MGluR-mediated and endocannabinoid-dependent long-term depression in the hilar region of the rat dentate gyrus

Neuropharmacology

Volumn 58, Issue 4-5, 2010, Pages 712-721

  Nahir, Ben ^b   Lindsly, Casie ^b   Frazier, Charles J ^a,b  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Dentate gyrus; Electrophysiology; Endocannabinoids; LTD; MGluRs; Synaptic plasticity

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; METABOTROPIC RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DEPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; MALE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; DENTATE GYRUS; ENDOCANNABINOIDS; INHIBITORY POSTSYNAPTIC POTENTIALS; LONG-TERM SYNAPTIC DEPRESSION; MALE; METHOXYHYDROXYPHENYLGLYCOL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 77649338337     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2009.12.022     Document Type: Article

References (51)

1. Acsady L., Katona I., Martinez-Guijarro F.J., Buzsaki G., Freund T.F. Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J. Neurosci. 2000, 20:6907-6919.
2. Adermark L., Lovinger D.M. Frequency-dependent inversion of net striatal output by endocannabinoid-dependent plasticity at different synaptic inputs. J. Neurosci. 2009, 29:1375-1380.
3. Azad S.C., Monory K., Marsicano G., Cravatt B.F., Lutz B., Zieglgansberger W., Rammes G. Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J. Neurosci. 2004, 24:9953-9961.
4. Bender V.A., Bender K.J., Brasier D.J., Feldman D.E. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J. Neurosci. 2006, 26:4166-4177.
5. Chevaleyre V., Castillo P.E. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 2003, 38:461-472.
6. Chevaleyre V., Castillo P.E. Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 2004, 43:871-881.
7. Chevaleyre V., Takahashi K.A., Castillo P.E. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 2006, 29:37-76.
8. Chiu C.Q., Castillo P.E. Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus. Neuropharmacology 2008, 54:68-78.
9. Edwards D.A., Kim J., Alger B.E. Multiple mechanisms of endocannabinoid response initiation in hippocampus. J. Neurophysiol. 2006, 95:67-75.
10. Edwards D.A., Zhang L., Alger B.E. Metaplastic control of the endocannabinoid system at inhibitory synapses in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8142-8147.
11. Frazier C.J., Strowbridge B.W., Papke R.L. Nicotinic receptors on local circuit neurons in dentate gyrus: a potential role in regulation of granule cell excitability. J. Neurophysiol. 2003, 89:3018-3028.
12. Galante M., Diana M.A. Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. J. Neurosci. 2004, 24:4865-4874.
13. Gerdeman G.L., Ronesi J., Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 2002, 5:446-451.
14. 2+ dependency for triggering retrograde endocannabinoid signal. Neuron 2005, 45:257-268.
15. Heifets B.D., Chevaleyre V., Castillo P.E. Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10250-10255.
16. Henneberger C., Redman S.J., Grantyn R. Cortical efferent control of subcortical sensory neurons by synaptic disinhibition. Cereb. Cortex 2007, 17:2039-2049.
17. Hofmann M.E., Nahir B., Frazier C.J. Endocannabinoid-mediated depolarization-induced suppression of inhibition in hilar mossy cells of the rat dentate gyrus. J. Neurophysiol. 2006, 96:2501-2512.
18. Hofmann M.E., Nahir B., Frazier C.J. Excitatory afferents to CA3 pyramidal cells display differential sensitivity to CB1 dependent inhibition of synaptic transmission. Neuropharmacology 2008, 55:1140-1146.
19. Howard A.L., Neu A., Morgan R.J., Echegoyen J.C., Soltesz I. Opposing modifications in intrinsic currents and synaptic inputs in post-traumatic mossy cells: evidence for single-cell homeostasis in a hyperexcitable network. J. Neurophysiol. 2007, 97:2394-2409.
20. Huang L., Rowan M.J., Anwyl R. Induction of long-lasting depression by (+)-alpha-methyl-4-carboxyphenylglycine and other group II mGlu receptor ligands in the dentate gyrus of the hippocampus in vitro. Eur. J. Popul. 1999, 366:151-158.
21. Huang Y., Yasuda H., Sarihi A., Tsumoto T. Roles of endocannabinoids in heterosynaptic long-term depression of excitatory synaptic transmission in visual cortex of young mice. J. Neurosci. 2008, 28:7074-7083.
