AMPAR-independent effect of striatal αCaMKII promotes the sensitization of cocaine reward

Journal of Neuroscience

Volumn 32, Issue 19, 2012, Pages 6578-6586

  Kourrich, Saïd ^a,c   Klug, Jason R ^a,d   Mayford, Mark ^b   Thomas, Mark J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; COCAINE; DOXYCYCLINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; LOCOMOTION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; NUCLEUS ACCUMBENS; POTASSIUM CURRENT; PRIORITY JOURNAL; PSYCHOMOTOR ACTIVITY; REWARD; SPIKE; SYNAPSE; TRANSGENE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; COCAINE; CONDITIONING (PSYCHOLOGY); CORPUS STRIATUM; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; RECEPTORS, AMPA; REWARD; SYNAPSES; UP-REGULATION;

EID: 84860656141     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6391-11.2012     Document Type: Article

References (62)

1. Ambroggi F, Ghazizadeh A, Nicola SM, Fields HL (2011) Roles of nucleus accumbens core and shell in incentivecue responding and behavioral inhibition. J Neurosci 31:6820-6830.
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. Bachtell RK, Self DW (2008) Renewed cocaine exposure produces transient alterations in nucleus accumbens AMPA receptor-mediated behavior. J Neurosci 28:12808-12814.
4. Bachtell RK, Choi KH, Simmons DL, Falcon E, Monteggia LM, Neve RL, Self DW (2008) Role of GluR1 expression in nucleus accumbens neurons in cocaine sensitization and cocaine-seeking behavior. Eur J Neurosci 27:2229-2240.
5. Bargas J, Galarraga E, Aceves J (1989) An early outward conductance modulates the firing latency and frequency of neostriatal neurons of the rat brain. Exp Brain Res 75:146-156.
6. Beck H, Yaari Y (2008) Plasticity of intrinsic neuronal properties in CNS disorders. Nat Rev Neurosci 9:357-369.
7. Bejar R, Yasuda R, Krugers H, Hood K, Mayford M (2002) Transgenic calmodulin-dependent protein kinase II activation: dose-dependent effects on synaptic plasticity, learning, and memory. J Neurosci 22:5719-5726.
8. Birnbaum SG, Varga AW, Yuan LL, Anderson AE, Sweatt JD, Schrader LA (2004) Structure and function of Kv4-family transient potassium channels. Physiol Rev 84:803-833.
9. Boudreau AC, Ferrario CR, Glucksman MJ, Wolf ME (2009) Signaling pathway adaptations and novel protein kinase A substrates related to behavioral sensitization to cocaine. J Neurochem 110:363-377.
10. Buard I, Coultrap SJ, Freund RK, Lee YS, Dell'Acqua ML, Silva AJ, Bayer KU (2010) CaMKII "autonomy" is required for initiating but not for maintaining neuronal long-term information storage. J Neurosci 30:8214-8220.
11. Carlezon WA Jr, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, Nestler EJ (1998) Regulation of cocaine reward by CREB. Science 282:2272-2275.
12. Carlezon WA Jr, Thomas MJ (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuro pharmacology 56 [Suppl 1]:122-132.
13. Conrad KL, Tseng KY, Uejima JL, Reimers JM, Heng LJ, Shaham Y, Marinelli M, Wolf ME (2008) Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454:118-121.
14. Cornish JL, Kalivas PW (2000) Glutamate transmission in the nucleus ac-cumbens mediates relapse in cocaine addiction. J Neurosci 20:RC89.
15. 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.
16. Ferrario CR, Li X, Wang X, Reimers JM, Uejima JL, Wolf ME (2010) The role of glutamate receptor redistribution in locomotor sensitization to cocaine. Neuro psycho pharmacology 35:818-833.
17. Guillem K, Peoples LL (2010) Progressive and lasting amplification of accumbal nicotine-seeking neural signals. J Neurosci 30:276-286.
18. Guillem K, Peoples LL (2011) Acute effects of nicotine amplify accumbal neural responses during nicotine-taking behavior and nicotine-paired environmental cues. PloS one 6:e24049.
19. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
20. 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.
21. Ishikawa M, Mu P, Moyer JT, Wolf JA, Quock RM, Davies NM, Hu XT, Schlüter OM, Dong Y (2009) Homeostatic synapse-driven membrane plasticity in nucleus accumbens neurons. J Neurosci 29:5820-5831.
22. Kalivas PW, Hu XT (2006) Exciting inhibition in psychostimulant addiction. Trends Neurosci 29:610-616.
23. Kasanetz F, Deroche-Gamonet V, Berson N, Balado E, Lafourcade M, Man-zoni O, Piazza PV (2010) Transition to addiction is associated with a persistent impairment in synaptic plasticity. Science 328:1709-1712.
24. Kelley AE (2004) Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44:161-179.
25. Kelz MB, Chen J, Carlezon WA Jr, Whisler K, Gilden L, Beckmann AM, Steffen C, Zhang YJ, Marotti L, Self DW, Tkatch T, Baranauskas G, Sur-meier DJ, Neve RL, Duman RS, Picciotto MR, Nestler EJ (1999) Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401:272-276.
26. Kourrich S, Thomas MJ (2009) Similar neurons, opposite adaptations: psychostimulant experience differentially alters firing properties in accumbens core versus shell. JNeurosci 29:12275-12283.
27. Kourrich S, Rothwell PE, Klug JR, Thomas MJ (2007) Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci 27:7921-7928.
28. Krause M, German PW, Taha SA, Fields HL (2010) A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. J Neurosci 30:4746-4756.
29. Leicher T, Bahring R, Isbrandt D, Pongs O (1998) Coexpression of the KCNA3B gene product with Kv1.5 leads to a novel A-type potassium channel. J Biol Chem 273:35095-35101.
30. Liao D, Scannevin RH, Huganir R (2001) Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J Neurosci 21:6008-6017.
31. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci U S A 92:11175-11179.
32. Loweth JA, Baker LK, Guptaa T, Guillory AM, Vezina P (2008) Inhibition of CaMKII in the nucleus accumbens shell decreases enhanced amphetamine intake in sensitized rats. Neurosci Lett 444:157-160.
33. Loweth JA, Singer BF, Baker LK, Wilke G, Inamine H, Bubula N, Alexander JK, Carlezon WA Jr, Neve RL, Vezina P (2010) Transient over expression of alpha-Ca2+/calmodulin-dependent protein kinase II in the nucleus accumbens shell enhances behavioral responding to amphetamine. J Neurosci 30:939-949.
34. Mameli M, Halbout B, Creton C, Engblom D, Parkitna JR, Spanagel R, Lüscher C (2009) Cocaine-evoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat Neurosci 12:1036-1041.
35. Mayford M, Wang J, Kandel ER, O'Dell TJ (1995) CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell 81:891-904.
36. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
37. Mu P, Moyer JT, Ishikawa M, Zhang Y, Panksepp J, Sorg BA, Schlüter OM, Dong Y (2010) Exposure to cocaine dynamically regulates the intrinsic membrane excitability of nucleus accumbens neurons. J Neurosci 30:3689-3699.
38. Nisenbaum ES, Xu ZC, Wilson CJ (1994) Contribution of a slowly inactivating potassium current to the transition to firing of neostriatal spiny projection neurons. J Neurophysiol 71:1174-1189.
39. Pascoli V, Turiault M, Lüscher C (2012) Reversal of cocaineevoked synaptic potentiation resets drug-induced adaptive behavior. Nature 481:71-75.
40. Peoples LL, Cavanaugh D (2003) Differential changes in signal and background firing of accumbal neurons during cocaine self administration. J Neurophysiol 90:993-1010.
41. Peoples LL, Lynch KG, Lesnock J, Gangadhar N (2004) Accumbal neural responses during the initiation and maintenance of intravenous cocaine self-administration. J Neurophysiol 91:314-323.
42. Peoples LL, Kravitz AV, Guillem K (2007a) The role of accumbal hypo activity in cocaine addiction. Scientific World Journal 7:22-45.
