Endogenous ACh effects on NMDA-induced interictal-like discharges along the septotemporal hippocampal axis of adult rats and their modulation by an early life generalized seizure

Epilepsia

Volumn 53, Issue 5, 2012, Pages 879-887

  Mikroulis, Apostolos V ^a   Psarropoulou, Caterina ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

Author keywords

Atropine; Brain; Epileptiform discharges; Eserine; Interictal; Muscarinic receptors; NMDA receptors; Seizures; Spontaneous discharges

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOPYRIDINE; ACETYLCHOLINE; ATROPINE; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PENTETRAZOLE; PHYSOSTIGMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; CEREBROSPINAL FLUID; CONTROLLED STUDY; DRUG MECHANISM; EPILEPTIC DISCHARGE; FEMALE; GRAND MAL SEIZURE; HIPPOCAMPUS; MALE; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ANALYSIS OF VARIANCE; ANIMALS; ATROPINE; CHOLINESTERASE INHIBITORS; CONVULSANTS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HIPPOCAMPUS; MALE; MUSCARINIC ANTAGONISTS; N-METHYLASPARTATE; NEURONS; PENTYLENETETRAZOLE; PHYSOSTIGMINE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SEX FACTORS; VALINE;

EID: 84860657352     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2012.03440.x     Document Type: Article

References (93)

