Endogenous cannabinoid signaling through the CB1 receptor is essential for cerebellum-dependent discrete motor learning

Journal of Neuroscience

Volumn 26, Issue 34, 2006, Pages 8829-8837

  Kishimoto, Yasushi ^a,b   Kano, Masanobu ^a,b  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

Associative learning; CB1 cannabinoid receptor; Cerebellum; Delay eyeblink conditioning; Endocannabinoid; Knock out mice; Motor learning; Purkinje cell; Trace eyeblink conditioning

Indexed keywords

CANNABINOID; CANNABINOID 1 RECEPTOR; RIMONABANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOPSY; CEREBELLUM; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; ELECTRIC SHOCK; EYELID REFLEX; HIPPOCAMPUS; LEARNING; MALE; MOTOR COORDINATION; NONHUMAN; PRIORITY JOURNAL; SENSORY DYSFUNCTION; SIGNAL TRANSDUCTION; STATE DEPENDENT LEARNING; WILD TYPE;

ACOUSTIC STIMULATION; ANIMALS; BLINKING; CEREBELLUM; CONDITIONING, CLASSICAL; ELECTROSHOCK; ENDOCANNABINOIDS; EXTINCTION, PSYCHOLOGICAL; LEARNING; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; MOTOR SKILLS; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; SENSATION; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 33748285228     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1236-06.2006     Document Type: Article

