Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons

Journal of Neuroscience

Volumn 19, Issue 11, 1999, Pages 4544-4558

  Katona, István ^a   Sperlágh, Beáta ^a   Sík, Attila ^a   Käfalvi, Attila ^a   Vizi, E Sylvester ^a   Mackie, Ken ^b   Freund, Tamás F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anxiety; Cannabinoids; Cholecystokinin; GABA; Hippoca mpus; Inhibition; Interneurons; Parvalbumin

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CANNABINOID RECEPTOR; CHOLECYSTOKININ; PARVALBUMIN; PRESYNAPTIC RECEPTOR; RIMONABANT; TRITIUM;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; COGNITION; CONTROLLED STUDY; ELECTRON MICROSCOPY; HIPPOCAMPUS; IMMUNOGOLD STAINING; IMMUNOPEROXIDASE STAINING; INTERNEURON; MALE; NERVE ENDING; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

EID: 0345621691     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-11-04544.1999     Document Type: Article

References (83)

1. Abood ME, Martin BR (1992) Neurobiology of marijuana abuse. Trends Pharmacol Sci 13:201-206.
2. Acsády L, Arabadzisz D, Freund TF (1996a) Correlated morphological and neurochemical features identify different subsets of vasoactive intestinal polypeptide-immunoreactive interneurons in rat hippocampus. Neuroscience 73:299-315.
3. Acsády L, Görcs TJ, Freund TF (1996b) Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73:317-334.
4. Acsády L, Katona I, Gulyás AI, Shigemoto R, Freund TF (1997) Immunostaining for substance P receptor labels GABAergic cells with distinct termination patterns in the hippocampus. J Comp Neurol 378:320-336.
5. Baimbridge KG, Miller JJ (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245:223-229.
6. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P (1993) The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
7. 3H]GABA release from striatal slices: evidence for a calcium-independent process via the GABA uptake system. Neuroscience 27:563-570.
8. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
9. Caulfield MP, Brown DA (1992) Cannabinoid receptor agonists inhibit Ca current in NG108-15 neuroblastoma cells via a pertussis toxin-sensitive mechanism. Br J Pharmacol 106:231-232.
10. Chan PK, Chan SC, Yung WH (1998) Presynaptic inhibition of GABAergic inputs to rat substantia nigra pars reticulata neurones by a cannabinoid agonist. NeuroReport 9:671-675.
11. Childers SR, Deadwyler SA (1996) Role of cyclic AMP in the actions of cannabinoid receptors. Biochem Pharmacol 52:819-827.
12. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
13. Collin C, Devane WA, Dahl D, Lee CJ, Axelrod J, Alkon DL (1995) Long-term synaptic transformation of hippocampal CA1gamma-aminobutyric acid synapses and the effect of anandamide. Proc Natl Acad Sci USA 92:10167-10171.
14. Compton DR, Gold LH, Ward SJ, Balster RL, Martin BR (1992) Aminoalkylindole analogs: cannabimimetic activity of a class of compounds structurally distinct from delta 9-tetrahydrocannabinol. J Pharmacol Exp Ther 263:1118-1126.
15. Constoe PF, Jones BC, Chin L (1975) Delta-9-tetrahydrocannabinol, EEG and behavior: the importance of adaptation to the testing milieu. Pharmacol Biochem Behav 3:173-177.
16. Coull MA, Johnston AT, Pertwee RG, Davies SN (1997) Action of delta-9-tetrahydrocannabinol on GABA(A) receptor-mediated responses in a grease-gap recording preparation of the rat hippocampal slice. Neuropharmacology 36:1387-1392.
17. D'Ambra TE, Estep KG, Bell MR, Eissenstat MA, Josef KA, Ward SJ, Haycock DA, Baizman ER, Casiano FM, Beglin NC, Chippari SM, Grego JD, Kullnig RK, Daley GT (1992) Conformationally restrained analogues of pravadoline: nanomolar potent, enantioselective, (aminoalkyl)indole agonists of the cannabinoid receptor. J Med Chem 35:124-135.
18. Deadwyler SA, Hampson RE, Mu J, Whyte A, Childers S (1995) Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J Pharmacol Exp Ther 273:734-743.
19. Devane WA, Dysarz FA, Johnson MR, Melvin LS, Howlett AC (1988) Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 34:605-613.
20. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946-1949.
21. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
22. Gao B, Fritschy JM (1994) Selective allocation of GABAA receptors containing the alpha 1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons. Eur J Neurosci 6:837-853.
