SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance

Nature Neuroscience

Volumn 15, Issue 2, 2012, Pages 284-293

  Nazzaro, Cristiano ^a   Greco, Barbara ^a   Cerovic, Milica ^b   Baxter, Paul ^c   Rubino, Tiziana ^d   Trusel, Massimo ^a   Parolaro, Daniela ^d   Tkatch, Tatiana ^a   Benfenati, Fabio ^a   Pedarzani, Paola ^c   Tonini, Raffaella ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA9(11) TETRAHYDROCANNABINOL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE MODEL; DRUG DEPENDENCE; DRUG TOLERANCE; HABIT; IN VIVO STUDY; LONG TERM DEPRESSION; MALE; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APAMIN; BENZAMIDES; BIOPHYSICS; CANNABINOIDS; CARBAMATES; CONDITIONING, OPERANT; CORPUS STRIATUM; CYCLOHEXANOLS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HABITS; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; OKADAIC ACID; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PROTEIN BINDING; PYRAZOLES; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; SODIUM CHANNEL BLOCKERS; TETRAHYDROCANNABINOL; TRITIUM;

EID: 84856247652     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3022     Document Type: Article

References (49)

1. Maldonado, R. The neurobiology of addiction. J. Neural Transm. Suppl. 66, 1-14 (2003). (Pubitemid 38339940)
2. Centonze, D. et al. Chronic cocaine prevents depotentiation at corticostriatal synapses. Biol. Psychiatry 60, 436-443 (2006). (Pubitemid 44292156)
3. Hoffman, A.F., Oz, M., Caulder, T. & Lupica, C.R. Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J. Neurosci. 23, 4815-4820 (2003). (Pubitemid 36793206)
4. Mato, S. et al. A single in-vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat. Neurosci. 7, 585-586 (2004). (Pubitemid 38691895)
5. Mato, S., Robbe, D., Puente, N., Grandes, P. & Manzoni, O.J. Presynaptic homeostatic plasticity rescues long-term depression after chronic Δ9-tetrahydrocannabinol exposure. J. Neurosci. 25, 11619-11627 (2005). (Pubitemid 43102487)
6. Tonini, R. et al. ERK-dependent modulation of cerebellar synaptic plasticity after chronic Δ9-tetrahydrocannabinol exposure. J. Neurosci. 26, 5810-5818 (2006). (Pubitemid 44315274)
7. Maldonado, R. & Rodriguez, F. Cannabinoid addiction: behavioral models and neural correlates. J. Neurosci. 22, 3326-3331 (2002). (Pubitemid 37465736)
8. Chaperon, F. & Thiebot, M.H. Behavioral effects of cannabinoid agents in animals. Crit. Rev. Neurobiol. 13, 243-281 (1999). (Pubitemid 30265251)
9. Rubino, T., Forlani, G., Vigano, D., Zippel, R. & Parolaro, D. Ras/ERK signaling in cannabinoid tolerance: from behavior to cellular aspects. J. Neurochem. 93, 984-991 (2005). (Pubitemid 40695757)
10. Surmeier, D.J., Plotkin, J. & Shen, W. Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection. Curr. Opin. Neurobiol. 19, 621-628 (2009).
11. Yin, H.H., Knowlton, B.J. & Balleine, B.W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 19, 181-189 (2004). (Pubitemid 38122084)
12. Yin, H.H., Ostlund, S.B., Knowlton, B.J. & Balleine, B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 22, 513-523 (2005). (Pubitemid 41097624)
13. Belin, D. & Everitt, B.J. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57, 432-441 (2008). (Pubitemid 351179162)
14. Hilário, M.R. & Costa, R.M. High on habits. Front Neurosci 2, 208-217 (2008).
15. Lovinger, D.M. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58, 951-961 (2010).
16. Kano, M., Ohno-Shosaku, T., Hashimotodani, Y., Uchigashima, M. & Watanabe, M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 89, 309-380 (2009).
17. Herkenham, M. et al. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11, 563-583 (1991).
18. Hilário, M.R., Clouse, E., Yin, H.H. & Costa, R.M. Endocannabinoid signaling is critical for habit formation. Front. Integr. Neurosci. 1, 6 (2007).
19. Calabresi, P., Maj, R., Pisani, A., Mercuri, N.B. & Bernardi, G. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J. Neurosci. 12, 4224-4233 (1992).
20. Gerdeman, G.L., Ronesi, J. & Lovinger, D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5, 446-451 (2002). (Pubitemid 34454250)
21. Kreitzer, A.C. & Malenka, R.C. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci. 25, 10537-10545 (2005). (Pubitemid 41628455)
