Cannabinoid-mediated inhibition of recurrent excitatoryCircuitry in the dentate gyrus in a mouse model of temporal lobe epilepsy

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Bhaskaran, Muthu D ^a,b   Smith, Bret N ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Tulane University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2 ARACHYDONOYLGLYCEROL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AGONIST; GLUTAMIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CELL ACTIVATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG MECHANISM; ELECTROSTIMULATION; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPUS; MALE; MOSSY FIBER; MOUSE; NERVE ENDING; NONHUMAN; PHOTOLYSIS; RECEPTOR UPREGULATION; TEMPORAL LOBE EPILEPSY; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; ARACHIDONIC ACIDS; BLOTTING, WESTERN; CANNABINOIDS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; EPILEPSY, TEMPORAL LOBE; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; MALE; MICE; MOSSY FIBERS, HIPPOCAMPAL; PHOTOLYSIS; PILOCARPINE; POLYUNSATURATED ALKAMIDES; RECEPTOR, CANNABINOID, CB1; STATUS EPILEPTICUS; SYNAPSES;

ANIMALIA; MUS;

EID: 77956533692     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010683     Document Type: Article

References (64)

1. Dudek FE, Spitz M (1997) Hypothetical mechanisms for the cellular and neurophysiologic basis of secondary epileptogenesis: proposed role of synaptic reorganization. J Clin Neurophysiol 14: 90-101.
2. Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolicmapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6: 1361-1391.
3. Nadler JV, Perry BW, Cotman CW (1980) Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res 182: 1-9.
4. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5: 1016-1022.
5. Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14: 375-403.
6. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF (1991) Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42: 351-363.
7. Shibley H, Smith BN (2002) Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res 49: 109-120.
8. Winokur RS, Kubal T, Liu D, Davis SF, Smith BN (2004) Recurrent excitation in the dentate gyrus of a murine model of temporal lobe epilepsy. Epilepsy Res 58: 93-105.
9. Patrylo PR, Dudek FE (1998) Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J Neurophysiol 79: 418-429.
10. Wuarin JP, Dudek FE (1996) Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainatetreated epileptic rats. J Neurosci 16: 4438-4448.
11. Cronin J, Dudek FE (1988) Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 474: 181-184.
12. Wuarin JP, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85: 1067-1077.
13. Lynch M, Sutula T (2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83: 693-704.
14. Smith BN, Dudek FE (1997) Enhanced population responses in the basolateral amygdala of kainate-treated, epileptic rats in vitro. Neurosci Lett 222: 1-4.
15. Smith BN, Dudek FE (2001) Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J Neurophysiol 85: 1-9.
16. Nakajima S, Franck JE, Bilkey D, Schwartzkroin PA (1991) Local circuit synaptic interactions between CA1 pyramidal cells and interneurons in the kainate-lesioned hyperexcitable hippocampus. Hippocampus 1: 67-78.
17. Perez Y, Morin F, Beaulieu C, Lacaille JC (1996) Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 8: 736-748.
18. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, et al. (1999) Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J Neurosci 19: 2987-2995.
19. Baker D, Pryce G (2003) The therapeutic potential of cannabis in multiple sclerosis. Expert Opin Investig Drugs 12: 561-567.
20. Mechoulam R, Panikashvili D, Shohami E (2002) Cannabinoids and brain injury: therapeutic implications. Trends Mol Med 8: 58-61.
21. Walter L, Stella N (2004) Cannabinoids and neuroinflammation. Br J Pharmacol 141: 775-785.
22. Gordon E, Devinsky O (2001) Alcohol and marijuana: effects on epilepsy and use by patients with epilepsy. Epilepsia 42: 1266-1272.
23. 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.
24. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, et al. (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19: 4544-4558.
25. Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, et al. (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21: 9506-9518.
26. 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.
27. Foldy C, Neu A, Jones MV, Soltesz I (2006) Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release. J Neurosci 26: 1465-1469.
28. Tsou K, Mackie K, Sanudo-Pena MC, Walker JM (1999) Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 93: 969-975.
29. Falenski KW, Blair RE, Sim-Selley LJ, Martin BR, DeLorenzo RJ (2007) Status epilepticus causes a long-lasting redistribution of hippocampal cannabinoid type 1 receptor expression and function in the rat pilocarpine model of acquired epilepsy. Neuroscience 146: 1232-1244.
30. Ludanyi A, Eross L, Czirjak S, Vajda J, Halasz P, et al. (2008) Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 28: 2976-2990.
31. Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ (2003) The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther 307: 129-137.
32. Deshpande LS, Sombati S, Blair RE, Carter DS, Martin BR, et al. (2007) Cannabinoid CB1 receptor antagonists cause status epilepticus-like activity in the hippocampal neuronal culture model of acquired epilepsy. Neurosci Lett 411: 11-16.
33. Braakman HMH, van Oostenbrugge RJ, van Kranen-Mastenbroek VHJM, de Krom MCTFM (2009) Rimonabant induces partial seizures in a patient with a history of generalized epilepsy. Epilepsia 50: 1.
34. Racine R, Okujava V, Chipashvili S (1972) Modification of seizure activity by electrical stimulation. 3. Mechanisms. Electroencephalogr Clin Neurophysiol 32: 295-299.
35. Callaway EM, Katz LC (1993) Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc Natl Acad Sci U S A 90: 7661-7665.
36. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495: 387-395.
37. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, et al. (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10: 267-282.
38. Magloczky Z, Wittner L, Borhegyi Z, Halasz P, Vajda J, et al. (2000) Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 96: 7-25.
39. Mathern GW, Babb TL, Pretorius JK, Leite JP (1995) Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci 15: 3990-4004.
40. Sloviter RS, Sollas AL, Barbaro NM, Laxer KD (1991) Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308: 381-396.
41. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L (1989) Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26: 321-330.
42. Zhu ZQ, Armstrong DL, Hamilton WJ, Grossman RG (1997) Disproportionate loss of CA4 parvalbumin-immunoreactive interneurons in patients with Ammon's horn sclerosis. J Neuropathol Exp Neurol 56: 988-998.
43. Borges K, Gearing M, McDermott DL, Smith AB, Almonte AG, et al. (2003) Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp Neurol 182: 21-34.
44. Epsztein J, Represa A, Jorquera I, Ben-Ari Y, Crepel V (2005) Recurrent mossy fibers establish aberrant kainate receptor-operated synapses on granule cells from epileptic rats. J Neurosci 25: 8229-8239.
45. Tu B, Timofeeva O, Jiao Y, Nadler JV (2005) Spontaneous release of neuropeptide Y tonically inhibits recurrent mossy fiber synaptic transmission in epileptic brain. J Neurosci 25: 1718-1729.
46. Swartzwelder HS, Lewis DV, Anderson WW, Wilson WA (1987) Seizure-like events in brain slices: suppression by interictal activity. Brain Res 410: 362-366.
47. Smith BN, Dudek FE (2002) Network interactions mediated by new excitatory connections between CA1 pyramidal cells in rats with kainate-induced epilepsy. J Neurophysiol 87: 1655-1658.
48. Chiu CQ, Castillo PE (2008) Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus. Neuropharmacology 54: 68-78.
49. Buckmaster PS, Strowbridge BW, Kunkel DD, Schmiege DL, Schwartzkroin PA (1992) Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2: 349-362.
50. Scharfman HE (1994) Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J Neurophysiol 72: 2167-2180.
51. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410: 588-592.
52. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296: 678-682.
53. Wallace MJ, Martin BR, DeLorenzo RJ (2002) Evidence for a physiological role of endocannabinoids in the modulation of seizure threshold and severity. Eur J Pharmacol 452: 295-301.
54. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, et al. (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302: 84-88.
55. Buckmaster PS, Dudek FE (1997) Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385: 385-404.
56. Chen K, Neu A, Howard AL, Foldy C, Echegoyen J, et al. (2007) Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. J Neurosci 27: 46-58.
57. Chen K, Ratzliff A, Hilgenberg L, Gulyas A, Freund TF, et al. (2003) Long-term plasticity of endocannabinoid signaling induced by developmental febrile seizures. Neuron 39: 599-611.
58. Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, et al. (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239-3249.
59. Kawamura Y, Fukaya M, Maejima T, Yoshida T, Miura E, et al. (2006) The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26: 2991-3001.
60. 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.
61. Katona I, Sperlagh B, Magloczky Z, Santha E, Kofalvi A, et al. (2000) GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 100: 797-804.
62. Hendriksen H, Datson NA, Ghijsen WE, van Vliet EA, da Silva FH, et al. (2001) Altered hippocampal gene expression prior to the onset of spontaneous seizures in the rat post-status epilepticus model. Eur J Neurosci 14: 1475-1484.
63. Cristino L, de Petrocellis L, Pryce G, Baker D, Guglielmotti V, et al. (2006) Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139: 1405-1415.
64. Bhaskaran M, Smith B (2010) Effects of TRPV1 activation on synaptic excitation in the dentate gyrus of a mouse model of temporal lobe epilepsy. Exp Neurol PMID: 20144892.