1. Acquas E, Wilson C, Fibiger H,. (1996) Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation and fear. J Neurosci 16: 3089-3096.
2. Alger BE, Dhanjal SS, Dingledine R, Garthwaite J, Henderson G, King GL, Lipton P, North A, Schwartzkroin PA, Sears TA, Segal M, Whittingham TS, Williams J,. (1984) Brain slice methods. In, Dingledine R, (Ed.) Brain slices. Plenum Press, New York, pp. 381-437.
3. Avoli M, Barbarosie M,. (1999) Interictal-ictal interactions and limbic seizure generation. Rev Neurol (Paris) 155: 468-471.
4. Avoli M, D'Antuono M, Louvel J, Köhling R, Biagini G, Pumain R, D'Arcangelo G, Tancredi V,. (2002) Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol 68: 167-207.
5. Binnie CD,. (2003) Cognitive impairment during epileptiform discharges: is it ever justifiable to treat the EEG? Lancet Neurol 2: 725-730.
6. Borck C, Jefferys JG,. (1999) Seizure-like events in disinhibited ventral slices of adult rat hippocampus. J Neurophysiol 82: 2130-2142.
7. Bragdon AC, Kojima H, Wilson WA,. (1992) Suppression of interictal bursting in hippocampus unleashes seizures in entorhinal cortex: a proepileptic effect of lowering [K+]o and raising [Ca2+]o. Brain Res 590: 128-135.
8. Bridgers SL,. (1987) Epileptiform abnormalities discovered on electroencephalographic screening of psychiatric inpatients. Arch Neurol 44: 312-316.
9. Brito GNO, Davis BJ, Stopp LC, Stanton ME,. (1983) Memory and the septo-hippocampal cholinergic system in the rat. Psychopharmacology 81: 315-320.
10. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G,. (1998) Endogenous ACh enhances striatal NMDA-responses via M1-like muscarinic receptors and PKC activation. Eur J Neurosci 10: 2887-2895.
11. Chrobak JJ, Buzsaki G,. (1994) Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14: 6160-6170.
12. Chrobak JJ, Lorincz A, Buzsaki G,. (2000) Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus 10: 457-465.
13. Daniel JM, Dohanich GP,. (2001) Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 21: 6949-6956.
14. Delatour B, Witter MP,. (2002) Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur J Neurosci 15: 1400-1407.
15. Derchansky M, Shahar E, Wennberg RA, Samoilova M, Jahromi SS, Abdelmalik PA, Zhang L, Carlen PL,. (2004) Model of frequent, recurrent, and spontaneous seizures in the intact mouse hippocampus. Hippocampus 14: 935-947.
16. Dolorfo CL, Amaral DG,. (1998) Entorhinal cortex of the rat: organization of intrinsic connections. J Comp Neurol 398: 49-82.
17. Elul R,. (1964) Regional differences in the hippocampus of the cat. Electroencephalogr Clin Neurophysiol 16: 470-488.
18. Fanselow MS, Dong H-W,. (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65: 7-19.
19. Fonseca LC, Tedrus GM, Moraes C, Vicente Machado A, Almeida MP, Oliveira DO,. (2008) Epileptiform abnormalities and quantitative EEG in children with attention-deficit/hyperactivity disorder. Arq Neuropsiquiatr 66: 462-467.
20. Fontán-Lozano A, Suárez-Pereira I, González-Forero D, Carriõn AM,. (2011) The A-current modulates learning via NMDA receptors containing the NR2B subunit. PLoS One 6 (9): e24915.
21. Gage FH, Thompson RG,. (1980) Differential distribution of norepinephrine and serotonin along the dorsal-ventral axis of the hippocampal formation. Brain Res Bull 5: 771-773.
22. Galvan M, Grafe P, ten Bruggencate G,. (1982) Convulsant actions of 4-aminopyridine on the guinea-pig olfactory cortex slice. Brain Res 241: 75-86.
23. Gardner C, Webster R,. (1977) Convulsant-anticonvulsant interactions on seizure activity and cortical acetylcholine release. Eur J Pharmacol 42: 247-256.
24. Gilbert M, Racine RJ, Smith GK,. (1985) Epileptiform burst responses in ventral vs dorsal hippocampal slices. Brain Res 361: 389-391.
25. Gray R, Rajan A, Radcliffe K, Yakehiro M, Dani J,. (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716.
26. Grybko M, Sharma G, Vijayaraghavan S,. (2010) Functional distribution of nicotinic receptors in CA3 region of the hippocampus. J Mol Neurosci 40: 114-120.