References (64)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
2. Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286.
3. Ameri A (1999) The effects of cannabinoids on the brain. Prog Neurobiol 58:315-348.
4. Bacci A, Huguenard JR, Prince DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312-316.
5. Bilkei-Gorzo A, Racz I, Valverde O, Otto M, Michel K, Sastre M, Zimmer A (2005) Early age-related cognitive impairment in mice lacking cannabinoid CB1 receptors. Proc Natl Acad Sci USA 102:15670-15675.
6. Bohme GA, Laville M, Ledent C, Parmentier M, Imperato A (2000) Enhanced long-term potentiation in mice lacking cannabinoid CB1 receptors. Neuroscience 95:5-7.
7. Brenowitz SD, Regehr WG (2003) Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23:6373-6384.
8. Brenowitz SD, Regehr WG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419-431.
9. Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048-1057.
10. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim JJ, Hashimoto K, Thompson RF, Tonegawa S (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKCγ mutant mice. Cell 83:1233-1242.
11. Chen L, Bao S, Thompson RF (1999) Bilateral lesions of the interpositus nucleus completely prevent eyeblink conditioning in Purkinje cell-degeneration mutant mice. Behav Neurosci 113:204-210.
12. Chen L, Bao S, Lockard JM, Kim JJ, Thompson RF (1996) Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J Neurosci 16:2829-2838.
13. Chevaleyre V, Castillo PE (2004) Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43:871-881.
14. Chhatwal JP, Davis M, Maguschak KA, Ressler KJ (2005) Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 30:516-524.
15. Compton DR, Aceto MD, Lowe J, Martin BR (1996) In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): inhibition of delta 9-tetrahydrocannabinol-induced responses and apparent agonist activity. J Pharmacol Exp Ther 277:586-594.
16. Degroot A, Nomikos GG (2004) Genetic deletion and pharmacological blockade of CB1 receptors modulates anxiety in the shock-probe burying test. Eur J Neurosci 20:1059-1064.
17. Diana MA, Levenes C, Mackie K, Marty A (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22:200-208.
18. Egertova M, Elphick MR (2000) Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422:159-171.
19. Elphick MR, Egertova M (2001) The neurobiology and evolution of cannabinoid signalling. Philos Trans R Soc Lond B Biol Sci 356:381-408.
20. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066.
21. Holter SM, Kallnik M, Wurst W, Marsicano G, Lutz B, Wotjak CT (2005) Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitively-motivated learning task. Eur J Pharmacol 510:69-74.
22. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
23. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, Aiba A (2000) mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288:1832-183 5.
24. Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85-102.
25. Kadotani H, Hirano T, Masugi M, Nakamura K, Nakao K, Katsuki M, Nakanishi S (1996) Motor discoordination results from combined gene disruption of the NMDA receptor NR2A and NR2C subunits, but not from single disruption of the NR2A or NR2C subunit. J Neurosci 16:7859-7867.
26. Kano M, Ohno-Shosaku T, Maejima T, Yoshida T, Hashimoto K (2003) Retrograde modulation of synaptic transmission mediated by endogenous cannabinoids. Curr Neuropharmacol 2:49-57.
27. Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiangs H, Wu Y, Jun K, Shin H-S, Inoue Y, Simon MI, Wu D (1998) PLCβ4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci USA 95:15724-15729.
28. Kawamura Y, Fukaya M, Maejima T, Yoshida T, Miura E, Watanabe M, Ohno-Shosaku T, Kano M (2006) The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic site in the hippocampus and cerebellum. J Neurosci 26:2991-3001.
29. Kishimoto Y, Kawahara S, Mori H, Mishina M, Kirino Y (2001a) Long-trace interval eyeblink conditioning is impaired in mutant mice lacking the NMDA receptor subunit ε1. Eur J Neurosci 13:1221-1227.
30. Kishimoto Y, Nakazawa K, Tonegawa S, Kirino Y, Kano M (2006) Hippocampal CA3 NMDA receptors are crucial for adaptive timing of trace eyeblink conditioned response. J Neurosci 26:1562-1570.
31. Kishimoto Y, Kawahara S, Suzuki M, Mori H, Mishina M, Kirino Y (2001b) Classical eyeblink conditioning in glutamate receptor subunit δ2 mutant mice is impaired in the delay paradigm but not in the trace paradigm. Eur J Neurosci 13:1249-1253.
32. Kishimoto Y, Fujimichi R, Araishi K, Kano M, Aiba A, Kirino Y (2002) mGluR1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Eur J Neurosci 16:2416-2424.
33. Kishimoto Y, Hirono M, Sugiyama T, Kawahara S, Nakao K, Kishio M, Katsuki M, Yoshioka T, Kirino Y (2001c) Impaired delay but normal trace eyeblink conditioning in PLCβ4 mutant mice. NeuroReport 12:2919-2922.
34. Kreitzer AC, Regehr WG (2001a) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
35. Kreitzer AC, Regehr WG (2001b) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174(1-5).
36. Kreitzer AC, Regehr WG (2002) Retrograde signaling by endocannabinoids. Curr Opin Neurobiol 12:324-330.
37. 1 receptor knockout mice. Science 283:401-404.
38. Maejima T, Ohno-Shosaku T, Kano M (2001a) Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40:205-210.
39. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001b) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
40. 2+-assisted metabotropic glutamate receptor subtype 1 to phospholipase C β4 signaling cascade in the cerebellum. J Neurosci 25:6826-6835.
41. 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.
42. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561-564.
43. McCormick DA, Thompson RF (1984) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223:296-299.
44. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, Wu Y, Jun K, Wu D, Kano M, Shin H-S (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C β4 mutant mice. Eur J Neurosci 13:1945-1954.
45. Moyer JRJ, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav Neurosci 104:243-252.
46. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61-65.
47. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738.
48. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884.
49. Rinaldi-Carmona M, Barth F, Heaulme M, Alonso R, Shire D, Congy C, Soubrie P, Breliere JC, Le Fur G (1995) Biochemical and pharmacological characterization of SR141716A, the first potent and selective brain cannabinoid receptor antagonist. Life Sci 56:1941-1947.
50. Safo PK, Regehr WG (2005) Endocannabinoids control the induction of cerebellar LTD. Neuron 48:647-659.
51. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, Wakatsuki H, Fujisaki T, Fujimoto K, Katoh A, Ikeda T, Chen C, Thompson RF, Itohara S (1996) Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 16:587-599.
52. Slanina KA, Roberto M, Schweitzer P (2005) Endocannabinoids restrict hippocampal long-term potentiation via CB1. Neuropharmacology 49:660-668.
53. Steiner H, Bonner TI, Zimmer AM, Kitai S, Zimmer A (1999) Altered gene expression in striatal projection neurons in CB1 cannabinoid receptor knockout mice. Proc Natl Acad Sci USA 96:5786-5790.
54. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787-4795.
55. Thompson RF, Kim JJ (1996) Memory systems in the brain and localization of a memory. Proc Natl Acad Sci USA 93:13438-13444.
56. Thompson RF, Bao S, Chen L, Cipriano BD, Grethe JS, Kim JJ, Thompson JK, Tracy JA, Weninger MS, Krupa DJ (1997) Associative learning. San Diego: Academic.
57. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393-411.
58. Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301:915-924.
59. Weiss C, Bouwmeester H, Power JM, Disterhoft JF (1999) Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav Brain Res 99:123-132.
60. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
61. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678-682.
62. Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K, Kano M (2002) The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22:1690-1697.
63. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M (2006) Localization of diacylglycerol lipase-α around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26:4740-4751.
64. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 96:5780-5785.