Analysis of the effects of cannabinoids on identified synaptic connections in the caudate-putamen by paired recordings in transgenic mice

Journal of Physiology

Volumn 575, Issue 3, 2006, Pages 789-806

  Freiman, Ilka ^a   Anton, Alexandra ^a   Monyer, Hannah ^b   Urbanski, Michal J ^a   Szabo, Bela ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID 1 RECEPTOR; CANNABINOID DERIVATIVE; ENDOCANNABINOID; ENHANCED GREEN FLUORESCENT PROTEIN; PARVALBUMIN; CANNABINOID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CAUDATE NUCLEUS; CONTROLLED STUDY; DENDRITIC CELL; EVOKED SOMATOSENSORY RESPONSE; FLUORESCENCE; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MEMBRANE CURRENT; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE ENDING; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUTAMEN; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; FIRING RATE; MEDIUM SPINY NEURON; MEMBRANE POTENTIAL; NERVE CELL; PATCH CLAMP TECHNIQUE;

ANIMALS; BENZOXAZINES; CANNABINOIDS; CAUDATE NUCLEUS; EVOKED POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GREEN FLUORESCENT PROTEINS; INTERNEURONS; MICE; MICE, TRANSGENIC; MORPHOLINES; NAPHTHALENES; NEURAL INHIBITION; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PRESYNAPTIC TERMINALS; PUTAMEN; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33748307560     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.114272     Document Type: Article

References (65)