22. Ronesi, J. & Lovinger, D.M. Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J. Physiol. (Lond.) 562, 245-256 (2005). (Pubitemid 40207801)
23. Wang, Z. et al. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50, 443-452 (2006).
24. Martin, B.R., Sim-Selley, L.J. & Selley, D.E. Signaling pathways involved in the development of cannabinoid tolerance. Trends Pharmacol. Sci. 25, 325-330 (2004). (Pubitemid 38692425)
25. Kreitzer, A.C. & Malenka, R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445, 643-647 (2007). (Pubitemid 46232883)
26. Kreitzer, A.C. Physiology and pharmacology of striatal neurons. Annu. Rev. Neurosci. 32, 127-147 (2009).
27. Shen, W., Flajolet, M., Greengard, P. & Surmeier, D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848-851 (2008).
28. Fino, E. et al. Distinct coincidence detectors govern the corticostriatal spike timing-dependent plasticity. J. Physiol. (Lond.) 588, 3045-3062 (2010).
29. Surmeier, D.J., Song, W.J. & Yan, Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci. 16, 6579-6591 (1996). (Pubitemid 26337379)
30. Picconi, B. et al. Inhibition of phosphodiesterases rescues striatal long-term depression and reduces levodopa-induced dyskinesia. Brain 134, 375-387 (2011).
31. Grueter, B.A., Brasnjo, G. & Malenka, R.C. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci. 13, 1519-1525 (2010).
32. Szallasi, A., Cortright, D.N., Blum, C.A. & Eid, S.R. The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat. Rev. Drug Discov. 6, 357-372 (2007). (Pubitemid 46705200)
33. Picconi, B. et al. Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat. Neurosci. 6, 501-506 (2003). (Pubitemid 36514698)
34. Uchigashima, M. et al. Subcellular arrangement of molecules for 2-arachidonoyl glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J. Neurosci. 27, 3663-3676 (2007). (Pubitemid 46557660)
35. Adermark, L. & Lovinger, D.M. Combined activation of L-type Ca2+ channels and synaptic transmission is sufficient to induce striatal long-term depression. J. Neurosci. 27, 6781-6787 (2007). (Pubitemid 46983430)
36. Stocker, M. Ca2+-activated K+ channels: molecular determinants and function of the SK family. Nat. Rev. Neurosci. 5, 758-770 (2004). (Pubitemid 39336213)
37. Ngo-Anh, T.J. et al. SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 8, 642-649 (2005). (Pubitemid 40594206)
38. Higley, M.J. & Sabatini, B.L. Competitive regulation of synaptic Ca2+ influx by D2 dopamine and A2A adenosine receptors. Nat. Neurosci. 13, 958-966 (2010).
39. Kathuria, S. et al. Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81 (2003). (Pubitemid 36098263)
40. Quinn, J.J., Hitchcott, P.K., Umeda, E.A., Arnold, A.P. & Taylor, J.R. Sex chromosome complement regulates habit formation. Nat. Neurosci. 10, 1398-1400 (2007). (Pubitemid 350014683)
41. Yin, H.H. & Knowlton, B.J. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464-476 (2006). (Pubitemid 44012286)
42. Derusso, A.L. et al. Instrumental uncertainty as a determinant of behavior under interval schedules of reinforcement. Front. Integr. Neurosci. 4, 17 (2010).
43. Katona, I. & Freund, T.F. Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat. Med. 14, 923-930 (2008).
44. Gulyas, A.I. et al. Segregation of two endocannabinoid-hydrolyzing enzymes into pre-and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur. J. Neurosci. 20, 441-458 (2004). (Pubitemid 38969629)
45. Yin, H.H. et al. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333-341 (2009).
46. Thorn, C.A., Atallah, H., Howe, M. & Graybiel, A.M. Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66, 781-795 (2010).
47. Venance, L. & Glowinski, J. Heterogeneity of spike frequency adaptation among medium spiny neurones from the rat striatum. Neuroscience 122, 77-92 (2003). (Pubitemid 37329949)
48. Fino, E., Glowinski, J. & Venance, L. Bidirectional activity-dependent plasticity at corticostriatal synapses. J. Neurosci. 25, 11279-11287 (2005). (Pubitemid 43083702)
49. Tkatch, T., Baranauskas, G. & Surmeier, D.J. Kv4.2 mRNA abundance and A-type K+ current amplitude are linearly related in basal ganglia and basal forebrain neurons. J. Neurosci. 20, 579-588 (2000). (Pubitemid 30225560)