Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum

Journal of Neuroscience

Volumn 25, Issue 45, 2005, Pages 10537-10545

  Kreitzer, Anatol C ^a   Malenka, Robert C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; Endocannabinoid; L type calcium channel; Medium spiny neuron; mGluR; Striatum

Indexed keywords

CALCIUM CHANNEL L TYPE; DOPAMINE; ENDOCANNABINOID; METABOTROPIC RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL TYPE; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; HIPPOCAMPUS; LEARNING; LONG TERM DEPRESSION; MEMBRANE DEPOLARIZATION; MOTOR CONTROL; NERVE CELL PLASTICITY; NEUROSECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REINFORCEMENT;

ANIMALS; ASPARTIC ACID; CALCIUM CHANNEL BLOCKERS; CEREBELLUM; CORPUS STRIATUM; DOPAMINE; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ENDOCANNABINOIDS; EPISTASIS, GENETIC; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM DEPRESSION (PHYSIOLOGY); MEMBRANE POTENTIALS; METHOXYHYDROXYPHENYLGLYCOL; MORPHOLINES; NAPHTHALENES; NEURONS; NITRENDIPINE; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PYRAZOLES; QUINPIROLE; RATS; RATS, SPRAGUE-DAWLEY; SULPIRIDE; TIME FACTORS;

EID: 27744517743     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2959-05.2005     Document Type: Article

References (61)

1. Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286.
2. Asztely F, Erdemli G, Kullmann DM (1997) Extrasynaptic glutamate spill-over in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18:281-293.
3. Azad SC, Monory K, Marsicano G, Cravatt BF, Lutz B, Zieglgansberger W, Kammes G (2004) Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci 24:9953-9961.
4. Bamford NS, Zhang H, Schmitz Y, Wu NP, Cepeda C, Levine MS, Schmauss C, Zakharenko SS, Zablow L, Sulzer D (2004) Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42:653-663.
5. Brenowitz SD, Regehr WG (2003) Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23:6373-6384.
6. Brenowitz SD, Regehr WG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419-431.
7. Brown TM, Brotchie JM, Fitzjohn SM (2003) Cannabinoids decrease corticostriatal synaptic transmission via an effect on glutamate uptake. J Neurosci 23:11073-11077.
8. Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G (1992) Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12:4224-4233.
9. 2 receptors. J Neurosci 17:4536-4544.
10. Carter AG, Sabatini BL (2004) State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44:483-493.
11. Centonze D, Picconi B, Gubellini P, Bernardi G, Calabresi P (2001) Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur J Neurosci 13:1071-1077.
12. Centonze D, Gubellini P, Pisani A, Bernardi G, Calabresi P (2003) Dopamine, acetylcholine and nitric oxide systems interact to induce corticostriatal synaptic plasticity. Rev Neurosci 14:207-216.
13. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
14. Choi S, Lovinger DM (1997) Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci USA 94:2665-2670.
15. Di Marzo V (1999) Biosynthesis and inactivation of endocannabinoids: relevance to their proposed role as neuromodulators. Life Sci 65:645-655.
16. Dos Santos Villar F, Walsh IP (1999) Modulation of long-term synaptic plasticity at excitatory striatal synapses. Neuroscience 90:1031-1041.
17. Galante M, Diana MA (2004) Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. J Neurosci 24:4865-4874.
18. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446-451.
19. Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26:184-192.
20. Giuffrida A, Parsons LH, Kerr TM, Rodriguez de Fonseca F, Navarro M, Piomelli D (1999) Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 2:358-363.
21. Gubellini P, Saulle E, Centonze D, Bonsi P, Pisani A, Bernardi G, Conquet F, Calabresi P (2001) Selective involvement of mGlu1 receptors in corticostriatal LTD. Neuropharmacology 40:839-846.
22. Hashimotodani Y, Ohno-Shosaku T, Tsubokawa H, Ogata H, Emoto K, Maejima T, Araishi K, Shin H-S, Kano M (2005) Phospholipase Cβ serves as a coincidence detector through its Ca dependency for triggering retrograde endocannabinoid signal. Neuron 45:257-268.
23. Hoffman AF, Oz M, Caulder T, Lupica CR (2003) Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J Neurosci 23:4815-4820.
24. Huang CC, Lo SW, Hsu KS (2001) Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol (Lond) 532 3:731-748.
25. Kim J, Alger BE (2001) Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21:9608-9618.
26. Kreitzer AC, Regehr WG (2001a) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
27. Kreitzer AC, Regehr WG (2001b) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174(1-5).
28. Kreitzer AC, Regehr WG (2002) Retrograde signaling by endocannabinoids. Curr Opin Neurobiol 12:324-330.
29. Kushmerick C, Price GD, Taschenberger H, Puente N, Renden R, Wadiche JI, Duvoisin RM, Grandes P, von Gersdorff H (2004) Retroinhibition of presynaptic calcium currents by endocannabinoids released via postsynaptic mGluR activation at a calyx synapse. J Neurosci 24:5955-5965.
30. Lovinger DM, Tyler EC, Merritt A (1993) Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70:1937-1949.
31. Maejima T, Ohno-Shosaku T, Kano M (2001) Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40:205-210.
32. Mao L, Wang JQ (2003) Group I metabotropic glutamate receptor-mediated calcium signalling and immediate early gene expression in cultured rat striatal neurons. Eur J Neurosci 17:741-750.
33. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534.
34. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL (2004) Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24:53-62.
35. Montague PR, Dayan P, Sejnowski TJ (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J Neurosci 16:1936-1947.
36. Montague PR, Hyman SE, Cohen JD (2004) Computational roles for dopamine in behavioural control. Nature 431:760-767.
37. Nicola SM, Malenka RC (1998) Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J Neurophysiol 79:1768-1776.
38. Nicola SM, Surmeier J, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185-215.
39. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738.
40. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M (2002a) Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 15:953-961.
41. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M (2002b) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864-3872.
42. Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni OJ (2001) Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21:109-116.
43. 2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J Neurosci 22:4346-4356.
44. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002b) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 99:8384-8388.
45. Ronesi J, Lovinger DM (2005) Induction of striatal long-term depression by moderate frequency activation of cortical afferents in rat. J Physiol (Lond) 562:245-256.
46. Rouach N, Nicoll RA (2003) Endocannabinoids contribute to short-term but not long-term mGluR-induced depression in the hippocampus. Eur J Neurosci 18:1017-1020.
47. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27.
48. Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241-263.
49. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593-1599.
50. Sjostrom PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641-654.
51. Sung KW, Choi S, Lovinger DM (2001) Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J Neurophysiol 86:2405-2412.
52. Tang K, Low MJ, Grandy DK, Lovinger DM (2001) Dopamine-dependent synaptic plasticity in striatum during in vivo development. Proc Natl Acad Sci USA 98:1255-1260.
53. Trettel J, Levine ES (2003) Endocannabinoids mediate rapid retrograde signaling at interneuron right-arrow pyramidal neuron synapses of the neocortex. J Neurophysiol 89:2334-2338.
54. Varma N, Carlson GC, Ledent C, Alger BE (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188(1-5).
55. Walsh JP (1993) Depression of excitatory synaptic input in rat striatal neurons. Brain Res 608:123-128.
56. Wickens JR, Reynolds JN, Hyland BI (2003) Neural mechanisms of reward-related motor learning. Curr Opin Neurobiol 13:685-690.
57. Wilson CJ (1998) Basal ganglia. In: The synaptic organization of the brain (Shepherd GM, ed), pp 329-375. New York: Oxford UP.
58. Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397-2410.
59. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
60. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678-682.
61. Yanovsky Y, Mades S, Misgeld U (2003) Retrograde signaling changes the venue of postsynaptic inhibition in rat substantia nigra. Neuroscience 122:317-328.