1. Abood ME (2005). Molecular biology of cannabinoid receptors. In Cannabinoids: Handbook of Experimental Pharmacology, vol. 168, ed. Pertwee R, pp. 81-115. Springer, Heidelberg.
2. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JRP & Jonas P (2002). Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal intecrneuron networks. Proc Natl Acad Sci U S A 99, 13222-13227.
3. Bracci E, Centonze D, Bernardi G & Calabresi P (2002). Dopamine excites fast-spiking interneurons in the striatum. J Neurophysiol 87, 2190-2194.
4. Brenowitz SD & Regehr WG (2003). Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23, 6373-6384.
5. Centonze D, Grande C, Usiello A, Gubellini P, Erbs E, Martin AB, Pisani A, Tognazzi N, Bernardi G, Moratalla R, Borrelli E & Calabresi P (2003). Receptor subtypes involved in the presynaptic and postsynaptic actions of dopamine on striatal interneurons. J Neurosci 23, 6245-6254.
6. Centonze D, Rossi S, Prosperetti C, Tscherter A, Bernardi G, Maccarrone M & Calabresi P (2005). Abnormal sensitivity to cannabinoid receptor stimulation might contribute to altered gamma-aminobutyric acid transmission in the striatum of R6/2 Huntington's disease mice. Biol Psychiatry 57, 1583-1589.
7. Clements JD (1990). A statistical test for demonstrating a presynaptic site of action for a modulator of synaptic amplitude. J Neurosci Meth 31, 75-88.
8. Czubayko U & Plenz D (2002). Fast synaptic transmission between striatal spiny projection neurons. Proc Natl Acad Sci U S A 99, 15764-15769.
9. Diana MA & Marty A (2004). Endocannabinoid-mediated short-term synaptic plasticity: Depolarisation-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). Br J Pharmacol 142, 9-19.
10. Edwards DA, Kim J & Alger BE (2006). Multiple mechanisms of endocannabinoid response initiation in hippocampus. J Neurophysiol 95, 67-75.
11. Egertova M, Cravatt BF & Elphick MR (2003). Comparative analysis of fatty acid amide hydrolase and CB1 cannabinoid receptor expression in the mouse brain: Evidence of a widespread role for fatty acid amide hydrolase in regulation of endocannabinoid signaling. Neuroscience 119, 481-496.
12. Freiman I & Szabo B (2005). Cannabinoids depress excitatory neurotransmission between the subthalamic nucleus and the globus pallidus. Neuroscience 133, 305-313.
13. Freund TF, Katona I & Piomelli D (2003). Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83, 1017-1066.
14. Galante M & Marty A (2003). Presynaptic ryanodine-sensitive calcium stores contribute to evoked neurotransmitter release at the basket cell-Purkinje cell synapse. J Neurosci 23, 11229-11234.
15. Gerdeman G & Lovinger DM (2001). CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85, 468-471.
16. Gerdeman GL, Ronesi J & Lovinger DM (2002). Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nature Neurosci 5, 446-451.
17. Gerfen CR (2004). Basal ganglia. In The Rat Nervous System, ed. Paxinos G, pp. 455-508. Academic Press, San Diego.
18. Grubbs FE & Beck G (1972). Extension of sample sizes and percentage points for significance tests for outlying observations. Technometrics 14, 847-854.
19. Herkenham M, Lynn AB, De Costa BR & Richfield EK (1991 a). Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res 547, 267-274.
20. Herkenham M, Lynn AB, Johnson MR, Melvin LS, De Costa BR & Rice KC (1991 b). Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. J Neurosci 11, 563-583.
21. Hoffman AF & Lupica CR (2000). Mechanisms of cannabinoid inhibition of GABA A synaptic transmission in the hippocampus. J Neurosci 20, 2470-2479.
22. Hohmann AG & Herkenham M (2000). Localization of cannabinoid CB1 receptor mRNA in neuronal subpopulations of rat striatum: A double-label in situ hybridization study. Synapse 37, 71-80.
23. 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.
24. Huang C-C, Lo S-W & Hsu K-S (2001). Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol 532, 731-748.
25. 1 receptors on presynaptic inhibitory terminals in cultured rat hippocampal neurons. Neuroscience 98, 253-262.
26. Kawaguchi Y (1993). Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13, 4908-4923.
27. Kawaguchi Y, Wilson CJ, Augood SJ & Emson PC (1995). Striatal interneurones: Chemical, physiological and morphological characterization. Trends Neurosci 18, 527-535.
28. Kawaguchi Y, Wilson CJ & Emson PC (1989). Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. J Neurophysiol 62, 1052-1068.
29. Köfalvi A, Rodrigues RJ, Ledent C, Mackie K, Vizi SE, Cunha RA & Sperlagh B (2005). Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: A combined immunochemical and pharmacological analysis. J Neurosci 25, 2874-2884.
30. Koos T & Tepper JM (1999). Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nature Neurosci 2, 467-472.
31. Koos T & Tepper JM (2002). Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 22, 529-535.