43. Peoples LL, Kravitz AV, Lynch KG, Cavanaugh DJ (2007b) Accumbal neurons that are activated during cocaine self-administration are spared from inhibitory effects of repeated cocaine self-administration. Neuropsycho-pharmacology 32:1141-1158.
44. Pierce RC, Bell K, Duffy P, Kalivas PW (1996) Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 16:1550-1560.
45. Pierce RC, Quick EA, Reeder DC, Morgan ZR, Kalivas PW (1998) Calcium-mediated second messengers modulate the expression of behavioral sensitization to cocaine. J Pharmacol Exp Ther 286:1171-1176.
46. Rettig J, Heinemann SH, Wunder F, Lorra C, Parcej DN, Dolly JO, Pongs O (1994) Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature 369:289-294.
47. Rothwell PE, Kourrich S, Thomas MJ (2011) Synaptic adaptations in the nucleus accumbens caused by experiences linked to relapse. Biological psychiatry 69:1124-1126.
48. Rumbaugh G, Vicini S (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19:10603-10610.
49. Sergeant GP, Ohya S, Reihill JA, Perrino BA, Amberg GC, Imaizumi Y, Horowitz B, Sanders KM, Koh SD (2005) Regulation of Kv4.3 currents by Ca2+/calmodulin-dependent protein kinase II. Am J Physiol Cell Physiol 288:C304-C313.
50. Singer BF, Loweth JA, Neve RL, Vezina P (2010) Transient viral-mediated over expression of alpha-calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell leads to long-lasting functional up regulation of alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate receptors: dopamine type-1 receptor and protein kinase A dependence. Eur J Neurosci 31:1243-1251.
51. Stewart J (2004) Pathways to relapse: factors controlling the re initiation of drug seeking after abstinence. Nebr Symp Motiv 50:197-234.
52. Sun P, Enslen H, Myung PS, Maurer RA (1994) Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev 8:2527-2539.
53. Suto N, Tanabe LM, Austin JD, Creekmore E, Pham CT, Vezina P (2004) Previous exposure to psychostimulants enhances the reinstatement of cocaine seeking by nucleus accumbens AMPA. Neuropsychopharmacol-ogy 29:2149-2159.
54. Sutton MA, Schmidt EF, Choi KH, Schad CA, Whisler K, Simmons D, Kara-nian DA, Monteggia LM, Neve RL, Self DW (2003) Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behavior. Nature 421:70-75.
55. Taha SA, Fields HL (2006) Inhibitions of nucleus accumbens neurons encode a gating signal for reward-directed behavior. J Neurosci 26:217-222.
56. Thomas MJ, Beurrier C, Bonci A, Malenka RC (2001) Long-term depression in the nucleus accumbens: aneural correlate of behavioral sensitization to cocaine. Nat Neurosci 4:1217-1223.
57. Vacher H, Diochot S, Bougis PE, Martin-Eauclaire MF, Mourre C (2006) Kv4 channels sensitivetoBmTX3inrat nervous system: autoradiographic analysis of their distribution during brain ontogenesis. Eur J Neurosci 24:1325-1340.
58. Varga AW, Anderson AE, Adams JP, Vogel H, Sweatt JD (2000) Input-specific immuno localization of differentially phosphorylated Kv4.2 in the mouse brain. Learn Mem 7:321-332.
59. Varga AW, Yuan LL, Anderson AE, Schrader LA, Wu GY, Gatchel JR, Johnston D, Sweatt JD (2004) Calcium-calmodulin-dependent kinase II modulates Kv4.2 channel expression and up regulates neuronal A-type potassium currents. J Neurosci 24:3643-3654.
60. Wayman GA, Lee YS, Tokumitsu H, Silva AJ, Silva A, Soderling TR (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59:914-931.
61. Wiltgen BJ, Law M, Ostlund S, Mayford M, Balleine BW (2007) The influence of Pavlovian cues on instrumental performance is mediated by CaMKII activity in the striatum. Eur J Neurosci 25:2491-2497.
62. Wu X, McMurray CT (2001) Calmodulin kinaseII attenuation of gene transcription by preventing cAMP response element-binding protein (CREB) dimerization and binding of the CREB-binding protein. J Biol Chem 276:1735-1741.