27. Gu Y, Ge SY, Ruan DY,. (2004) Effect of 4-aminopyridine on synaptic transmission in rat hippocampal slices. Brain Res 1006: 225-232.
28. Gulyas-Kovacs A, Doczi J, Tarnawa I, Detari L, Banczerowski-Pelyhe I, Vilagi I,. (2002) Comparison of spontaneous and evoked epileptiform activity in three in vitro epilepsy models. Brain Res 945: 174-180.
29. Hamilton SE, Loose MD, Qi M, Levey AI, Hille B, McKnight GS, Idzerda RL, Nathanson NM,. (1997) Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. PNAS 94: 13311-13316.
30. Harata N, Ebihara S, Akaike N,. (1992) Modulation of NMDA receptors by ACh in the central nervous system. Prog Neuropsychopharmacol Biol Psychiatry 16: 977-984.
31. Huang RQ, Bell-Horner CL, Dibas MI, Covey DF, Drewe JA, Dillon GH,. (2001) Pentylenetetrazole-induced inhibition of recombinant gamma-aminobutyric acid type A (GABA(A)) receptors: mechanism and site of action. J Pharmacol Exp Ther 298: 986-995.
32. Imperato A, Dazzi L, Carta G, Colombo G, Biggio G,. (1998) Rapid increase in basal acetylcholine release in the hippocampus of freely moving rats induced by withdrawal from long-term ethanol intoxication. Brain Res 784: 347-350.
33. Inui K, Motomura E, Okushima R, Kaige H, Inoue K, Nomura J,. (1998) Electroencephalographic findings in patients with DSM-IV mood disorder, schizophrenia, and other psychotic disorders. Biol Psychiatry 43: 69-75.
34. James JR, Villanueva HF, Johnson JH, Arezo S, Rosecrans JA,. (1994) Evidence that nicotine can acutely desensitize central nicotinic acetylcholinergic receptors. Psychopharmacology (Berl) 114: 456-462.
35. Jensen MS, Yaari Y,. (1988) The relationship between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Ann Neurol 24: 591-598.
36. Joyce JN, Gibbs RB, Cotman CW, Marshall JF,. (1989) Regulation of muscarinic receptors in hippocampus following cholinergic denervation and reinnervation by septal and striatal transplants. J Neurosci 9: 2776-2791.
37. Kametani H, Kawamura H,. (1990) Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis. Life Sci 47: 421-426.
38. Kerr KM, Agster KL, Furtak SC, Burwell RD,. (2007) Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 17: 697-708.
39. Kleen JK, Scott RC, Holmes GL, Lenck-Santini PP,. (2010) Hippocampal interictal spikes disrupt cognition in rats. Ann Neurol 67: 250-257.
40. Kojima H, Kowada M, Bragdon AC,. (1991) Mechanism of electrographic seizure generation in the rat brain slice in low magnesium medium: modulatory effect of interictal bursting on seizure generation. Jpn J Psychiatry Neurol 45: 279-283.
41. Lapchak P, Araujo D, Quirion R, Beaudet A,. (1990) Chronic estradiol treatment alters central cholinergic function in the female rat: effect on choline acetyltransferase activity, acetylcholine content, and nicotinic autoreceptor function. Brain Res 525: 249-255.
42. Lee KS, Reddington M, Schubert P, Kreutzberg G,. (1983) Regulation of the strength of adenosine modulation in the hippocampus by a differential distribution of the density of A1 receptors. Brain Res 260: 156-159.
43. Lewis DV, Jones LS, Mott DD,. (1990) Hippocampal epileptiform activity induced by magnesium-free medium: differences between areas CA1 and CA2-3. Epilepsy Res 6: 95-101.
44. Li B, Duysen EG, Volpicelli-Daley LA, Levey AI, Lockridge O,. (2003) Regulation of muscarinic acetylcholine receptor function in acetylcholinesterase knockout mice. Pharmacol Biochem Behav 74: 977-986.
45. Liu J, Rasul I, Sun Y, Wu G, Li L, Premont RT, Suo WZ,. (2009) GRK5 deficiency leads to reduced hippocampal acetylcholine level via impaired presynaptic M2/M4 autoreceptor desensitization. J Biol Chem 284: 19564-19571.
46. Lopantsev V, Avoli M,. (1998) Participation of GABAA-mediated inhibition in ictallike discharges in the rat entorhinal cortex. J Neurophysiol 79: 352-360.
47. Lu WY, Xiong ZG, Lei S, Orser BA, Dudek E, Browning MD, MacDonald JF,. (1999) G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat Neurosci 2: 331-338.
