy SG, Leszkiewicz DN (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004:re16.
9. David HN, Sissaoui K, Abraini JH (2004) Modulation of the locomotor responses induced by D1-like and D2-like dopamine receptor agonists and D-amphetamine byNMDAand non-NMDA glutamate receptor agonists and antagonists in the core of the rat nucleus accumbens. Neuropharmacology 46:179-191.
10. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
11. Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC (2006) CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9:475-477.
12. Durand GM, Kovalchuk Y, Konnerth A (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381:71-75.
13. 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.
14. Groc L, Gustafsson B, Hanse E (2006) AMPA signalling in nascent glutamatergic synapses: there and not there! Trends Neurosci 29:132-139.
15. Hooks MS, Jones GH, Hemby SE, Justice JB Jr (1993) Environmental and pharmacological sensitization: effects of repeated administration of systemic or intra-nucleus accumbens cocaine. Psychopharmacology (Berl) 111:109-116.
16. Hsia AY, Malenka RC, Nicoll RA (1998) Development of excitatory circuitry in the hippocampus. J Neurophysiol 79:2013-2024.
17. Huang YH, Lin Y, Brown TE, Han MH, Saal DB, Neve RL, Zukin RS, Sorg BA, Nestler EJ, Malenka RC, Dong Y (2007) CREB modulates the functional output of nucleus accumbens neurons: a critical role of N-methyl-Daspartate glutamate (NMDA) receptors. J Biol Chem 283:2751-2760 [Erratum 283:11860].
18. Huang YH, Lin Y, Mu P, Lee BR, Brown TE, Wayman G, Marie H, Liu W, Yan Z, Sorg BA, Schlüter OM, Zukin RS, Dong Y (2009) In vivo cocaine experience generates silent synapses. Neuron 63:40-47.
19. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565-598.
20. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
21. Isaac JT, Nicoll RA, Malenka RC (1999) Silent glutamatergic synapses in the mammalian brain. Can J Physiol Pharmacol 77:735-737.
22. Kaddis FG, Wallace LJ, Uretsky NJ (1993) AMPA/kainate antagonists in the nucleus accumbens inhibit locomotor stimulatory response to cocaine and dopamine agonists. Pharmacol Biochem Behav 46:703-708.
23. Kafetzopoulos E (1986) Effects of amphetamine and apomorphine on locomotor activity after kainic acid lesion of the nucleus accumbens septi in the rat. Psychopharmacology (Berl) 88:271-274.
24. Kalivas PW (2004) Glutamate systems in cocaine addiction. Curr Opin Pharmacol 4:23-29.
25. Kalivas PW (2007) Neurobiology of cocaine addiction: implications for new pharmacotherapy. Am J Addict 16:71-78.
26. Kalivas PW, Lalumiere RT, Knackstedt L, Shen H (2009) Glutamate transmission in addiction. Neuropharmacology 56 [Suppl 1]:169-173.
27. Kauer JA, Malenka RC (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8:844-858.
28. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813-825.
29. Kim J, Dittgen T, Nimmerjahn A, Waters J, Pawlak V, Helmchen F, Schlesinger S, Seeburg PH, Osten P (2004) Sindbis vector SINrep(nsP2S726): a tool for rapid heterologous expression with attenuated cytotoxicity in neurons. J Neurosci Methods 133:81-90.
30. Klein M, Pieri I, Uhlmann F, Pfizenmaier K, Eisel U (1998) Cloning and characterization of promoter and 5'-UTR of theNMDAreceptor subunit epsilon 2: evidence for alternative splicing of 5'-non-coding exon. Gene 208:259-269.
31. Kolb B, Gorny G, Li Y, Samaha AN, Robinson TE (2003) Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens. Proc Natl Acad Sci U S A 100:10523-10528.
32. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217-238.
33. Kourrich S, Rothwell PE, Klug JR, Thomas MJ (2007) Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci 27:7921-7928.
34. KullmannDM (1994) Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12:1111-1120.
35. Kullmann DM, Erdemli G, Asztély F (1996) LTP of AMPA and NMDA receptor-mediated signals: evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17:461-474.
36. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN, Neve RL, Self DW, Nestler EJ (2005) Chromatin remodeling is a key mechanism underlying cocaineinduced plasticity in striatum. Neuron 48:303-314.
37. Lau CG, Zukin RS (2007) NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8:413-426.
38. Lee KW, Kim Y, Kim AM, Helmin K, Nairn AC, Greengard P (2006) Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc Natl Acad Sci U S A 103:3399-3404.
39. Lee MC, Yasuda R, Ehlers MD (2010) Metaplasticity at single glutamatergic synapses. Neuron 66:859-870.
40. Le Moine C, Bloch B (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J Comp Neurol 355:418-426.
41. Li Y, Hu XT, Berney TG, Vartanian AJ, Stine CD, Wolf ME, White FJ (1999) Both glutamate receptor antagonists and prefrontal cortex lesions prevent induction of cocaine sensitization and associated neuroadaptations. Synapse 34:169-180.
42. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 2:37-43.
43. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
44. Logan SM, Partridge JG, Matta JA, Buonanno A, Vicini S (2007) LonglastingNMDAreceptor-mediated EPSCs in mouse striatal medium spiny neurons. J Neurophysiol 98:2693-2704.
45. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
46. Lonze BE, Riccio A, Cohen S, Ginty DD (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34:371-385.
47. Losi G, Prybylowski K, Fu Z, Luo JH, Vicini S (2002) Silent synapses in developing cerebellar granule neurons. J Neurophysiol 87:1263-1270.
48. Mao LM, Wang W, Chu XP, Zhang GC, Liu XY, Yang YJ, Haines M, Papasian CJ, Fibuch EE, Buch S, Chen JG, Wang JQ (2009) Stability of surface NMDA receptors controls synaptic and behavioral adaptations to amphetamine. Nat Neurosci 12:602-610.
49. Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752.
50. Mattson BJ, Bossert JM, Simmons DE, Nozaki N, Nagarkar D, Kreuter JD, Hope BT (2005) Cocaine-induced CREB phosphorylation in nucleus accumbens of cocaine-sensitized rats is enabled by enhanced activation of extracellular signal-related kinase, but not protein kinase A. J Neurochem 95:1481-1494.
51. Maze I, Covington HE 3rd, Dietz DM, LaPlant Q, Renthal W, Russo SJ, Mechanic M, Mouzon E, Neve RL, Haggarty SJ, Ren Y, Sampath SC, Hurd YL, Greengard P, Tarakhovsky A, Schaefer A, Nestler EJ (2010) Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327:213-216.
52. McClung CA, Nestler EJ (2003) Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6:1208-1215.
53. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
54. Morishita W, Lu W, Smith GB, Nicoll RA, Bear MF, Malenka RC (2007) Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression. Neuropharmacology 52:71-76.
55. O'Donnell P, Grace AA (1993) Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J Neurosci 13:3456-3471.
56. Philpot BD, Zukin RS (2010) Synapse-specific metaplasticity: to be silenced is not to silence 2B. Neuron 66:814-816.
57. Pickard L, Noël J, Henley JM, Collingridge GL, Molnar E (2000) Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J Neurosci 20:7922-7931.
58. Pierce RC, Quick EA, Reeder DC, Morgan ZR, Kalivas PW (1998) Calciummediated second messengers modulate the expression of behavioral sensitization to cocaine. J Pharmacol Exp Ther 286:1171-1176.
59. Rani CS, Qiang M, Ticku MK (2005) Potential role of cAMP response element-binding protein in ethanol-induced N-methyl-D-aspartate receptor 2B subunit gene transcription in fetal mouse cortical cells. Mol Pharmacol 67:2126-2136.
60. Renthal W, Kumar A, Xiao G, Wilkinson M, Covington HE 3rd, Maze I, Sikder D, Robison AJ, LaPlant Q, Dietz DM, Russo SJ, Vialou V, Chakravarty S, Kodadek TJ, Stack A, Kabbaj M, Nestler EJ (2009) Genomewide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62:335-348.
61. Robinson TE, Berridge KC (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95 [Suppl 2]:S91- S117.
62. Robinson TE, Berridge KC (2001) Incentive-sensitization and addiction. Addiction 96:103-114.
63. Robinson TE, Berridge KC (2008) Review. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci 363:3137-3146.
64. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47 [Suppl 1]:33-46.
65. Russo SJ, Wilkinson MB, Mazei-Robison MS, Dietz DM, Maze I, Krishnan V, Renthal W, Graham A, Birnbaum SG, Green TA, Robison B, Lesselyong A, Perrotti LI, Bolaños CA, Kumar A, Clark MS, Neumaier JF, Neve RL, Bhakar AL, Barker PA, Nestler EJ (2009) Nuclear factor kappa B signaling regulates neuronal morphology and cocaine reward. J Neurosci 29:3529-3537.
66. Schultz W, Apicella P, Scarnati E, Ljungberg T (1992) Neuronal activity in monkey ventral striatum related to the expectation of reward. J Neurosci 12:4595-4610.
67. Shen H, Sesack SR, Toda S, Kalivas PW (2008) Automated quantification of dendritic spine density and spine head diameter in medium spiny neurons of the nucleus accumbens. Brain Struct Funct 213:149-157.
68. 2+] signaling in individual hippocampal dendritic spines. J Neurosci 25:6037-6046.
69. Strack S, Colbran RJ (1998) Autophosphorylation-dependent targeting of calcium/ calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 273:20689-20692.
70. Thomas MJ, Kalivas PW, Shaham Y (2008) Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br J Pharmacol 154:327-342.
71. Tirelli E, Laviola G, Adriani W (2003) Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 27:163-178.
72. Todtenkopf MS, Carreiras T, Melloni RH, Stellar JR (2002) The dorsome-dial shell of the nucleus accumbens facilitates cocaine-induced locomotor activity during the induction of behavioral sensitization. Behav Brain Res 131:9-16.
73. Vanderschuren LJ, Kalivas PW (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berl) 151:99-120.
74. Washbourne P, Bennett JE, McAllister AK (2002) Rapid recruitment ofNMDA receptor transport packets to nascent synapses. Nat Neurosci 5:751-759.
75. Williams SR, Mitchell SJ (2008) Direct measurement of somatic voltage clamp errors in central neurons. Nat Neurosci 11:790-798.
76. Wolf JA, Moyer JT, Lazarewicz MT, Contreras D, Benoit-Marand M, O'Donnell P, Finkel LH (2005) NMDA/AMPA ratio impacts state transitions and entrainment to oscillations in a computational model of the nucleus accumbens medium spiny projection neuron. J Neurosci 25:9080-9095.
77. Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679-720.
78. Wolf ME, Ferrario CR (2010) AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci Biobehav Rev 35:185-211.
79. Yao WD, Gainetdinov RR, Arbuckle MI, Sotnikova TD, Cyr M, Beaulieu JM, Torres GE, Grant SG, Caron MG (2004) Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 41:625-638.
80. Zhang Y, Schlussman SD, Ho A, Kreek MJ (2003) Effect of chronic "binge cocaine" on basal levels and cocaine-induced increases of dopamine in the caudate putamen and nucleus accumbens of C57BL/6J and 129/J mice. Synapse 50:191-199.
81. Zito K, Scheuss V, Knott G, Hill T, Svoboda K (2009) Rapid functional maturation of nascent dendritic spines. Neuron 61:247-258.