Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus

Neuroscience

Volumn 108, Issue 4, 2001, Pages 587-600

  Wittner, L ^a   Magloczky Zs ^a   Borhegyi, Zs ^a   Halasz P ^b   Toth Sz ^c   Eross, L ^c   Szabo Z ^c   Freund, T F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c MAV Hospital   (Hungary)

Author keywords

Axon initial segment; GABA; Parvalbumin; Sprouting; Synaptic reorganization; Synchronization

Indexed keywords

4 AMINOBUTYRIC ACID; PARVALBUMIN;

ADOLESCENT; ADULT; ARTICLE; CHEMISTRY; CORTICAL SYNCHRONIZATION; DENDRITE; DENTATE GYRUS; ELECTRON MICROSCOPY; FEMALE; HUMAN; INTERNEURON; MALE; NERVE CELL INHIBITION; NERVE FIBER; NERVE TRACT; PATHOLOGY; SYNAPSE; TEMPORAL LOBE EPILEPSY; ULTRASTRUCTURE;

ADOLESCENT; ADULT; AXONS; CORTICAL SYNCHRONIZATION; DENDRITES; DENTATE GYRUS; EPILEPSY, TEMPORAL LOBE; FEMALE; GAMMA-AMINOBUTYRIC ACID; HUMAN; INTERNEURONS; MALE; MICROSCOPY, ELECTRON; MIDDLE AGE; NEURAL INHIBITION; NEURAL PATHWAYS; PARVALBUMINS; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; SYNAPSES;

EID: 0035226351     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(01)00446-8     Document Type: Article

References (68)

