Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus

Neuroscience

Volumn 96, Issue 1, 2000, Pages 7-25

  Magloczky Z S ^a   Wittner, L ^a   Borhegyi, Z S ^a   Halasz P ^b   Vajda, J ^c   Czirjak S ^c   Freund, T F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b POB 1 H 1281 ^*  (Hungary)

^c NATIONAL INSTITUTE OF NEUROSURGERY   (Hungary)

Author keywords

Calcium binding proteins; Epilepsy; Hippocampus; Substance P receptor; Synaptic reorganization

Indexed keywords

CALCIUM BINDING PROTEIN; SUBSTANCE P;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; EPILEPSY; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; INTERNEURON; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY;

ADOLESCENT; ADULT; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHILD; DENTATE GYRUS; EPILEPSY, TEMPORAL LOBE; FEMALE; HUMANS; INTERNEURONS; MALE; MIDDLE AGED; NEURONS; RECEPTORS, NEUROKININ-1;

EID: 0343593734     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00474-1     Document Type: Article

References (68)

1. Acsády L., Görcs T., Freund T.F. Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience. 73:1996;317-334.
2. Acsády L., Katona I., Gulyás A.I., Shigemoto R., Freund T.F. Immunostaining for substance P receptor labels GABAergic cells with distinct termination pattern in the hippocampus. J. comp. Neurol. 378:1997;320-336.
3. Babb T.L., Kupfer W.R., Pretorius J.K., Crandall P.H., Levesque M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 42:1991;351-364.
4. Babb T.L., Pretorius J.K., Kupfer W.R., Crandall P.H. Glutamate decarboxylase-immunorective neurons are preserved in human epileptic hippocampus. J. Neurosci. 9:1989;2562-2574.
5. Babb T.L., Pretorius J.K., Mello L.E., Mathern G.W., Levesque M.F., Meldrum B.C. Synaptic reorganizations in epileptic human and rat kainate hippocampus may contribute to feedback and feedforward excitation. Epilepsy Res. 5:(suppl. 9):1992;193-203.
6. Baimbridge K.G., Miller J.J., Parkes C.O. Calcium-binding protein distribution in the rat brain. Brain Res. 239:1982;519-525.
7. Blümcke I., Beck H., Nitsch R., Eickhoff C., Scheffler B., Celio M.R., Schramm J., Elger C.E., Wolf H.K., Wiestler O.D. Preservation of calretinin-immunoreactive neurons in the hippocampus of epileptic patients with Ammon's horn sclerosis. J. Neuropath. exp. Neurol. 55:1996;329-341.
8. Borhegyi Zs., Leranth C. Distinct substance P- and calretinin-containing projections from the supramammillary area to the hippocampus in rats; a species difference between rats and monkeys. Expl Brain Res. 115:1997;369-374.
9. Bornstein R.A., Pakalnis A., Drake M.E. Jr, Suga L.J. Effects of seizure type and waveform abnormality on memory and attention. Archs Neurol. 45:1988;884-887.
10. Bridgman P.A., Malamut B.L., Sperling M.R., Saykin A.J., O'Connor M.J. Memory during subclinical hippocampal seizures. Neurology. 39:1989;853-856.
11. de Lanerolle N.C., Sloviter R.S., Kim J.H., Robbins R.J., Spencer D.D. Evidence for hippocampal interneuron loss in human temporal lobe epilepsy. Epilepsia. 29:1988;674.
12. Dupuy-Davies S., Houser C.R. Evidence for changing position of GABA neurons in the developing rat dentate gyrus. Hippocampus. 9:1999;186-199.
13. Ernfors P., Bengzon J., Kokaia Z., Persson H., Lindvall O. Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron. 7:1991;165-176.
14. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus. 6:1996;347-470.
15. Freund T.F., Maglóczky Zs. Early degeneration of calretinin-containing neurons in the rat hippocampus after ischemia. Neuroscience. 56:1993;581-596.
16. Freund T.F., Ylinen A., Miettinen R., Pitkanen A., Lahtinen H., Baimbridge K.G., Riekkinen P.J. Pattern of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability. Brain Res. Bull. 28:1991;27-38.
17. Fried I., Kim J.H., Spencer D.D. Hippocampal pathology in patients with intractable seizures and temporal lobe masses. J. Neurosurg. 76:1992;735-740.
18. Green R. C. (1991) Neuropathology and behavior in epilepsy. In Epilepsy and Behavior (eds Devinsky C. and Theodore W. H.) pp. 345-359. Wiley-Liss, New York.
19. Gulyás A.I., Hájos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 16:1996;3397-3411.
