Lateral entorhinal cortex lesions rearrange afferents, glutamate receptors, increase seizure latency and suppress seizure-induced c-fos expression in the hippocampus of adult rat

Journal of Neurochemistry

Volumn 95, Issue 1, 2005, Pages 111-124

  Kopniczky, Zsolt ^a   Dobó, Endre ^a,c   Borbély, Sándor ^b   Világi, Ildikó ^b   Détári, László ^b   Krisztin Péva, Beáta ^b   Bagosi, Andrea ^a   Molnár, Elek ^c   Mihály, András ^a,c  

^a UNIVERSITY OF SZEGED   (Hungary)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

4 aminopyridine; c fos; Entorhinal cortex; Hippocampus; Seizure; Sprouting

Indexed keywords

4 AMINOPYRIDINE; AMPA RECEPTOR; CALRETININ; GLUTAMATE RECEPTOR; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX LESION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CONVULSION; DEAFFERENTATION; DENTATE GYRUS; ELECTROENCEPHALOGRAPHY; ENTORHINAL CORTEX; EPILEPSY; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; LATENT PERIOD; MALE; NERVE CELL STIMULATION; NERVE SPROUTING; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; SEIZURE; SENSORY NERVE; SUBICULUM;

4-AMINOPYRIDINE; AFFERENT PATHWAYS; ANIMALS; BRAIN DISEASES; DISEASE SUSCEPTIBILITY; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; HIPPOCAMPUS; MALE; NEURONAL PLASTICITY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; REACTION TIME; RECEPTORS, GLUTAMATE; SEIZURES;

EID: 25644452042     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03347.x     Document Type: Article

References (67)

