The addicted synapse: Mechanisms of synaptic and structural plasticity in nucleus accumbens

Trends in Neurosciences

Volumn 33, Issue 6, 2010, Pages 267-276

  Russo, Scott J ^a   Dietz, David M ^a   Dumitriu, Dani ^a   Morrison, John H ^a   Malenka, Robert C ^b   Nestler, Eric J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIN DEPENDENT KINASE 5; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIM KINASE; METHYLPHENIDATE; MORPHINE; MYOCYTE ENHANCER FACTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; OPIATE; PROTEIN CDC42; RAC1 PROTEIN; RAS PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR FOSB; WISKOTT ALDRICH SYNDROME PROTEIN; STREET DRUG;

CELL SPECIFICITY; COCAINE DEPENDENCE; DENDRITIC SPINE; DRUG DEPENDENCE; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MORPHINE ADDICTION; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; OPIATE ADDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; REWARD; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WITHDRAWAL SYNDROME; ADDICTION; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECTS; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPSE;

ANIMALS; DENDRITIC SPINES; MODELS, BIOLOGICAL; NEURONAL PLASTICITY; NEURONS; NUCLEUS ACCUMBENS; SIGNAL TRANSDUCTION; STREET DRUGS; SUBSTANCE-RELATED DISORDERS; SYNAPSES;

EID: 77953544634     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2010.02.002     Document Type: Review

References (92)