20. Gulyás A.I., Miettinen R., Jacobowitz D.M., Freund T.F. Calretinin is present in non-pyramidal cells of the rat hippocampus - I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience. 48:1992;1-27.
21. Houser C.R. GABA neurons in seizure disorders: a review of immunocytochemical studies. Neurochem. Res. 3:1991;295-308.
22. Houser C.R. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res. 5:(suppl. 9):1992;223-234.
23. Houser C. R., Swartz B. E., Walsh G. O. and Delgado-Escueta A. V. (1992) Granule cell disorganization in the dentate gyrus - possible alterations of neuronal migration in human temporal lobe epilepsy. In Molecular Neurobiology of Epilepsy (eds Engel J., Wasterlain C., Cavalhiero E. A., Heinemann U. and Avanzini G.), Epilepsy Research Suppl. 9, pp. 41-49. Elsevier Science, Amsterdam.
24. Hughes P.E., Alexi T., Walton M., Williams C.E., Dragunow M., Clark R.G., Gluckman P.D. Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system. Prog. Neurobiol. 57:1999;421-450.
25. Ip N.Y., Li Y., Yancopoulos G.D., Lindsay R.M. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J. Neurosci. 13:1993;3394-3405.
26. 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. 13:1993;1511-1522.
27. Jacobowitz D.M., Winsky L. Immunocytochemical localization of calretinin in the forebrain of the rat. J. comp. Neurol. 304:1991;198-218.
28. Lang U., Frotscher M. Postnatal development of nonpyramidal neurons in the rat hippocampus (Area-CA1 and Area-CA3) - a combined Golgi electron microscope study. Anat. Embryol. 181:1990;533-545.
29. Larmet Y., Reibel S., Carnahan J., Nawa H., Marescaux C., Depaulis A. Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. NeuroReport. 6:1995;1937-1941.
30. Maglóczky Zs., Acsády L., Freund T.F. Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus. 4:1994;322-334.
31. Maglóczky Zs., Freund T.F. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience. 56:1993;317-336.
32. Maglóczky Zs., Freund T.F. Delayed cell death in the contralateral hippocampus following kainate injection into the CA3 subfield. Neuroscience. 66:1995;847-860.
33. Maglóczky Zs., Halász P., Vajda J., Czirják S., Freund T.F. Loss of Calbindin-D28k immunoreactivity from dentate granule cells in human temporal lobe epilepsy. Neuroscience. 76:1997;377-385.
34. Maisonpierre P.C., Belluscio L., Friedman B., Alderson R., Weigand S., Furth M.E., Lindsay R.M., Yancopoulos G.D. NT-3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron. 5:1990;501-509.
35. Mantyh P.W., Allen C.J., Ghilardi J.R., Rogers S.D., Mantyh C.R., Liu H., Basbaum A.I., Vigna S.R., Maggio J.E. Rapid endocytosis of a G protein-coupled receptor: substance P-evoked internalization of its receptor in the rat striatum in vivo. Proc. natn. Acad. Sci. U.S.A. 92:1995;2622-2626.
36. Margerison J.H., Corsellis J.A.N. Epilepsy and the temporal lobe. Brain. 89:1966;499-530.
37. Martinez-Guijarro F.J., Freund T.F. Distribution of GABAergic interneurons immunoreactive for calretinin, calbindin D28k, and parvalbumin in the cerebral cortex of the lizard Podarcis hispanica. J. comp. Neurol. 322:1992;449-460.
38. Marty S., Berninger B., Caroll P., Thoenen H. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron. 16:1996;565-570.
39. Marty S., Carroll P., Cellerino A., Castern E., Staiger V., Thoenen H., Lindholm D. Brain-derived neurotrophic factor promotes the differentiation of various hippocampal nonpyramidal neurons, including Cajal-Retzius cells, in organotypic slice culture. J. Neurosci. 16:1996;675-687.
40. Masukawa L.M., Uruno K., Sperling M., Oconnor M.J., Burdette L.J. The functional relationship between antidromically evoked field responses of the dentate gyrus and mossy fiber reorganization in temporal lobe epileptic patients. Brain Res. 579:1992;119-127.
41. Mathern G.W., Babb T.L., Micevych P.E., Blanco C.E., Pretorius J.K. Granule cell mRNA levels for BDNF, NGF, and NT-3 correlate with neuron losses or supragranular mossy fiber sprouting in the chronically damaged and epileptic human hippocampus. Molec. chem. Neuropath. 30:1997;53-76.
42. Mathern G.W., Babb T.L., Pretorius J.K., Leite J.P. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J. Neurosci. 15:1995;3990-4004.
43. Meencke H. J. and Veith G. (1991) Hippocampal sclerosis in epilepsy. In Epilepsy Surgery (ed. Luders H.), pp. 705-715. Raven, New York.