1. Acsády L., Kamondi A., Sík A., Freund T. and Buzsáki G. (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386-3403.
2. Adams M. M., Gazzaley A. H. and Morrison J. H. (2001) Attenuated lesion-induced N-methyl-D-aspartate receptor (NMDA) plasticity in the dentate gyrus of aged rats following perforant path lesions. Exp. Neurol. 172, 244-249.
3. Amaral D. G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182, 851-914.
4. Avoli M., D'Antuono M., Louvel J., Kohling R., Biagini G., Pumain R., D'Arcangelo G. and Tancredi V. (2002) Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog. Neurobiol. 68, 167-207.
5. Barbarosie M., Louvel J., Kurcewicz I. and Avoli M. (2000) CA3-released entorhinal seizures disclose dentate gyrus epileptogenicity and unmask a temporoammonic pathway. J. Neurophysiol. 83, 1115-1124.
6. Bartolomei F., Khalil M., Wendling F., Sontheimer A., Regis J., Ranjeva J. P., Guye M. and Chauvel P. (2005) Entorhinal cortex involvement in human mesial temporal lobe epilepsy: an electrophysiologic and volumetric study. Epilepsia 46, 677-687.
7. Bear J., Fountain N. B. and Lothman E. W. (1996) Responses of the superficial entorhinal cortex in vitro in slices from naive and chronically epileptic rats. J. Neurophysiol. 76, 2928-2940.
8. Bragin A., Csicsvari J., Penttonen B. and Buzsaki G. (1997) Epileptic after discharge in the hippocampal-entorhinal system: current source density and unit studies. Neuroscience 76, 1187-1203.
9. Burwell R. D. and Amaral D. G. (1998) Cortical afferents of the perirhinal, postrhinal and entorhinal cortices of the rat. J. Comp. Neurol. 398, 179-205.
10. Caceres A. and Steward O. (1983) Dendritic reorganization in the denervated dentate gyrus of the rat following entorhinal cortical lesions: a Golgi and electron microscopic analysis. J. Comp. Neurol. 214, 387-403.
11. D'Antuono M., Benini R., Biagini G., D'Arcangelo G., Barbarosie M., Tancredi V. and Avoli M. (2001) Limbic network interactions leading to hyperexcitability in a model of temporal lobe epilepsy. J. Neurophysiol. 87, 634-639.
12. Del Turco D., Woods A. G., Gebhardt C., Phinney A. L., Jucker M., Frotscher M. and Deller T. (2003) Comparison of commissural sprouting in the mouse and rat fascia dentata after entorhinal cortex lesion. Hippocampus 13, 685-699.
13. Deller T. and Frotscher M. (1997) Lesion-induced plasticity of central neurons: sprouting of single fibres in the rat hippocampus after unilateral entorhinal cortex lesion. Prog. Neurobiol. 53, 687-727.
14. Dolorfo C. L. and Amaral D. G. (1998) Entorhinal cortex of the rat: organization of intrinsic connections. J. Comp. Neurol. 398, 49-82.
15. Freund T. F. and Buzsaki G. (1996) Interneurons of the hippocampus. Hippocampus. 6, 347-470.
16. Gallyas F. Jr, Ball S. M. and Molnar E. (2003) Assembly and cell surface expression of KA-2 subunit-containing kainite receptors. J. Neurochem. 86, 1414-1427.
17. Gazzaley A. H., Benson D. L., Huntley G. W. and Morrison J. H. (1997) Differential subcellular regulation of NMDAR1 protein and mRNA in dendrites of dentate gyrus granule cells following perforant path transaction. J. Neurosci. 17, 2006-2017.
18. Glaser E. M. (1982) Snell's law: the bane of computer microscopists. J. Neurosci. Meth. 5, 201-202.
19. de Guzman P., D'Antonuo M. and Avoli M. (2004) Initiation of electrographic seizures by neuronal networks in entorhinal and periehinal cortices in vitro. Neuroscience 123, 875-886.
20. Hjorth-Simonsen A. and Jeune B. (1972) Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144, 215-232.
21. Iida K., Sasa M., Serikawa T., Noda A., Ishihara K., Akimitsu T., Hanaya R., Arita K. and Kurisu K. (1998) Induction of convulsive seizures by acustic priming in a new genetically defined model of epilepsy (Noda epileptic rat: NER). Epilepsy Res. 30, 115-126.
22. Iijima T., Witter M. P., Ichikawa M., Tominaga T., Kajiwara R. and Matsumoto G. (1996) Entorhinal-hippocampal interactions revealed by real-time imaging. Science 272, 1176-1179.
23. Insausti R., Amaral D. G. and Cowan W. M. (1987) The entorhinal cortex of the monkey. III. Subcortical afferents. J. Comp. Neurol. 264, 396-408.