22. Kano M., Ohno-Shosaku T., Hashimotodani Y., Uchigashima M., Watanabe M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 2009, 89:309-380.
23. 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. 1999, 19:4544-4558.
24. Kawamura Y., Fukaya M., Maejima T., Yoshida T., Miura E., Watanabe M., Ohno-Shosaku T., Kano M. The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J. Neurosci. 2006, 26:2991-3001.
25. Kreitzer A.C., Malenka R.C. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci. 2005, 25:10537-10545.
26. Kreitzer A.C., Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 2007, 445:643-647.
27. Larimer P., Strowbridge B.W. Nonrandom local circuits in the dentate gyrus. J. Neurosci. 2008, 28:12212-12223.
28. Lovinger D.M. Presynaptic modulation by endocannabinoids. Handb. Exp. Pharmacol. 2008, 435-477.
29. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgansberger W., Di Marzo V., Lutz B. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002, 418:530-534.
30. Melis M., Pistis M., Perra S., Muntoni A.L., Pillolla G., Gessa G.L. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J. Neurosci. 2004, 24:53-62.
31. Nahir B., Bhatia C., Frazier C.J. Presynaptic inhibition of excitatory afferents to hilar mossy cells. J. Nephrol. 2007, 97:4036-4047.
32. Naie K., Tsanov M., Manahan-Vaughan D. Group I metabotropic glutamate receptors enable two distinct forms of long-term depression in the rat dentate gyrus in vivo. Eur. J. Neurosci. 2007, 25:3264-3275.
33. 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. 2002, 15:953-961.
34. Pan B., Hillard C.J., Liu Q.S. Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J. Neurosci. 2008, 28:1385-1397.
35. Robbe D., Kopf M., Remaury A., Bockaert J., Manzoni O.J. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:8384-8388.
36. Rodriguez-Moreno A., Paulsen O. Spike timing-dependent long-term depression requires presynaptic NMDA receptors. Nat. Neurosci. 2008, 11:744-745.
37. Scharfman H.E. Characteristics of spontaneous and evoked EPSPs recorded from dentate spiny hilar cells in rat hippocampal slices. J. Nephrol. 1993, 70:742-757.
38. Scharfman H.E. Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J. Neurophysiol. 1994, 72:2167-2180.
39. Sergeeva O.A., Doreulee N., Chepkova A.N., Kazmierczak T., Haas H.L. Long-term depression of cortico-striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis. Eur. J. Neurosci. 2007, 26:1889-1894.
40. Singla S., Kreitzer A.C., Malenka R.C. Mechanisms for synapse specificity during striatal long-term depression. J. Neurosci. 2007, 27:5260-5264.
41. Sjostrom P.J., Turrigiano G.G., Nelson S.B. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 2003, 39:641-654.
42. Soler-Llavina G.J., Sabatini B.L. Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat. Neurosci. 2006, 9:798-806.
43. Strowbridge B.W., Buckmaster P.S., Schwartzkroin P.A. Potentiation of spontaneous synaptic activity in rat mossy cells. Neurosci. Lett. 1992, 142:205-210.
44. Trommer B.L., Liu Y.B., Pasternak J.F. Long-term depression at the medial perforant path-granule cell synapse in developing rat dentate gyrus. Brain Res. Dev. Brain Res. 1996, 96:97-108.
45. 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 1999, 93:969-975.
46. Tzounopoulos T., Rubio M.E., Keen J.E., Trussell L.O. Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity. Neuron 2007, 54:291-301.
47. Varma N., Carlson G.C., Ledent C., Alger B.E. Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J. Neurosci. 2001, 21:RC188.
48. Wang Z., Kai L., Day M., Ronesi J., Yin H.H., Ding J., Tkatch T., Lovinger D.M., Surmeier D.J. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 2006, 50:443-452.
49. Williams P.A., Larimer P., Gao Y., Strowbridge B.W. Semilunar granule cells: glutamatergic neurons in the rat dentate gyrus with axon collaterals in the inner molecular layer. J. Neurosci. 2007, 27:13756-13761.
50. Wilson R.I., Kunos G., Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 2001, 31:453-462.
51. Yasuda H., Huang Y., Tsumoto T. Regulation of excitability and plasticity by endocannabinoids and PKA in developing hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3106-3111.