44. Miller L.A., Munoz D.G., Finmore M. Hippocampal sclerosis and human memory. Archs Neurol. 50:1993;391-394.
45. Mudo G., Jiang X.H., Timmusk T., Bindoni M., Belluardo N. Change in neurotrophins and their receptor mRNAs in the rat forebrain after status epilepticus induced by pilocarpine. Epilepsia. 37:1996;198-207.
46. Nakaya Y.T., Kaneko R., Shigemoto R., Nakanishi S., Mizuno N. Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. J. comp. Neurol. 347:1994;249-274.
47. Nitsch R., Leranth C. Calretinin immunoreactivity in the monkey hippocampal formation - II. Intrinsic GABAergic and hypothalamic nonGABAergic systems. An experimental tracing and coexistence study. Neuroscience. 55:1993;797-812.
48. Nitsch R., Ohm T.G. Calretinin immunoreactive structures in the human hippocampal formation. J. comp. Neurol. 360:1995;475-487.
49. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17:1997;3727-3738.
50. Resibois A., Rogers J.H. Calretinin in rat brain - an immunohistochemical study. Neuroscience. 46:1992;101-134.
51. Rihn L.L., Claiborne B.J. Dendritic growth and regression in rat dentate granule cells during late postnatal development. Devl Brain Res. 54:1990;115-124.
52. Rogers J.H. Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J. Cell Biol. 105:1987;1343-1353.
53. Sato K., Kashihara K., Morimoto K., Hayabara T. Regional increases in barin-derived neurotrophic factor and nerve growth factor mRNAs during amygdaloid kindling, but not in acidic and basic growth factor mRNAs. Epilepsia. 37:1996;6-14.
54. Seay-Lowe S.L., Claiborne B.J. Morphology of intracellularly labeled interneurons in the dentate gyrus of the immature rat. J. comp. Neurol. 324:1992;23-36.
55. Seress L., Gulyás A.I., Ferrer I., Tunon T., Soriano E., Freund T.F. Distribution, morphological features, and synaptic connections of parvalbumin-immunoreactive and calbindin-d(28k)-immunoreactive neurons in the human hippocampal formation. J. comp. Neurol. 337:1993;208-230.
56. Seress L., Léránth C., Frotscher M. Distribution of calbindin D28k immunoreactive cells and fibers in the monkey hippocampus, subicular complex and entorhinal cortex. Light and electron microscopic study. J. Brain Res. 4:1994;473-486.
57. Seress L., Nitsch R., Léránth C. Calretinin immunoreactivity in the monkey hippocampal formation - I. Light and electron microscopic characteristics and co-localization with other calcium-binding proteins. Neuroscience. 55:1993;775-796.
58. Seress L., Ribak C.E. Postnatal development of the light and electron microscopic features of basket cells in the hippocampal dentate gyrus of the rat. Anat. Embryol. 181:1990;547-565.
59. Shigemoto R., Nakaya Y.T., Nomura S., Ogawa-Meguro R., Ohishi H., Kaneko T., Nakanishi S., Mizuno N. Immunocytochemical localization of rat substance P receptor in striatum. Neurosci. Lett. 153:1993;157-160.
60. Sloviter R.S. Calcium-binding protein (Calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. comp. Neurol. 280:1989;183-196.
61. Sloviter R.S., Sollas A.L., Barbaro N.M., Laxer K.D. Calcium-binding protein (Calbindin-D28k) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J. comp. Neurol. 308:1991;381-396.
62. Sommer W. Erkrankung des Ammonshornes als aetiologisches Moment der Epilepsie. Arch. Psychiat. NervKrankh. 10:1880;631-675.
63. Sutula T.P., Cascino G., Cavazos J.E., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26:1989;321-330.
64. Takahashi M., Hayashi S., Kakita A., Wakabayashi K., Fukuda M., Kameyama S., Tanaka R., Takahashi H., Nawa H. Patients with temporal lobe epilepsy show an increase in brain-derived neurotrophic factor and its correlation with neuropeptide Y. Brain Res. 818:1999;579-582.
65. Tongiorgi E., Righi M., Cattaneo A. Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J. Neurosci. 17:1997;9492-9505.
66. Widmer H.R., Hefti F. Stimulation of GABAergic neuron differentiation by NT-4/5 in cultures of rat cerebral cortex. Devl Brain Res. 80:1994;279-284.
67. Yan Q., Rosenfeld R.D., Matheson C.R., Hawkins N., Lopez O.T., Bennett L., Welcher A.A. Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience. 78:1997;431-448.
68. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 6:1986;2950-2967.