24. Iwakiri M., Mizukami K., Ishikawa M., Hidaka S. and Asada T. (2002) Alterations of NMDAR1 and NMDAR2A/B immunoreactivity in the hippocampus after perforant path lesion. Neuropathology 22, 154-160.
25. Jones R. S. G. (1993) Entorhinal-hippocampal connections: a speculative view of their function. Trends Neurosci. 16, 58-64.
26. Jones R. S. G. and Lambert J. D. C. (1990) The role of excitatory amino acid receptor sin the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyrus in vitro. Exp. Brain Res. 80, 310-322.
27. Jorgensen M. B., Johansen F. F. and Diemer N. H. (1987) Removal of the entorhinal cortex protects hippocampal CA-1 neurons from ischemic damage. Acta Neuropathol. (Berl.) 73, 189-194.
28. Kamovsky M. J. and Roots L. (1964) A direct-coloring thiocholine method for cholinesterase. J. Histochem. Cytochem. 12, 219-222.
29. Kloosterman F., Van Haeften T. and Lopes Silva F. H. (2000) Functional characterization of hippocampal output to the entorhinal cortex in the rat. Ann. NY Acad. Sci. 911, 459-461.
30. Kloosterman F., van Haeften T., Witter M. P. and Lopes da Silva F. H. (2003) Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re-entrance in the hippocampal-entorhinal system. Eur. J. Neurosci. 18, 3037-3052.
31. Li X.-G., Somogyi P., Ylinen A. and Buzsaki G. (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 339, 181-208.
32. Mattson M. P., Lee R. E., Adams M. E., Guthrie P. B. and Kater S. B. (1988) Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry. Neuron 1, 865-876.
33. Mihály A., Szente M., Dubravcsik Z., Boda B., Kiraly E., Nagy T. and Domonkos A. (1997) Parvalbumin- and calbindin-containing neurons express c-fos protein in primary and secondary (mirror) epileptic foci of the rat neocortex. Brain Res. 761, 135-145.
34. Mihály A., Shihab-Eldeen A., Owunwanne A., Gopinath S., Ayesha A. and Mathew M. (2000) Acute 4-aminopyridine seizures increase the regional cerebral blood flow in the thalamus and neocortex, but not in the entire allocortex of the mouse brain. Acta Physiol. Hung. 87, 43-52.
35. Mihály A., Szakacs R., Bohata C., Dobo E. and Krisztin-Peva B. (2001) Time-dependent distribution and neuronal localization of c-fos protein in the rat hippocampus following 4-aminopyridine seizures. Epilepsy Res. 44, 97-108.
36. Mihály A., Borbély S., Világi I., Détári L., Weiczner R., Zádor Zs., Krisztin-Péva B., Bagosi A., Kopniczky Z. and Zádor E. (2005) Neocortical c-fos mRNA transcription in repeated, brief, acute seizures: is c-fos a coincidence detector? Int. J. Mol. Med. 15, 481-486.
37. Mitchell S. J. and Ranck J. B. Jr (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res. 189, 49-66.
38. Mizukami K., Mishizen A., Ikonovic M. D., Sheffield R. and Armstrong D. M. (1997) Alterations of AMPA-selected glutamate subtype immunoreactivity in the dentate gyrus after perforant pathway lesion. Brain Res. 768, 354-360.
39. Molnar E. and Isaac J. T. R. (2002) Developmental and activity dependent regulation of ionotropic glutamate receptors at synapses. Scientificworldjournal 2, 27-47.
40. Molnar E., Varadi A., McIlhinney R. A. J. and Ashcroft S. J. H. (1995) Identification of functional ionotropic glutamate receptor proteins in pancreatic β-cells and islets of Langerhans. FEBS Lett. 371, 253-257.
41. Molnar E., Pickard L. and Duckworth J. K. (2002) Developmental changes in ionotropic glutamate receptors: Lessons from hippocampal synapses. Neuroscientist 8, 143-153.
42. Nadler J. V., Cotman C. W. and Lynch G. S. (1977) Histochemical evidence of altered development of cholinergic fibers in the rat dentate gyrus following lesions. I. Time course after complete unilateral entorhinal lesion at various ages. J. Comp. Neurol. 171, 561-588.
43. Nicolle M. M., Shivers A., Gill T. M. and Gallagher M. (1997) Hippocampal N-ethyl-D-aspartate and kainate binding in response to entorhinal cortex aspiration or 192 IgG-saponin lesions of the basal forebrain. Neuroscience 77, 649-659.
44. Okada M., Zhu G., Yoshida S., Hirose S. and Kaneko S. (2004) Protein kinase associated with gating and closing transmission mechanisms in temporoammonic pathway. Neuropharmacology 47, 485-504.