1. Sklair-Tavron L., et al. Chronic morphine induces visible changes in the morphology of mesolimbic dopamine neurons. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11202-11207.
2. Robinson T.E., Kolb B. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J. Neurosci. 1997, 17:8491-8497.
3. Robinson T.E., Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 2004, 47(Suppl. 1):33-46.
4. Li Y., et al. The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur. J. Neurosci. 2004, 20:1647-1654.
5. Pulipparacharuvil S., et al. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 2008, 59:621-633.
6. Russo S.J., et al. Nuclear factor kappa B signaling regulates neuronal morphology and cocaine reward. J. Neurosci. 2009, 29:3529-3537.
7. Maze I., et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 2010, 327:213-216.
8. Norrholm S.D., et al. Cocaine-induced proliferation of dendritic spines in nucleus accumbens is dependent on the activity of cyclin-dependent kinase-5. Neuroscience 2003, 116:19-22.
9. Russo S.J., et al. Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 2009, 56(Suppl. 1):73-82.
10. Dietz D.M., et al. Molecular mechanisms of psychostimulant-induced structural plasticity. Pharmacopsychiatry 2009, 42(Suppl. 1):S69-S78.
11. Nestler E.J. Molecular mechanisms of drug addiction. J. Neurosci. 1992, 12:2439-2450.
12. Russo S.J., et al. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat. Neurosci. 2007, 10:93-99.
13. Robinson T.E., et al. Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 2002, 46:271-279.
14. Robinson T.E., et al. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 2001, 39:257-266.
15. Robinson T.E., Kolb B. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur. J. Neurosci. 1999, 11:1598-1604.
16. Sarti F., et al. Acute cocaine exposure alters spine density and long-term potentiation in the ventral tegmental area. Eur. J. Neurosci. 2007, 26:749-756.
17. Lee K.W., et al. 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. 2006, 103:3399-3404.
18. Koob G.F., Le Moal M. Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat. Neurosci. 2005, 8:1442-1444.
19. Zito K., et al. Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 2004, 44:321-334.
20. Hamilton G.F., et al. Postnatal binge-like alcohol exposure decreases dendritic complexity while increasing the density of mature spines in mPFC Layer II/III pyramidal neurons. Synapse 2010, 64:127-135.
21. Luscher C., Bellone C. Cocaine-evoked synaptic plasticity: a key to addiction?. Nat. Neurosci. 2008, 11:737-738.
22. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 2007, 56:27-78.
23. Belin D., Everitt B.J. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 2008, 57:432-441.
24. Bourne J., Harris K.M. Do thin spines learn to be mushroom spines that remember?. Curr. Opin. Neurobiol. 2007, 17:381-386.
25. Carlisle H.J., Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci. 2005, 28:182-187.
26. Tada T., Sheng M. Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 2006, 16:95-101.
27. Nagerl U.V., et al. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 2004, 44:759-767.
28. Okamoto K., et al. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 2004, 7:1104-1112.
29. Zuo Y., et al. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 2005, 46:181-189.
30. Matsuzaki M., et al. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
31. Harris K.M., et al. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 1992, 12:2685-2705.
32. Holtmaat A.J., et al. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
33. Shen H.W., et al. Altered dendritic spine plasticity in cocaine-withdrawn rats. J. Neurosci. 2009, 29:2876-2884.
34. Thomas M.J., et al. Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat. Neurosci. 2001, 4:1217-1223.
35. Huang Y.H., et al. In vivo cocaine experience generates silent synapses. Neuron 2009, 63:40-47.
36. Malenka R.C., Nicoll R.A. Long-term potentiation - a decade of progress?. Science 1999, 285:1870-1874.
37. Marie H., et al. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 2005, 45:741-752.
38. Sheng M., et al. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994, 368:144-147.
39. Elias G.M., et al. Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20953-20958.
40. Boudreau A.C., et al. Cell surface AMPA receptors in the rat nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases. J. Neurosci. 2007, 27:10621-10635.
41. Boudreau A.C., Wolf M.E. Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J. Neurosci. 2005, 25:9144-9151.
42. Conrad K.L., et al. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 2008, 454:118-121.
43. Anderson S.M., et al. CaMKII: a biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking. Nat. Neurosci. 2008, 11:344-353.
44. Bachtell R.K., et al. Role of GluR1 expression in nucleus accumbens neurons in cocaine sensitization and cocaine-seeking behavior. Eur. J. Neurosci. 2008, 27:2229-2240.
45. Kourrich S., et al. Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J. Neurosci. 2007, 27:7921-7928.
46. Toda S., et al. Cocaine increases actin cycling: effects in the reinstatement model of drug seeking. J. Neurosci. 2006, 26:1579-1587.
47. Spijker S., et al. Morphine exposure and abstinence define specific stages of gene expression in the rat nucleus accumbens. FASEB J. 2004, 18:848-850.
48. Roche K.W. The expanding role of PSD-95: a new link to addiction. Trends Neurosci. 2004, 27:699-700.
