Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation

Journal of Neurophysiology

Volumn 82, Issue 4, 1999, Pages 1883-1894

  Molnár, Péter ^a   Nadler, J Victor ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PILOCARPINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; EPILEPTOGENESIS; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPUS; HISTOCHEMISTRY; LASER; MALE; MOSSY FIBER; NONHUMAN; PATCH CLAMP; PHOTOSTIMULATION; PRIORITY JOURNAL; RAT; SYNAPSE; TEMPORAL LOBE EPILEPSY;

EID: 0032857293     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.82.4.1883     Document Type: Article

References (70)

1. ALLEN, C. AND STEVENS, C. F. An evaluation of causes for unreliability of synaptic transmission. Proc. Natl. Acad. Sci. USA 91: 10380-10383, 1994.
2. ASZTELY, F., ERDEMLI, G., AND KULLMANN, D. M. Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18: 281-293, 1997.
3. BABB, T. L., KUPFER, W. R., PRETORIUS, J. K., CRANDALL, P. H., AND LEVESQUE, M. F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42: 351-363, 1991.
4. BLANTON, M. G., LO TURCO, J., AND KRIEGSTEIN, A. R. Whole-cell recording from neurons in slices of reptilian and mammalian cortex. J. Neurosci. Methods 30: 203-210, 1989.
5. BOSS, B. D., PETERSON, G. M., AND COWAN, W. M. On the number of neurons in the dentate gyrus of the rat. Brain Res. 338: 144-150, 1985.
6. BUCKMASTER, P. S. AND DuDEK, F. E. Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. J. Neurophysiol. 77: 2685-2696, 1997a.
7. BUCKMASTER, P. S. AND DUDEK, F. E. Neuron loss, granule cell reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol. 222: 461-471, 1997b.
8. BUCKMASTER, P. S. AND DUDEK, F. E. In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J. Neurophysiol. 81: 712-721, 1999.
9. BUCKMASTER, P. S., STROWBRIDGE, B. W., KUNKEL, D. D., SCHMIEGE, D. L., AND SCHWARTZKROIN, P. A. Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2: 349-362, 1992.
10. CARNEVALE, N. T., TSAI, K. Y., CLAIBORNE, B. J., AND BROWN, T. H. Comparative electrotonic analysis of three classes of rat hippocampal neurons. J. Neurophysiol. 78: 703-720, 1997.
11. CHICUREL, M. E. AND HARRIS, K. M. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J. Comp. Neurol. 325: 169-182, 1992.
12. CRONIN, J., OBENAUS, A., HOUSER, C. R., AND DUDEK, F. E. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res. 573: 305-310, 1992.
13. DANSCHER, G. Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electron microscopy. Histochemistry 71: 1-16, 1981.
14. FRANCK, J. E., POKORNY, J., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36: 543-558, 1995.
15. FREUND, T. F. AND BUZSÁKI, G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996.
16. FROTSCHER, M. AND ZIMMER, J. Lesion-induced mossy fibers to the molecular layer of the rat fascia dentata: identification of postsynaptic granule cells by the Golgi-EM technique. J. Comp. Neurol. 215: 299-311, 1983.
17. GAARSKJAER, F. B. Organization of the mossy fiber system of the rat studied in extended hippocampi. I. Terminal area related to number of granule and pyramidal cells. J. Comp. Neurol. 178: 49-72, 1978.
18. HAUG, F.-M.S. Light microscopical mapping of the hippocampal region, the pyriform cortex and the corticoamygdaloid nuclei of the rat with Timm's sulphide silver method. I. Area dentata, hippocampus and subiculum. Z. Anat. Entwickl.-Gesch. 145: 1-27, 1974.
19. HOSOKAWA, T., RUSAKOV, D. A., BLISS, T.V.P., AND FINE, A. Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J. Neurosci. 15: 5560-5573, 1995.
20. HOUSER, C. R., MIYASHIRO, J. E., SWARTZ, B. E., WALSH, G. O., RICH, J. R., AND DELOADO-ESCUETA, A. V. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10: 267-282, 1990.