45. Paxinos G. and Watson C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, San Diego.
46. Pickard L., Noel J., Henley J. M., Collingridge G. L. and Molnar E. (2000) Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J. Neurosci. 20, 7922-7931.
47. Raisman G., Cowan W. M. and Powell T. P. S. (1965) The extrinsic afferent, commissural and association fibres of the hippocampus. Brain 88, 963-998.
48. Rappert A., Bechmann I., Pivneva T. et al. (2004) CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J. Neurosci. 24, 8500-8509.
49. Reutens D. C. (1999) Entorhinal cortex in temporal lobe epilepsy: a quantitative MRI study. Neurology 52, 1870-1876.
50. Scharfman H. E. (1996) Hyperexcitability of entorhinal cortex and hippocampus after application of aminooxyacetic acid (AOAA) to layer III of the rat medial entorhinal cortex in vitro. J. Neurophysiol. 76, 2986-3001.
51. Schwarz P., Stichel C. C. and Luhmann H. J. (2000) Characterization of neuronal migration disorders in neocortical structures: loss or preservation of inhibitory intemeurons? Epilepsia 41, 781-787.
52. Sloviter R. S. (1983) 'Epileptic' brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res. Bull. 10, 675-697.
53. Steward O. and Scoville S. A. (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169, 347-370.
54. Stoop R. and Pralong E. (2000) Functional connections and epileptic spread between hippocampus, entorhinal cortex and amygdala in a modified horizontal slice preparation of the rat brain. Eur. J. Neurosci. 12, 3651-3663.
55. Stringer J. L. and Lothman E. W. (1992) Reverberatory seizure discharges in hippocampal-parahippocampal circuits. Exp. Neurol. 116, 198-203.
56. Sunanda, Meti B. L. and Raju T. R. (1997) Entorhinal cortex lesioning protects hippocampal CA3 neurons from stress-induced damage. Brain Res. 770, 302-306.
57. Swanson L. W. and Köhler C. (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J. Neurosci. 6, 3010-3023.
58. Szakács R., Weiczner R., Mihaly A., Krisztin-Peva B., Zador Z. and Zador E. (2003) Non-competitive NMDA receptor antagonists moderate seizure-induced c-fos expression in the rat cerebral cortex. Brain Res. Bull. 59, 485-493.
59. Tago H., Kimura H. and Maeda T. (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem. 34, 1431-1438.
60. Tonnes J., Stierli B., Cerletti C., Behrmann J. T., Molnar E. and Streit P. (1999) Regional distribution and developmental changes of GluR1-flop protein revealed by monoclonal antibody in rat brain. J. Neurochem. 73, 2195-2205.
61. Ułas J., Monaghan D. T. and Cotman C. W. (1990a) Kainate receptors in the rat hippocampus: a distribution and time course of changes in response to unilateral lesions of the entorhinal cortex. J. Neurosci. 10, 2352-2362.
62. Ułas J., Monaghan D. T. and Cotman C. W. (1990b) Plastic response of hippocampal excitatory amino acid receptors to deafferentation and reinnervation. Neuroscience 34, 9-17.
63. Weissinger F., Buchheim K., Siegmund H., Heinemann U. and Meierkord H. (2000) Optical imaging reveals characteristic seizure onsets, spread patterns, and propagation velocities in hippocampal-entorhinal cortex slices of juvenile rats. Neurobiol. Dis. 7, 286-298.
64. White L. E. and Price J. L. (1993) The functional anatomy of limbic status epilepticus in the rat. II. The effects of focal deactivation. J. Neurosci. 13, 4810-4830.
65. Wisden W., Seeburg P. H. and Monyer H. (2000) AMPA, kainate and NMDA ionotropic glutamate receptor expression: an in situ hybridization atlas, in Glutamate. Handbook of Chemical Neuroanatomy (Ottersen O. P. and Storm-Mathisen J., eds), Vol. 18, pp. 99-143. Elsevier.
66. Witter M. P., Naber P. A., van Haeften T., Machielsen W. C., Rombouts S. A., Barkhof F., Scheltens P. and Lopes da Silva F. H. (2000) Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10, 398-410.
67. Xu B., McIntyre D. C., Fahnestock M. and Racine R. J. (2004) Strain differences affect the induction of status epilepticus and seizure-induced morphological changes. Eur. J. Neurosci. 20, 403-418.