32. Koos T, Tepper JM & Wilson CJ (2004). Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 24, 7916-7922.
33. Kreitzer AC, Carter AG & Regehr WG (2002). Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34, 787-796.
34. Kreitzer AC & Malenka RC (2005). Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 25, 10537-10545.
35. Kuster JE, Stevenson JI, Ward SJ, D'Ambra TE & Haycock DA (1993). Aminoalkylindole binding in rat cerebellum: Selective displacement by natural and synthetic cannabinoids. J Pharmacol Exp Ther 264, 1352-1363.
36. Lacey MG, Mercuri NB & North RA (1987). Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol 392, 397-416.
37. Leterrier C, Laine J, Darmon M, Boudin H, Rossier J & Lenkei Z (2006). Constitutive activation drives compartment- selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 26, 3141-3153.
38. Mackie K (2005). Distribution of cannabinoid receptors in the central and peripheral nervous system. In Cannabinoids: Handbook of Experimental Pharmacology, vol. 168, ed. Pertwee R, pp. 299-325. Springer, Heidelberg.
39. 2+-assisted metabotropic glutamate receptor subtype 1 to phospholipase C β4 signaling cascade in the cerebellum. J Neurosci 25, 6826-6835.
40. Marsicano G & Lutz B (1999). Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11, 4213-4225.
41. Matsuda LA, Bonner TI & Lolait SJ (1993). Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327, 535-550.
42. Meyer AH, Katona I, Blatow M, Rozov A & Monyer H (2002). In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22, 7055-7064.
43. Munro S, Thomas KL & Abu-Shaar M (1993). Molecular characterization of a peripheral receptor for cannabinoids. Nature 365, 61-65.
44. 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.
45. Pertwee R (2005). Pharmacological actions of cannabinoids. In Cannabinoids: Handbook of Experimental Pharmacology, Vol. 168, ed. Pertwee R, pp. 1-51. Springer, Heidelberg.
46. Plenz D (2003). When inhibition goes incognito: Feedback interaction between spiny projection neurons in striatal function. Trends Neurosci 26, 436-443.
47. Plenz D & Kitai ST (1998). Up and down states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures. J Neurosci 18, 266-283.
48. Rodriguez JJ, Mackie K & Pickel VM (2001). Ultrastructural localization of the CB1 cannabinoid receptor in μ-opioid receptor patches of the rat caudate putamen nucleus. J Neurosci 21, 823-833.
49. Ronesi J, Gerdeman GL & Lovinger DM (2004). Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J Neurosci 24, 1673-1679.
50. Sanudo-Pena CM, Tsou K & Walker MJ (1999). Motor actions of cannabinoids in the basal ganglia output nuclei. Life Sci 65, 703-713.
51. Szabo B, Dörner L, Pfreundtner C, Nörenberg W & Starke K (1998). Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85, 395-403.
52. Szabo B, Fröhlich R & Illes P (1996). No evidence for functional imidazoline receptors on locus coeruleus neurons. Naunyn Schmiedebergs Arch Pharmacol 353, 557-563.
53. Szabo B, Müller T & Koch H (1999). Effects of cannabinoids on dopamine release in the corpus striatum and the nucleus accumbens in vitro. J Neurochem 73, 1084-1089.
54. Szabo B & Schlicker E (2005). Effects of cannabinoids on neurotransmission. In Cannabinoids: Handbook of Experimental Pharmacology, vol. 168, ed. Pertwee R, pp. 318-356. Springer, Heidelberg.
55. Szabo B, Than M, Wallmichrath I & Thorn D (2004). Analysis of the effects of cannabinoids on synaptic transmission between basket and Purkinje cells in the cerebellar cortex of the rat. J Pharmacol Exp Ther 310, 915-925.
56. Tepper JM & Bolam PJ (2004). Functional diversity and specificity of neostriatal interneurons. Current Opinion Neurobiol 14, 685-692.
57. Tepper JM, Koos T & Wilson CJ (2004). GABAergic microcircuits in the neostriatum. Trends Neurosci 11, 662-669.
58. Tepper JM, Sharpe NA, Koos TZ & Trent F (1998). Postnatal development of the rat neostriatum: Electrophysiological, light- and electron-microscopic studies. Dev Neurosci 20, 125-145.
59. B receptors on inhibitory afferent neurons of Purkinje cells in the cerebellar cortex of the rat. Eur J Neurosci 15, 1575-1584.
60. Trettel J & Levine ES (2003). Endocannabinoids mediate rapid retrograde signaling at interneuron (r) pyramidal neuron synapses of the neocortex. J Neurophysiol 89, 2334-2338.
61. 1 receptors in the rat central nervous system. Neuroscience 83, 393-411.
62. Tunstall MJ, Oorschot DE, Kean A & Wickens JR (2002). Inhibitory interactions between spiny projection neurons in the rat striatum. J Neurophysiol 88, 1263-1269.
63. Wallmichrath I & Szabo B (2002). Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neuroscience 113, 671-682.
64. Wilson RI & Nicoll RA (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.
65. Wilson RI & Nicoll RA (2002). Endocannabinoid signaling in the brain. Science 296, 678-682.