48. Marino MJ, Rouse ST, Levey AI, Potter LT, Conn PJ,. (1998) Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. PNAS 95: 11465-11470.
49. Markram H, Segal M,. (1992) The inositol 1,4,5-trisphosphate pathway mediates cholinergic potentiation of rat hippocampal neuronal responses to NMDA. J Physiol 447: 513-533.
50. Marrosu F, Portas C, Mascia MS, Casu MA, Fá M, Giagheddu M, Imperato A, Gessa GL,. (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671: 329-332.
51. Meilleur S, Carmant L, Psarropoulou C,. (2000) Immature rat convulsions and long term effects on hippocampal cholinergic neurotransmission. Neuroreport 11: 521-524.
52. Meilleur S, Aznavour N, Descarries L, Carmant L, Mamer OA, Psarropoulou C,. (2003) Pentylenetetrazol-induced seizures in immature rats provoke long-term changes in adult hippocampal cholinergic excitability. Epilepsia 44: 507-517.
53. Mitsushima D, Takase K, Funabashi T, Kimura F,. (2008) Gonadal steroid hormones maintain the stress-induced acetylcholine release in the hippocampus: simultaneous measurements of the extracellular acetylcholine and serum corticosterone levels in the same subjects. Endocrinology 149: 802-811.
54. Moor E, Schirm E, Jacso J, Westerink B,. (1998) Involvement of medial septal glutamate and GABAA receptors in behaviour-induced acetylcholine release in the hippocampus: a dual probe microdialysis study. Brain Res 789: 1-8.
55. Moser MB, Moser EI,. (1998) Functional differentiation in the hippocampus. Hippocampus 8: 608-619.
56. Nicoll RA,. (1985) The septo-hippocampal projection: a model cholinergic pathway. Trends Neurosci 8: 533-536.
57. Ogita K, Okuda H, Watanabe M, Nagashima R, Sugiyama C, Yoneda Y,. (2005) In vivo treatment with the K+ channel blocker 4-aminopyridine protects against kainate-induced neuronal cell death through activation of NMDA receptors in murine hippocampus. Neuropharmacology 48: 810-821.
58. Olson IR, Berryhill M,. (2009) Some surprising findings on the involvement of the parietal lobe in human memory. Neurobiol Learn Mem 91: 155-165.
59. áztekin I, McElree B, Staresina BP, Davachi L,. (2011) Working memory retrieval: contributions of the left prefrontal cortex, the left posterior parietal cortex, and the hippocampus. J Cogn Neurosci 21: 581-593.
60. Pandis C, Sotiriou E, Kouvaras E, Asprodini E, Papatheodoropoulos C, Angelatou F,. (2006) Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus. Neuroscience 140: 163-175.
61. Papatheodoropoulos C, Kostopoulos G,. (2000a) Decreased ability of rat temporal hippocampal CA1 region to produce long-term potentiation. Neurosci Lett 279: 177-180.
62. Papatheodoropoulos C, Kostopoulos G,. (2000b) Dorsal-ventral differentiation of short-term synaptic plasticity in rat CA1 hippocampal region. Neurosci Lett 286: 57-60.
63. Papatheodoropoulos C, Asprodini E, Nikita I, Koutsona C, Kostopoulos G,. (2002) Weaker synaptic inhibition in CA1 region of ventral compared to dorsal rat hippocampal slices. Brain Res 948: 117-121.
64. Papatheodoropoulos C, Moschovos C, Kostopoulos G,. (2005) Greater contribution of N-methyl-d-aspartic acid receptors in ventral compared to dorsal hippocampal slices in the expression and long-term maintenance of epileptiform activity. Neuroscience 135: 765-779.
65. Pena F, Tapia R,. (2000) Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 101: 547-561.
66. Perreault P, Avoli M,. (1991) Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J Neurophysiol 65: 771-785.
67. Perreault P, Avoli M,. (1992) 4-aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus. J Neurosci 12: 104-115.
68. Pillmann F, Rohde A, Ullrich S, Draba S, Sannemuller U, Marneros A,. (1999) Violence, criminal behavior, and the EEG: significance of left hemispheric focal abnormalities. J Neuropsychiatry Clin Neurosci 11: 454-457.
69. Potier S, J S, Chabot JG, Psarropoulou C, Descarries L,. (2005) A pentylenetetrazole-induced generalized seizure in early life enhances the efficacy of muscarinic receptor coupling to G-protein in hippocampus and neocortex of adult rat. Eur J Neurosci 21: 1828-1836.