23. Cessa GL, Casu MA, Carta G, Mascia MS (1998) Cannabinoids decrease acetylcholine release in the medial prefrontal cortex and hippocampus, reversal by SR141716A. Eur J Pharmacol 21:119-124.
24. Gifford AN, Ashby Jr CR (1996) Electrically evoked acetylcholine release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. J Pharmacol Exp Ther 277:1431-1436.
25. Gifford AN, Samiian L, Gatley SJ, Ashby Jr CR (1997) Examination of the effect of the cannabinoid receptor agonist, CP 55,940, on electrically evoked transmitter release from rat brain slices. Eur J Pharmacol 324:187-192.
26. Gulyás AI, Görcs TJ, Freund TF (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37:31-44.
27. Hájos N, Papp EC, Acsády L, Levey AI, Freund TF (1998) Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82:355-376.
28. Hársing Jr LG, Zigmond MJ (1998) Postsynaptic integration of cholinergic and dopaminergic signals on medium-sized GABAergic projection neurons in the neostriatum. Brain Res Bull 45:607-613.
29. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87:1932-1936.
30. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583.
31. Heyser CJ, Hampson RE, Deadwyler SA (1993) Effects of delta-9-tetrahydrocannabinol on delayed match to sample performance in rats: alterations in short-term memory associated with changes in task specific firing of hippocampal cells. J Pharmacol Exp Ther 264:294-307.
32. Iversen LL, Kelly JS (1975) Uptake and metabolism of gamma-aminobutyric acid by neurones and glial cells. Biochem Pharmacol 24:933-938.
33. Jansen EM, Haycock DA, Ward SJ, Seybold VS (1992) Distribution of cannabinoid receptors in rat brain determined with aminoalkylindoles. Brain Res 575:93-102.
34. Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347-362.
35. Kelly JS, Dick F (1976) Differential labeling of glial cells and GABA inhibitory interneurons and nerve terminals following the microinjection of (β-3)alanine. In: Cold Spring Harbor symposia on quantitative biology, XL, the synpase, pp 93-106. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
36. Kosaka T, Kosaka K, Tateishi K, Hamaoka Y, Yanaihara N, Wu JY, Hama K (1985) GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J Comp Neurol 239:420-430.
37. Kujtan PW, Carlen PL, Kapur BM (1983) delta 9-Tetrahydrocannabinol and cannabidiol: dose-dependent effects on evoked potentials in the hippocampal slice. Can J Physiol Pharmacol 61:420-426.
38. Lévenes C, Daniel H, Soubrie P, Crepel F (1998) Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol (Lond) 510:867-879.
39. Lichtman AH, Martin BR (1996) Delta 9-tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacology (Berl) 126:125-131.
40. Lichtman AH, Dimen KR, Martin BR (1995) Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology (Berl) 119:282-290.
41. 3H]aminobutyric acid in rabbit caudate nucleus slices. J Neurochem 46:1102-1108.
42. Lipparini F, Scotti de Carolis A, Longo VG (1969) A neuropharmacological investigation of some transtetra-hydrocannabinol derivatives. Physiol Behav 4:527-532.
43. Maccaferri G, McBain CJ (1995) Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15:137-145.
44. Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 89:3825-3829.
45. Mackie K, Lai Y, Westenbroek R, Mitchell R (1995) Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosi 15:6552-6561.
46. Mailleux P, Vanderhaeghen JJ (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655-668.
47. Mallet PE, Beninger RJ (1998) Delta9-tetrahydrocannabinol, but not the endogenous cannabinoid receptor ligand anandamide, produces conditioned place avoidance. Life Sci 62:2431-2439.
48. Maneuf YP, Crossman AR, Brotchie JM (1996) Modulation of GABAergic transmission in the globus pallidus by the synthetic cannabinoid WIN 55,212-2. Synapse 22:382-385.
49. Matsuda LA, Bonner TI (1995) Molecular biology of the cannabinoid receptor. In: Cannabinoid receptors (Pertwee RG, ed), pp 117-143. London: Academic.
50. 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.
51. Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550.
52. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
53. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61-65.