1. Babb, T.L., Kupfer, W.R., Pretorius, J.K., Crandall, P.H., Levesque, M.F., 1991. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42, 351-364.
2. Babb, T.L., Pretorius, J.K., Kupfer, W.R., Crandall, P.H., 1989. Glutamate decarboxylase-immunorective neurons are preserved in human epileptic hippocampus. J. Neurosci. 9, 2562-2574.
3. Bazzett, T.J., Becker, J.B., Falik, R.C., Albin, R.L., 1994. Chronic intrastriatal quinolinic acid produces reversible changes in perikaryal calbindin and parvalbumin immunoreactivity. Neuroscience 60, 837-841.
4. 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.
5. Best, N., Mitchell, J., Baimbridge, K.G., Wheal, H.V., 1993. Changes in parvalbumin-immunoreactive neurons in the rat hippocampus following a kainic acid lesion. Neurosci. Lett. 155, 1-6.
6. Braak, E., Strotkamp, B., Braak, H., 1991. Parvalbumin-immunoreactive structures in the hippocampus of the human adult. Cell Tissue Res. 264, 33-48.
7. Buckmaster, P.S., Dudek, F.E., 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.
8. Buhl, E.H., Halasy, K., Somogyi, P., 1994. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites [see comments] [published erratum appears in Nature 397 (1997) 106]. Nature 368, 823-828.
9. Buzsaki, G., Horvath, Z., Urioste, R., Hetke, J., Wise, K., 1992. High-frequency network oscillation in the hippocampus. Science 256, 1025-1027.
10. Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O., Somogyi, P., 1995. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78.
11. Corsellis, J.A.N., 1955. The incidence of Ammon's horn sclerosis. Brain 80, 193-208.
12. Cossart, R., Dinocourt, C., Hirsch, J.C., Merchan-Perez, A., De Felipe, J., Esclapez, M., Bernard, C., Ben-Ari, Y., 2001. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nature Neurosci. 4, 52-62.
13. Csiffary, A., Gorcs, T.J., Palkovits, M., 1990. Neuropeptide Y innervation of ACTH immunoreactive neurons in the arcuate nucleus of rats: a correlated light and electron microscopic double immunolabelling study. Brain Res. 506, 215-222.
14. Davenport, C.J., Brown, W.J., Babb, T.L., 1990. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp. Neurol. 109, 180-190.
15. de Lanerolle, N.C., Kim, J.H., Robbins, R.J., Spencer, D., 1989. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 495, 387-395.
16. de Lanerolle, N.C., Sloviter, R.S., Kim, J.H., Robbins, R.J., Spencer, D.D., 1988. Evidence for hippocampal interneuron loss in human temporal lobe epilepsy. Epilepsia 29, 674.
17. de Lanerolle, N.C., Thapar, K., Partington, J.P., Robbins, R.J., 1987. Comparison of somatostatin immunoreactivity in epileptogenic and normal human hippocampi. Epilepsia 28, 600-601.
18. DeFelipe, J., 1999. Chandelier cells and epilepsy. Brain 122, 1807-1822.
19. DeFelipe, J., Garcia Sola, R., Marco, P., Del Rio, M.R., Pulido, P., Ramon, C., 1993. Selective changes in the microorganization of the human epileptogenic neocortex revealed by parvalbumin immunoreactivity. Cereb. Cortex 3, 39-48.
20. Falconer, M., 1974. Mesial temporal (Ammon's horn) sclerosis as a common cause of epilepsy. Aetiology, treatment and prevention. Lancet 2, 767-770.
21. Freund, T.F., Buzsaki, G., 1996. Interneurons of the hippocampus. Hippocampus 6, 347-470.
22. Frotscher, M., Zimmer, J., 1983. Lesion-induced mossy fibers to the inner molecular layer of the rat fascia dentata: identification of postsynaptic granule cells by the golgi-EM technique. J. Comp. Neurol. 215, 299-311.
23. Gaarskjaer, F.B., 1978. Organization of the mossy fiber system of the rat studied in extended hippocampi. J. Comp. Neurol. 178, 73-88.
24. Halasy, K., Buhl, E.H., Lorinczi, Z., Tamas, G., Somogyi, P., 1996. Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6, 306-329.
25. Holm, I.E., Geneser, F.A., Zimmer, J., Baimbridge, K.G., 1990. Immunocytochemical demonstration of the calcium-binding proteins calbindin-D 28k and parvalbumin in the subiculum, hippocampus and dentate area of the domestic pig. Prog. Brain Res. 83, 85-97.
26. Houser, C.R., 1991. GABA neurons in seizure disorders: A review of immunocytochemical studies. Neurochem. Res. 3, 295-308.
27. Houser, C.R., 1992. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res. Suppl. 7, 223-234.
28. Isokawa, M., Levesque, M.F., Babb, T.L., Engel, J., 1993. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J. Neurosci. 13, 1511-1522.
29. Isokawa-Akesson, M., Wilson, C.L., Babb, T.L., 1989. Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res. 3, 236-247.
30. Johansen, F.F., Tonder, N., Zimmer, J., Baimbridge, K.G., Diemer, N.H., 1990. Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia. Neurosci. Lett. 120, 171-174.
31. Jolkkonen, J., Jolkkonen, E., Pitkanen, A., 1997. Seizure-induced damage to somatostatin-immunoreactive neurons in the rat hippocampus is regulated by fimbria-fornix transection. Exp. Neurol. 145, 141-153.
32. Kamphuis, W., Huisman, E., Wadman, W.J., Lopes da Silva, F.H., 1989. Decrease in GABA immunoreactivity and alteration of GABA metabolism after kindling in the rat hippocampus. Exp. Brain Res. 74, 375-386.
33. Katsumaru, H., Kosaka, T., Heizmann, C.W., Hama, K., 1988. Immunocytochemical study of Gabaergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp. Brain Res. 72, 347-362.
34. Kosaka, T., Katsumaru, H., Hama, K., Wu, J.Y., Heizmann, C.W., 1987. GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419, 119-130.
35. Maglóczky, Z., Freund, T.F., 1993. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience 56, 317-336.
36. Maglóczky, Z., Freund, T.F., 1995. Delayed cell death in the contralateral hippocampus following kainate injection into the CA3 subfield. Neuroscience 66, 847-860.