70. Pressler RM, Robinson RO, Wilson GA, Binnie CD,. (2005) Treatment of interictal epileptiform discharges can improve behavior in children with behavioral problems and epilepsy. J Pediatr 146: 112-117.
71. Psarropoulou C, Avoli M,. (1992) CPP, an NMDA-receptor antagonist, blocks 4-aminopyridine-induced spreading depression episodes but not epileptiform activity in immature rat hippocampal slices. Neurosci Lett 135: 139-143.
72. A-mediated inhibition induces synchronous epileptiform activity in immature rat hippocampus. Neuroscience 82: 1067-1077.
73. Racine RJ,. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
74. Racine R, Rose PA, Burnham WM,. (1977) Afterdischarge thresholds and kindling rates in dorsal and ventral hippocampus and dentate gyrus. Can J Neurol Sci 4: 273-278.
75. Ragozzino ME, Unick KE, Gold PE,. (1996) Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. PNAS 93: 4693-4698.
76. Rakhade SN, Shah AK, Agarwal R, Yao B, Asano E, Loeb JA,. (2007) Activity-dependent gene expression correlates with interictal spiking in human neocortical epilepsy. Epilepsia 48 (Suppl. 5): 86-95.
77. Ramanjaneyulu R, Ticku MK,. (1984) Interactions of pentamethylenetetrazole and tetrazole analogues with the picrotoxinin site of the benzodiazepine-GABA receptor-ionophore complex. Eur J Pharmacol 98: 337-345.
78. Richer LP, Shevell MI, Rosenblatt BR,. (2002) Epileptiform abnormalities in children with attention-deficit-hyperactivity disorder. Pediatr Neurol 26: 125-129.
79. Schurr A, Reid KH, Tseng MT, Edmonds HL Jr,. (1984) The stability of the hippocampal slice preparation: an electrophysiological and ultrastructural analysis. Brain Res 297: 357-362.
80. Schwarcz R, Witter MP,. (2002) Memory impairment in temporal lobe epilepsy: the role of entorhinal lesions. Epilepsy Res 50: 161-177.
81. Segal M,. (1992) Acetylcholine enhances NMDA-evoked calcium rise in hippocampal neurons. Brain Res 587: 83-87.
82. Silvestri R, Gagliano A, Calarese T, Arico I, Cedro C, Condurso R, Germano E, Vita G, Tortorella G,. (2007) Ictal and interictal EEG abnormalities in ADHD children recorded over night by video-polysomnography. Epilepsy Res 75: 130-137.
83. Sotiriou E, Papatheodoropoulos C, Angelatou F,. (2005) Differential expression of gamma-aminobutyric acid-A receptor subunits in rat dorsal and ventral hippocampus. J Neurosci Res 82: 690-700.
84. Staley K, Hellier JL, Dudek FE,. (2005) Do interictal spikes drive epileptogenesis? Neuroscientist 11: 272-276.
85. Thompson KW, Sankar R,. (2006) Seizure-induced damage in the immature brain:overcoming the burden of proof. In, Wasterlain CG, Treiman DM, (Eds) Status epilepticus: mechanisms and management. MIT Press, Cambridge, MA, pp. 339-345.
86. Toth E,. (1996) Effect of nicotine on the level of extracellular amino acids in the hippocampus of rat. Neurochem Res 21: 903-907.
87. Traynelis SF, Dingledine R,. (1988) Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 59: 259-276.
88. Turski L, Ikonomidou C, Turski WA, Bortolotto ZA, Cavalheiro EA,. (1989) Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 3: 154-171.
89. Verney C, Baulac M, Berger B, Alvarez C, Vigny A, Helle KB,. (1985) Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat. Neuroscience 14: 1039-1052.
90. Wall SJ, Wolfe BB, Kromer LF,. (2008) Cholinergic deafferentation of dorsal hippocampus by fimbria-fornix lesioning differentially regulates subtypes (m1-m5) of muscarinic receptors. J Neurochem 62: 1345-1351.
91. Wang H, Sun X,. (2005) Desensitized nicotinic receptors in brain. Brain Res Rev 48: 420-437.
92. Wyss JM, Swanson LW, Cowan WM,. (1980) The organization of the fimbria, dorsal fornix and ventral hippocampal commissure in the rat. Anat Embryol (Berl) 158: 303-316.
93. Zhou J-L, Lenck-Santini P-P, Zhao Q, Holmes GL,. (2007) Effect of interictal spikes on single-cell firing patterns in the hippocampus. Epilepsia 48: 720-731.