Distinct cannabinoid sensitive receptors regulate hippocampal excitation and inhibition

Chemistry and Physics of Lipids

Volumn 121, Issue 1-2, 2002, Pages 73-82

  Hájos, Norbert ^a   Freund, Tamás F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

CB1 receptor; GABA; Glutamate; Hippocampus; Knockout; Vanilloid

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID; CANNABINOID RECEPTOR; GLUTAMIC ACID;

BRAIN FUNCTION; CONFERENCE PAPER; HIPPOCAMPUS; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; CANNABINOIDS; EVOKED POTENTIALS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; HUMANS; INTERNEURONS; MORPHOLINES; NAPHTHALENES; NEURAL INHIBITION; RECEPTORS, CANNABINOID; RECEPTORS, DRUG; RECEPTORS, GABA; RECEPTORS, GLUTAMATE; SYNAPTIC TRANSMISSION;

EID: 0037207070     PISSN: 00093084     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0009-3084(02)00149-4     Document Type: Conference Paper

References (55)

1. Alger B.E., Pitler T.A. Retrograde signaling at GABAA-receptor synapses in the mammalian CNS. Trends Neurosci. 18:1995;333-340.
2. Al-Hayani A., Wease K.N., Ross R.A., Pertwee R.G., Davies S.N. The endogenous cannabinoid anandamide activates vanilloid receptors in the rat hippocampal slice. Neuropharmacology. 41:2001;1000-1005.
3. Ameri A. The effects of cannabinoids on the brain. Prog. Neurobiol. 58:1999;315-348.
4. Ameri A., Wilhelm A., Simmet T. Effects of the endogeneous cannabinoid, anandamide, on neuronal activity in rat hippocampal slices. Br. J. Pharmacol. 126:1999;1831-1839.
5. Auclair N., Otani S., Soubrie P., Crepel F. Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J. Neurophysiol. 83:2000;3287-3293.
6. Bodor, A., Katona, I., Mackie, K., Freund, T.F., 2002. Cellular and subcellular localization of CB1 cannabinoid receptor in rat somatosensory cortex. FENS Abst. 112.5.
7. Bragin A., Penttonen M., Buzsaki G. Termination of epileptic after discharge in the hippocampus. J. Neurosci. 17:1997;2567-2579.
8. Breivogel C.S., Griffin G., Di Marzo V., Martin B.R. Evidence for a new G protein-coupled cannabinoid receptor in mouse brain. Mol. Pharmacol. 60:2001;155-163.
9. Calignano A., La Rana G., Giuffrida A., Piomelli D. Control of pain initiation by endogenous cannabinoids. Nature. 394:1998;277-281.
10. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 389:1997;816-824.
11. Diana M.A., Levenes C., Mackie K., Marty A. Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J. Neurosci. 22:2002;200-208.
12. Di Marzo V., Breivogel C.S., Tao Q., Bridgen D.T., Razdan R.K., Zimmer A.M., Zimmer A., Martin B.R. Levels, metabolism, and pharmacological activity of anandamide in CB(1) cannabinoid receptor knockout mice: evidence for non-CB(1), non-CB(2) receptor-mediated actions of anandamide in mouse brain. J. Neurochem. 75:2000;2434-2444.
13. Egertova M., Giang D.K., Cravatt B.F., Elphick M.R. A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc. R. Soc. Lond. B. Biol. Sci. 265:1998;2081-2085.
14. Eilers J., Konnerth A. Dendritic signal integration. Curr. Opin. Neurobiol. 7:1997;385-390.
15. Fagni L., Chavis P., Ango F., Bockaert J. Complex interactions between mGluRs, intracellular Ca2+ stores and ion channels in neurons. Trends Neurosci. 23:2000;80-88.
16. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 6:1996;347-470.
17. Hájos N., Freund T.F. Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology. 43:2002;503-510.
18. Hájos N., Katona I., Naiem S.S., MacKie K., Ledent C., Mody I., Freund T.F. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur. J. Neurosci. 12:2000;3239-3249.
19. Hájos N., Ledent C., Freund T.F. Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience. 106:2001;1-4.
20. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11:1991;563-583.
21. Hoffman A.F., Lupica C.R. Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. J. Neurosci. 20:2000;2470-2479.
22. Hosey M.M. Diversity of structure, signaling and regulation within the family of muscarinic cholinergic receptors. FASEB J. 6:1992;845-852.
23. Irving A.J., Coutts A.A., Harvey J., Rae M.G., Mackie K., Bewick G.S., Pertwee R.G. Functional expression of cell surface cannabinoid CB(1) receptors on presynaptic inhibitory terminals in cultured rat hippocampal neurons. Neuroscience. 98:2000;253-262.
