Granule cell dispersion in temporal lobe epilepsy is associated with changes in dendritic orientation and spine distribution

Experimental Neurology

Volumn 229, Issue 2, 2011, Pages 332-338

  Freiman, Thomas M ^a   Eismann Schweimler, Jessica ^a   Frotscher, Michael ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Ammon's horn sclerosis; Dendrite; Granule cell; Hippocampus; Reelin; Spine; Temporal lobe epilepsy

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELLULAR DISTRIBUTION; CHILD; CLINICAL ARTICLE; DENDRITIC SPINE; DENTATE GYRUS; DENTATE HILUS; FEMALE; GOLGI STAIN; GRANULE CELL; HIPPOCAMPAL MOSSY FIBER; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY;

ADULT; DENDRITES; DENDRITIC SPINES; EPILEPSY, TEMPORAL LOBE; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; NEURONS; SILVER STAINING;

EID: 79956067926     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.02.017     Document Type: Article

References (37)

1. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998, 393:805-809.
2. Bamburg J.R. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Biol. 1999, 15:185-230.
3. Blümcke I., Suter B., Behle K., Kuhn R., Schramm J., Elger C.E., et al. Loss of hilar mossy cells in Ammon's horn sclerosis. Epilepsia 2000, 41:S174-S180.
4. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 1999, 89:717-729.
5. Bratz E. Ammonshornbefunde bei Epileptikern. Arch. Psychiatr. Nervenkr. 1899, 32:820-835.
6. Buckmaster P.S., Jongen-Relo A.L., Davari S.B., Wong E.H. Testing the disinhibition hypothesis of epileptogenesis in vivo and during spontaneous seizures. J. Neurosci. 2000, 20:6232-6240.
7. Buckmaster P.S., Zhang G.F., Yamawaki R. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J. Neurosci. 2002, 22:6650-6658.
8. Chai X., Förster E., Zhao S., Bock H.H., Frotscher M. Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J. Neurosci. 2009, 29:288-299.
9. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374:719-723.
10. D'Arcangelo G., Nakajima K., Miyata T., Ogawa M., Mikoshiba K., Curran T. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J. Neurosci. 1997, 17:23-31.
11. Drakew A., Deller T., Heimrich B., Gebhardt C., Del Turco D., Tielsch A., et al. Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp. Neurol. 2002, 176:12-24.
12. Fahrner A., Kann G., Flubacher A., Heinrich C., Freiman T.M., Zentner J., et al. Granule cell dispersion is not accompanied by enhanced neurogenesis in temporal lobe epilepsy patients. Exp. Neurol. 2007, 203:320-332.
13. Frotscher M. Application of the Golgi/electron microscopy technique for cell identification in immunocytochemical, retrograde labeling, and developmental studies of hippocampal neurons. Microsc. Res. Tech. 1992, 23:306-323.
14. Frotscher M. Role for Reelin in stabilizing cortical architecture. Trends Neurosci. 2010, 33:407-414.
15. Haas C.A., Dudeck O., Kirsch M., Huszka C., Kann G., Pollak S., et al. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 2002, 22:5797-5802.
16. Heinrich C., Nitta N., Flubacher A., Muller M., Fahrner A., Kirsch M., et al. Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci. 2006, 26:4701-4713.
17. Hermann B.P., Wyler A.R., Somes G., Berry A.D., Dohan F.C. Pathological status of the mesial temporal lobe predicts memory outcome from left anterior temporal lobectomy. Neurosurgery 1992, 31:652-656.
18. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 1990, 535:195-204.
19. Isokawa M. Preservation of dendrites with the presence of reorganized mossy fiber collaterals in hippocampal dentate granule cells in patients with temporal lobe epilepsy. Brain Res 1997;744:339-43. Erratum in. Brain Res. 1997, 758:263.
20. Isokawa M., Levesque M.F., Babb T.L., Engel J. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J. Neurosci. 1993, 13:1511-1522.
21. Mathern G.W., Kuhlman P.A., Mendoza D., Pretorius J.K. Human fascia dentata anatomy and hippocampal neuron densities differ depending on the epileptic syndrome and age at first seizure. J. Neuropathol. Exp. Neurol. 1997, 56:199-212.
22. Müller M.C., Osswald M., Tinnes S., Häussler U., Jacobi A., Förster E., et al. Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp. Neurol. 2009, 216:390-397.
23. Ribak C.E., Tran P.H., Spigelman I., Okazaki M.M., Nadler J.V. Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry. J. Comp. Neurol. 2000, 428:240-253.
24. Scheibel M.E., Crandall P.H., Scheibel A.B. The hippocampal-dentate complex in temporal lobe epilepsy. A Golgi study. Epilepsia 1974, 15:55-80.
25. Seress L., Frotscher M. Morphological variability is a characteristic feature of granule cells in the primate fascia dentata: a combined Golgi/electron microscope study. J. Comp. Neurol. 1990, 293:253-267.
26. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 1953, 87:387-406.
27. Sloviter R.S. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann. Neurol. 1994, 35:640-654.
28. Sloviter R.S., Zappone C.A., Harvey B.D., Frotscher M. Kainic acid-induced recurrent mossy fiber innervation of dentate gyrus inhibitory interneurons: possible anatomical substrate of granule cell hyper-inhibition in chronically epileptic rats. J. Comp. Neurol. 2006, 494:944-960.
29. Sommer W. Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch. Psychiatr. Nervenkr. 1880, 10:631-675.
30. Spearman C. "General Intelligence", objectively determined and measured. Am. J. Psychol. 1904, 15:201-293.
31. Spigelman I., Yan X.-X., Obenaus A., Lee E.Y.-S., Wasterlain C.G., Ribak C.E. Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience 1998, 86:109-120.
32. Stanfield B.B., Cowan W.M. The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 1979, 185:393-422.
33. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 1989, 26:321-330.
34. Suzuki F., Makiura Y., Guilhem D., Sorensen J.C., Onteniente B. Correlated axonal sprouting and dendritic spine formation during kainate-induced neuronal morphogenesis in the dentate gyrus of adult mice. Exp. Neurol. 1997, 145:203-213.
35. Valverde F. Apical dendritic spines and light deprivation in the mouse. Exp. Brain Res. 1967, 3:337-352.
36. Valverde F. Structural changes in the area striata of the mouse after enucleation. Exp. Brain Res. 1968, 5:274-292.
37. von Campe G., Spencer D.D., de Lanerolle N.C. Morphology of dentate granule cells in the human epileptogenic hippocampus. Hippocampus 1997, 7:472-488.