49. Szumlinski K.K., et al. Homer isoforms differentially regulate cocaine-induced neuroplasticity. Neuropsychopharmacology 2006, 31:768-777.
50. Yao W.-D., et al. Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 2004, 41:625-638.
51. Heiman M., et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 2008, 135:738-748.
52. Kim W.Y., et al. Cocaine regulates ezrin-radixin-moesin proteins and RhoA signaling in the nucleus accumbens. Neuroscience 2009, 163:501-505.
53. Hope B.T., et al. Induction of a long-lasting AP-1 complex composed of altered Fos-like proteins in brain by chronic cocaine and other chronic treatments. Neuron 1994, 13:1235-1244.
54. Alibhai I.N., et al. Regulation of fosB and DeltafosB mRNA expression: in vivo and in vitro studies. Brain Res. 2007, 1143:22-33.
55. Shaw-Lutchman T.Z., et al. Regional and cellular mapping of cAMP response element-mediated transcription during naltrexone-precipitated morphine withdrawal. J. Neurosci. 2002, 22:3663-3672.
56. Shaw-Lutchman T.Z., et al. Regulation of CRE-mediated transcription in mouse brain by amphetamine. Synapse 2003, 48:10-17.
57. Perrotti L.I., et al. Distinct patterns of DeltaFosB induction in brain by drugs of abuse. Synapse 2008, 62:358-369.
58. McClung C.A., Nestler E.J. Regulation of gene expression and cocaine reward by CREB and [Delta]FosB. Nat. Neurosci. 2003, 6:1208-1215.
59. Zachariou V., et al. An essential role for [Delta]FosB in the nucleus accumbens in morphine action. Nat. Neurosci. 2006, 9:205-211.
60. Renthal W., et al. Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 2009, 62:335-348.
61. Carlezon W.A., et al. The many faces of CREB. Trends Neurosci. 2005, 28:436-445.
62. Murphy D.D., Segal M. Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1482-1487.
63. Seigo S., et al. Opposing functions of CREB and MKK1 synergistically regulate the geometry of dendritic spines in visual cortex. J. Comp. Neurol. 2007, 503:605-617.
64. Graham D.L., et al. Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat. Neurosci. 2007, 10:1029-1037.
65. Pu L., et al. BDNF-dependent synaptic sensitization in midbrain dopamine neurons after cocaine withdrawal. Nat. Neurosci. 2006, 9:605-607.
66. Vo N., et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16426-16431.
67. Abe K., et al. Vav2 is an activator of Cdc42, Rac1, and RhoA. J. Biol. Chem. 2000, 275:10141-10149.
68. Farnsworth C.L., et al. Calcium activation of Ras mediated by neuronal exchange factor Ras-GRF. Nature 1995, 376:524-527.
69. Krapivinsky G., et al. The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 2003, 40:775-784.
70. Penzes P., et al. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 2003, 37:263-274.
71. Tolias K.F., et al. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 2005, 45:525-538.
72. Edlund S., et al. Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol. Biol. Cell 2002, 13:902-914.
73. Wang J.Q., et al. Glutamate signaling to Ras-MAPK in striatal neurons: mechanisms for inducible gene expression and plasticity. Mol. Neurobiol. 2004, 29:1-14.
74. Yuan X.B., et al. Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat. Cell Biol. 2003, 5:38-45.
75. Machesky L.M., et al. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3739-3744.
76. Miki H., et al. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 1998, 391:93-96.
77. Miki H., et al. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 1998, 17:6932-6941.
78. Fasano S., et al. Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) controls activation of extracellular signal-regulated kinase (ERK) signaling in the striatum and long-term behavioral responses to cocaine. Biol. Psychiatry 2009, 66:758-768.
79. Rothenfluh A., et al. Distinct behavioral responses to ethanol are regulated by alternate RhoGAP18B isoforms. Cell 2006, 127:199-211.
80. Kumar A., et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 2005, 48:303-314.
81. Kim Y., et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 2006, 442:814-817.
82. Sung J.Y., et al. WAVE1 controls neuronal activity-induced mitochondrial distribution in dendritic spines. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3112-3126.
83. Benavides D.R., et al. Cdk5 modulates cocaine reward, motivation, and striatal neuron excitability. J. Neurosci. 2007, 27:12967-12976.
84. Bibb J.A., et al. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 2001, 410:376-380.
85. Berglind W.J., et al. A single intra-PFC infusion of BDNF prevents cocaine-induced alterations in extracellular glutamate within the nucleus accumbens. J. Neurosci. 2009, 29:3715-3719.
86. Kim Y., et al. Methylphenidate-induced dendritic spine formation and DeltaFosB expression in nucleus accumbens. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2915-2920.
87. Nestler E.J. Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:3245-3255.
88. Bateup H.S., et al. Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat. Neurosci. 2008, 11:932-939.
89. Ambroggi F., et al. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat. Neurosci. 2009, 12:247-249.
90. Lisman J.E., et al. The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat. Rev. Neurosci. 2007, 8:597-609.
91. Steiner P., et al. Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 2008, 60:788-802.
92. Kantevari S., et al. Two-color, two-photon uncaging of glutamate and GABA. Nat. Methods 2010, 7:123-125.