21. JONAS, P., MAJOR, G., AND SAKMANN, B. Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. (Lond.) 472: 615-663, 1993.
22. JUNG, M. W. AND MCNAUCHTON, B. L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3: 165-182, 1993.
23. KANDLER, K., KATZ, L. C., AND KAUER, J. A. Focal photolysis of caged glutamate produces long-term depression of hippocampal glutamate receptors. Nature Neurosci. 1: 119-123, 1998.
24. KATZ, L. C. AND DALVA, M. B. Scanning laser photostimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54: 205-218, 1994.
25. KNEISLER, T. B. AND DINGLEDINE, R. Spontaneous and synaptic input from granule cells and the perforant path to dentate basket cells in the rat hippocampus. Hippocampus 5: 151-164, 1995.
26. KOTTI, T., RIEKKINEN, P. J., AND MIETTINEN, R. Characterization of target cells for aberrant mossy fiber collaterals in the dentate gyrus of epileptic rat. Exp. Neurol. 146: 323-330, 1997.
27. KULLMANN, D. M. AND ASZTELY, F. Extrasynaptic glutamate spillover in the hippocampus - evidence and implications. Trends Neurosci. 21: 8-14, 1998.
28. LEMOS, T. AND CAVALHEIRO, E. A. Status epilepticus and the late development of spontaneous seizures in the pilocarpine model of epilepsy. Epilepsy Res. Suppl. 12: 137-144, 1996.
29. LONGO, B. M. AND MELLO, L.E.A.M. Blockade of pilocarpine- or kainate-induced mossy fiber sprouting by cycloheximide does not prevent subsequent epileptogenesis in rats. Neurosci. Lett. 226: 163-166, 1997.
30. LOTHMAN, E. W., STRINGER, J. L., AND BERTRAM, E. H. The dentate gyrus as a control point for seizures in the hippocampus and beyond. Epilepsy Res. Suppl. 7: 301-313, 1992.
31. LÜSCHER, H.-R. AND SHINER, J. S. Simulation of action potential propagation in complex terminal arborizations. Biophys. J. 58: 1389-1399, 1990.
32. MACVICAR, B. A. AND DUDEK, F. E. Electrotonic coupling between granule cells of rat dentate gyms: physiological and anatomical evidence. J. Neurophysiol. 47: 579-592, 1982.
33. MASUKAWA, L. M., URUNO, K., SPERLING, M., O'CONNOR, M. J., AND 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: 119-127, 1992.
34. MELLO, L.E.A.M., CAVALHEIRO, E. A., TAN, A. M., KUPFER, W. R., PRETORIUS, J. K., BABB, T. L., AND FINCH, D. M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34: 985-995, 1993.
35. MILES, R., WONG, R.K.S., AND TRAUB, R. D. Synchronized afterdischarges in the hippocampus: contribution of local circuit interaction. Neuroscience 12: 1016-1022, 1984.
36. 3H]glutamate binding sites in rat brain. J. Neurosci. 5: 2909-2919, 1985.
37. MOTT, D. D., TURNER, D. A., OKAZAKI, M. M., AND LEWIS, D. V. Interneurons of the dentate-hilus border of the rat dentate gyrus: morphological and electrophysiological heterogeneity. J. Neurosci. 17: 3990-4005, 1997.
38. B autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus. J. Neurophysiol. 69: 674-691, 1993.
39. NADLER, J. V., PERRY, B. W., AND COTMAN, C. W. Selective reinnervation of area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182: 1-9, 1980.
40. OKAZAKI, M. M., EVENSON, D. A., AND NADLER, J. V. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J. Comp. Neurol. 352: 515-534, 1995.
41. OKAZAKI, M. M., MOLNÁR, P., AND NADLER, J. V. Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth. J. Neurophysiol. 81: 1645-1660, 1999.
42. OTIS, T. S., STALEY, K. J., AND MODY, I. Perpetual inhibitory activity in mammalian brain slices generated by spontaneous GABA release. Brain Res. 545: 142-150, 1991.
43. PATRYLO, P. R. AND DUDEK, F. E. Physiological unmasking of new glulamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J. Neurophysiol. 79: 418-429, 1998.
44. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Coordinates (2nd ed.). Orlando, FL: Academic, 1986.
45. PETTIT, D. L., WANG, S.S.-H., GEE, K. R., AND AUGUSTINE, G. J. Chemical two-photon uncaging: a novel approach to mapping glutamate receptors. Neuron 19: 465-471, 1997.
46. RAASTAD, M., STORM, J. F., AND ANDERSEN, P. Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur. J. Neurosci. 4: 113-117, 1992.
47. RACINE, R. J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32: 281-284, 1972.
48. REPRESA, A., JORQUERA, I., LE GAL LA SALLE, G., AND BEN-ARI, Y. Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus 3: 257-268, 1993.
49. REPRESA, A., ROBAIN, O., TREMBLAY, E., AND BEN-ARI, Y. Hippocampal plasticity in childhood epilepsy. Neurosci. Lett. 99: 351-355, 1989.
50. RIBAK, C. E., SERESS, L., AND AMARAL, D. G. The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J. Neurocytol. 14: 835-857, 1985.
51. 2+ and ATP. J. Physiol. (Lond.) 470: 705-729, 1993.
52. SALIN, P. A., SCANZIANI, M., MALENKA, R. C., AND NICOLL, R. A. Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc. Natl. Acad. Sci. USA 93: 13304-13309, 1996.
53. SCHARFMAN, H. E. Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J. Neurophysiol. 74: 179-194, 1995.
54. SCHARFMAN, H. E., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37: 693-707, 1990.
55. SCHARFMAN, H. E. AND SCHWARTZKROIN, P. A. Electrophysiology of morphologically-identified dentate hilar "mossy" cells in rat hippocampal slices. J. Neurosci. 8: 3812-3821, 1988.
56. SCHARFMAN, H. E. AND SCHWARTZKROIN, P. A. Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246: 257-260, 1989.
57. SCHARFMAN, H. E. AND SCHWARTZKROIN, P. A. Responses of cells of the rat fascia dentata to prolonged stimulation of the perforant path: sensitivity of hilar cells and changes in granule cell excitability. Neuroscience 35: 491-504, 1990.
58. SCHWEITZER, J. S., PATRYLO, P. R., AND DUDEK, F. E. Prolonged field bursts in the dentate gyrus: dependence on low calcium, high potassium and nonsynaptic mechanisms. J. Neurophysiol. 68: 2016-2025, 1992.
59. SLOVITER, R. S. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235: 73-76, 1987.
60. SLOVITER, R. S. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett. 137: 91-96, 1992.
61. SPRUSTON, N., JAFFE, D. B., WILLIAMS, S. H., AND JOHNSTON, D. Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70: 781-802, 1993.
62. STALEY, K., OTIS, T. S., AND MODY, I. Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J. Neurophysiol. 67: 1346-1358, 1992.
63. STANFIELD, B. B. Excessive intra- and supragranular mossy fibers in the dentate gyrus of tottering (tg/tg) mice. Brain Res. 480: 294-299, 1989.
64. SUTULA, T., CASCINO, G., CAVAZOS, J., PARADA, I., AND RAMIREZ, L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26: 321-330, 1989.
65. SUTULA, T., HE, X.-X., CAVAZOS, J., AND SCOTT, G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239: 1147-1150, 1988.
66. SUTULA, T., ZHANG, P., LYNCH, M., SAYIN, U., GOLARAI, G., AND ROD, R. Synaplic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J. Comp. Neurol. 390: 578-594, 1998.
67. TAUCK, D. L. AND NADLER, J. V. Evidence of functional mossy fiber sprouting in the hippocampal formation of kainic acid-treated rats. J. Neurosci. 5: 1016-1022, 1985.
68. WANG, S.S.-H. AND AUGUSTINE, G. J. Confocal imaging and local photolysis of caged compounds: dual probes of synaptic function. Neuron 15: 755-760, 1995.
69. WEISSKOPF, M. G. AND NICOLL, R. A. Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. Nature 376: 256-259, 1995.
70. WUARIN, J.-P. AND DUDEK, F. E. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rat. J. Neurosci. 16: 4438-4448, 1996.