24. Jarai Z., Wagner J.A., Varga K., Lake K.D., Compton D.R., Martin B.R., Zimmer A.M., Bonner T.I., Buckley N.E., Mezey E., Razdan R.K., Zimmer A., Kunos G. Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proc. Natl. Acad. Sci. USA. 96:1999;14136-14141.
25. Katona I., Sperlagh B., Sik A., Kafalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19:1999;4544-4558.
26. Katona I., Sperlagh B., Magloczky Z., Santha E., Kofalvi A., Czirjak S., Mackie K., Vizi E.S., Freund T.F. GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience. 100:2000;797-804.
27. Katona I., Rancz E.A., Acsády L., Ledent C., Mackie K., Hájos N., Freund T.F. Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J. Neurosci. 21:2001;9506-9518.
28. Kreitzer A.C., Regehr W.G. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J. Neurosci. 21:2001;RC174.
29. Kreitzer A.C., Regehr W.G. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron. 29:2001;717-727.
30. Kujtan P.W., Carlen P.L., Kapur B.M. delta 9-Tetrahydrocannabinol and cannabidiol: dose-dependent effects on evoked potentials in the hippocampal slice. Can. J. Physiol. Pharmacol. 61:1983;420-426.
31. Llano I., Leresche N., Marty A. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron. 6:1991;565-574.
32. Maejima T., Hashimoto K., Yoshida T., Aiba A., Kano M. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron. 31:2001;463-475.
33. Marsicano G., Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 11:1999;4213-4225.
34. McDonald A.J., Mascagni F. Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons. Neuroscience. 107:2001;641-652.
35. Misner D.L., Sullivan J.M. Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J. Neurosci. 19:1999;6795-6805.
36. Nakamura T., Barbara J.G., Nakamura K., Ross W.N. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron. 24:1999;727-737.
37. Ohno-Shosaku T., Maejima T., Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron. 29:2001;729-738.
38. Ohno-Shosaku T., Shosaku J., Tsubokawa H., Kano M. Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur. J. Neurosci. 15:2002;953-961.
39. Ohno-Shosaku T., Tsubokawa H., Mizushima I., Yoneda N., Zimmer A., Kano M. Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J. Neurosci. 22:2002;3864-3872.
40. Paton G.S., Pertwee R.G., Davies S.N. Correlation between cannabinoid mediated effects on paired pulse depression and induction of long term potentiation in the rat hippocampal slice. Neuropharmacology. 37:1998;1123-1130.
41. Pitler T.A., Alger B.E. Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J. Neurosci. 12:1992;4122-4132.
42. Shen M., Piser T.M., Seybold V.S., Thayer S.A. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J. Neurosci. 16:1996;4322-4334.
43. Sullivan J.M. Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J. Neurophysiol. 82:1999;1286-1294.
44. Szabo B., Dorner L., Pfreundtner C., Norenberg W., Starke K. Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience. 85:1998;395-403.
45. Takahashi K.A., Linden D.J. Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J. Neurophysiol. 83:2000;1167-1180.
46. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 83:1998;393-411.
47. Tsou K., Mackie K., Sanudo-Pena M.C., Walker J.M. Cannabinoid CB1 receptors are localized primarily on cholecystokinin- containing GABAergic interneurons in the rat hippocampal formation. Neuroscience. 93:1999;969-975.
48. Tsubokawa H., Ross W.N. Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci. 17:1997;5782-5791.
49. Twitchell W., Brown S., Mackie K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J. Neurophysiol. 78:1997;43-50.
50. Varma N., Carlson G.C., Ledent C., Alger B.E. Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J. Neurosci. 4:2001;4.
51. Weisz D.J., Gunnell D.L., Teyler T.J., Vardaris R.M. Changes in hippocampal CA1 population spikes following administration of delta-9-THC. Brain Res. Bull. 8:1982;155-162.
52. Wilson R.I., Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 410:2001;588-592.
53. Wilson R.I., Kunos G., Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron. 31:2001;453-462.
54. Woodson W., Nitecka L., Ben-Ari Y. Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study. J. Comp. Neurol. 280:1989;254-271.
55. Zygmunt P.M., Petersson J., Andersson D.A., Chuang H., Sorgard M., Di Marzo V., Julius D., Hogestatt E.D. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature. 400:1999;452-457.