54. Navarro M, Hernandez E, Munoz RM, del Arco I, Villanua MA, Carrera MR, Rodriguez de Fonseca F (1997) Acute administration of the CB1 cannabinoid receptor antagonist SR 141716A induces anxiety-like responses in the rat. NeuroReport 8:491-496.
55. Nunzi MG, Gorio A, Milan F, Freund TF, Somogyi P, Smith AD (1985) Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus. J Comp Neurol 237:485-505.
56. Okada Y, Hassler R (1973) Uptake and release of T-aminobutyric acid (GABA) in slices of substantia nigra of rat. Brain Res 49:214-217.
57. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
58. Pacheco M, Childers SR, Arnold R, Casiano F, Ward SJ (1991) Aminoalkylindoles: actions on specific G protein-linked receptors. J Pharmacol Exp Ther 257:170-183.
59. Paton GS, Pertwee RG, Davies SN (1998) Correlation between cannabinoid mediated effects on paired pulse depression and induction of long term potentiation in the rat hippocampal slice. Neuropharmacology 37:1123-1130.
60. Penttonen M, Kamondi A, Acsády L, Buzsáki G (1998) Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 10:718-728.
61. Pertwee RG (1997) Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol Ther 74:129-180.
62. Pettit DA, Harrison MP, Olson JM, Spencer RF, Cabral GA (1998) Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J Neurosci Res 51:391-402.
63. Rinaldi-Carmona M, Barth F, Héaulme M, Shire D, Calandra B, Congy C, Martinez S, Maruani J, Néliat G, Caput D, Ferrara P, Soubrié P, Bréliere JC, Le Fur G (1994) SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 350:240-244.
64. Sagratella S, Pezzola A, Scotti de Carolis A (1986) An EEG investigation on nabilone, a synthetic cannabinoid, in rabbits. Pharmacol Res Commun 18:653-662.
65. Schlicker E, Timm J, Zentner J, Gothert M (1997) Cannabinoid CB1 receptor-mediated inhibition of noradrenaline release in the human and guinea-pig hippocampus. Naunyn Schmiedebergs Arch Pharmacol 356:583-589.
66. Shen M, Thayer SA (1998) The cannabinoid agonist Win55212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Res 783:77-84.
67. Shen M, Piser TM, Seybold VS, Thayer SA (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16:4322-4334.
68. Singh L, Lewis AS, Field MJ, Hughes J, Woodruff GN (1991) Evidence for an involvement of the brain cholecystokinin B receptor in anxiety. Proc Natl Acad Sci USA 88:1130-1133.
69. Soltész I, Deschenes M (1993) Low-and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70:97-116.
70. Stella N, Piomelli D (1998) Receptor-dependent formation of 2-arachidonylglycerol (2-AG), an endogenous cannabinoid ligand. Soc Neurosci Abstr 24:1245.
71. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778.
72. Szabó B, Dorner L, Pfreundtner C, Norenberg W, Starke K (1998) Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85:395-403.
73. Tsou K, Brown S, Sañudo-Peña MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393-411.
74. Tsou K, Mackie K, Sañudo-Peña MC, Walker JM (1999) Cannabinoid CB1 receptors are primarily localized on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience, in press.
75. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
76. Vardaris RM, Weisz DJ (1977) delta9-tetrahydrocannabinol and the hippocampus: effects on CA1 field potentials in rats. Brain Res Bull 2:181-187.
77. Vizi ES (1998) Different temperature dependence of carrier-mediated (cytoplasmic) and stimulus-evoked (exocytotic) release of transmitter: a simple method to separate the two types of release. Neurochem Int 33:359-366.
78. Vizi ES, Kiss JP (1998) Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and non-synaptic interactions. Hippocampus 8:566-607.
79. Ward SJ, Mastriani D, Casiano F, Arnold R (1990) Pravadoline: profile in isolated tissue preparations. J Pharmacol Exp Ther 255:1230-1239.
80. Weisz DJ, Gunnell DL, Teyler TJ, Vardaris RM (1982) Changes in hippocampal CA1 population spikes following administration of delta-9-THC. Brain Res Bull 8:155-162.
81. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
82. Willinsky MD, Scotti de Carolis A, Longo VG (1973) EEG and behavioral effects of natural, synthetic and biosynthetic cannabinoids. Psychopharmacologia 31:365-374.
83. Ylinen A, Soltész I, Bragin A, Penttonen M, Sík A, Buzsáki G (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.