37. Maglóczky, Z., Wittner, L., Borhegyi, Z., Halász, P., Vajda, J., Czirják, S., Freund, T.F., 2000. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 96, 7-25.
38. Marco, P., Sola, R.G., Cayal, S.R.Y., DeFelipe, J., 1997. Loss of inhibitory synapses on the soma and axon intial segment of pyramidal cells in human epileptic peritumoral neocortex: implications for epilepsy. Brain Res. Bull. 44, 47-66.
39. Marco, P., Sola, R.G., Pulido, P., Alijarde, M.T., Sanchez, A., Ramon y Cajal, S., DeFelipe, J., 1996. Inhibitory neurons in the human epileptogenic temporal neocortex. An immunocytochemical study. Brain 119, 1327-1347.
40. Margerison, J.H., Corsellis, J.A.N., 1966. Epilepsy and the temporal lobe. Brain 89, 499-530.
41. Mathern, G.W., Babb, T.L., Leite, J.P., Pretorius, K., Yeoman, K.M., Kuhlman, P.A., 1996. The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res. 26, 151-161.
42. Mathern, G.W., Bertram, E.H., III, Babb, T.L., Pretorius, J.K., Kuhlman, P.A., Spradlin, S., Mendoza, D., 1997. In contrast to kindled seizures, the frequency of spontaneous epilepsy in the limbic status model correlates with greater aberrant fascia dentata excitatory and inhibitory axon sprouting, and increased staining for N-methyl-D-aspartate, AMPA and GABA(A) receptors. Neuroscience 77, 1003-1019.
43. Miles, R., Tóth, K., Gulyás, A.I., Hájos, N., Freund, T.F., 1996. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815-823.
44. Motalli, R., Louvel, J., Tancredi, V., Kurcewicz, I., Wan-Chow-Wah, D., Pumain, R., Avoli, M., 1999. GABA(B) receptor activation promotes seizure activity in the juvenile rat hippocampus. J. Neurophysiol. 82, 638-647.
45. Nitsch, R., Soriano, E., Frotscher, M., 1990. The parvalbumin-containing nonpyramidal neurons in the rat hippocampus. Anat. Embryol. 181, 413-425.
46. 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.
47. Prince, D.A., Jacobs, K., 1998. Inhibitory function in two models of chronic epileptogenesis. Epilepsy Res. 32, 83-92.
48. Represa, A., Niquet, J., Pollard, H., Khrestchatisky, M., Ben-Ari, Y., 1994. From seizures to neo-synaptogenesis: intrinsic and extrinsic determinants of mossy fiber sprouting in the adult hippocampus. Hippocampus 4, 270-274.
49. Ribak, C.E., Nitsch, R., Seress, L., 1990. Proportion of parvalbumin-positive basket cells in the Gabaergic innervation of pyramidal and granule cells of the rat hippocampal formation. J. Comp. Neurol. 300, 449-461.
50. Robbins, R.J., Brines, M.L., Kim, J.H., Adrian, T., de Lanerolle, N.C., Welsh, S., Spencer, D.D., 1991. A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy. Ann. Neurol. 29, 325-332.
51. Rowley, H.L., Martin, K.F., Marsden, C.A., 1995. Decreased GABA release following tonic-clonic seizures is associated with an increase in extracellular glutamate in rat hippocampus in vivo. Neuroscience 68, 415-422.
52. Scotti, A., Bollag, O., Kalt, G., Nitsch, C., 1997a. Loss of perikaryal parvalbumin immunoreactivity from surviving GABAergic neurons in the CA1 field of epileptic gerbils. Hippocampus 7, 524-535.
53. Scotti, A.L., Kalt, G., Bollag, O., Nitsch, C., 1997b. Parvalbumin disappears from GABAergic CA1 neurons of the gerbil hippocampus with seizure onset while its presence persists in the perforant path. Brain Res. 760, 109-117.
54. Seress, L., Gulyás, A.I., Ferrer, I., Tunon, T., Soriano, E., Freund, T.F., 1993. Distribution, morphological features, and synaptic connections of parvalbumin-immunoreactive and calbindin-d(28k)-immunoreactive neurons in the human hippocampal formation. J. Comp. Neurol. 337, 208-230.
55. Seress, L., Gulyás, A.I., Freund, T.F., 1991. Parvalbumin- and calbindin D28k-immunoreactive neurons in the hippocampal formation of the macaque monkey. J. Comp. Neurol. 313, 162-177.
56. Sik, A., Penttonen, M., Buzsaki, G., 1997. Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur. J. Neurosci. 9, 573-588.
57. Sloviter, R.S., 1987. Decreased hippocampal inhibition and selective loss of interneurons in experimental epilepsy. Science 235, 73-76.
58. Sloviter, R.S., 1991. Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the 'dormant basket cell' hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1, 41-66.
59. Sloviter, R.S., Sollas, A.L., Barbaro, N.M., Laxer, K.D., 1991. Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J. Comp. Neurol. 308, 381-396.
60. Sommer, W., 1880. Erkrankung des Ammonshornes als Aetiologisches Moment der Epilepsie. Arch. Psychiatrie Nervenkrankh. 10, 631-675.
61. Somogyi, P., Freund, T.F., Hodgson, A.J., Somogyi, J., Beroukas, D., Chubb, I.W., 1985. Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res. 332, 143-149.
62. Somogyi, P., Nunzi, M.G., Gorio, A., Smith, A.D., 1983. A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res. 259, 137-142.
63. Spencer, D.D., Spencer, S.S., 1985. Surgery for epilepsy. Neurol. Clin. 3, 313-330.
64. Sutula, T.P., Cascino, G., Cavazos, J.E., Ramirez, L., 1989. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26, 321-330.
65. Tauck, D., Nadler, J.V., 1985. Evidence of functional mossy fiber sprouting in the hippocampal formation of kainic acid treated rats. J. Neurosci. 5, 1016-1022.
66. Tortosa, A., Ferrer, I., 1993. Parvalbumin immunoreactivity in the hippocampus of the gerbil after transient forebrain ischaemia: a qualitative and quantitative sequential study. Neuroscience 55, 33-43.
67. Wasterlain, C.G., Shirasaka, Y., Mazarati, A.M., Spigelman, I., 1996. Chronic epilepsy with damage restricted to the hippocampus: possible mechanisms. Epilepsy Res. 26, 255-265.
68. Zhu, Z.Q., Armstrong, D.L., Hamilton, W.J., Grossman, R.G., 1997. Disproportionate loss of CA4 parvalbumin-immunoreactive interneurons in patients with Ammon's horn sclerosis. J. Neuropathol. Exp. Neurol. 56, 988-998.