Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: The 'irritable mossy cell' hypothesis

Journal of Physiology

Volumn 524, Issue 1, 2000, Pages 117-134

  Santhakumar, Vijayalakshmi ^a,b   Bender, Roland ^c   Frotscher, Michael ^c   Ross, Stephen T ^a   Hollrigel, Greg S ^a   Toth, Zsolt ^a   Soltesz, Ivan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 AMINOPHENYL) 3,4 DIHYDRO 4 METHYL 3 METHYLCARBAMOYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR ANTAGONIST; BICUCULLINE; CELL PROTEIN; GADOLINIUM 67; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PARVALBUMIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HEAD INJURY; INTERNEURON; MALE; NERVE CELL EXCITABILITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; ADULT; CALCIUM CELL LEVEL; CELL POPULATION; CYTOCHEMISTRY; DENTATE GYRUS GRANULAR LAYER; MEMORY DISORDER; MOSSY FIBER; NERVE CELL STIMULATION; NERVE POTENTIAL; SEIZURE; WHOLE CELL PATCH CLAMP;

EID: 0034177955     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-7793.2000.00117.x     Document Type: Article

References (61)

1. AMARAL, D. G. (1978). A Golgi study of cell types in the hilar region of the hippocampus in the rat. Journal of Comparative Neurology 182, 851-914.
2. ANNEGERS, J. F., GRABOW, J. D., GROOVER, R. V., LAWS, E. R. JR, EIVEBACK, L. R. & KURKLAND, L. T. (1980). Seizures after head trauma: A population study. Neurology 30, 683-689.
3. ASIKAINEN, I., KASTE, M. & SARNA, S. (1999). Early and late posttraumatic seizures in traumatic brain injury rehabilitation patients: brain injury factors causing late seizures and influence of seizures on long-term outcome. Epilepsia 40, 584-589.
4. BERNARD, C., ESCLAPEZ, M., HIRSCH, J. C. & BEN-ARI, Y. (1998). Interneurones are not so dormant in temporal lobe epilepsy: a critical reappraisal of the dormant basket cell hypothesis. Epilepsy Research 32, 93-103.
5. BINDER, L. M. (1986). Persisting symptoms after mild head injury: a review of the postconcussive syndrome. Journal of Clinical and Experimental Neuropsychology 8, 323-346.
6. BRAMLETT, H. M., GREEN, E. J. & DIETRICH, W. D. (1997). Hippocampally dependent and independent chronic spatial navigational deficits following parasagittal fluid percussion brain injury in the rat. Brain Research 762, 195-202.
7. BRUTON, C. (1988). The Neuropathology of Temporal Lobe Epilepsy. Oxford University Press, New York.
8. BUCKMASTER, P. S. & DUDEK, F. E. (1997). Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. Journal of Neurophysiology 77, 2685-2696.
9. BUCKMASTER, P. S. & SCHWARTZKROIN, P. A. (1994). Hippocampal mossy cell function: a speculative view. Hippocampus 4, 393-402.
10. BUCKMASTER, P. S., STROWBRIDGE, B. W., KUNKEL, D. D., SCHMIEGE, D. L. & SCHWARTZKROIN, P. A. (1992). Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2, 349-362.
11. BUCKMASTER, P. S., STROWBRIDGE, B. W. & SCHWARTZKROIN, P. A. (1993). A comparison of rat hippocampal mossy cells and CA3c pyramidal cells. Journal of Neurophysiology 70, 1281-1299.
12. BUHL, E. H., OTIS, T. S. & MODY, I. (1996). Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271, 309-373.
13. BUZSÁKI, G., LEUNG, L. W. & VANDERWOLF, C. H. (1983). Cellular bases of hippocampal EEG in the behaving rat. Brain Research 287, 139-171.
14. CAVAZOS, J. E., GOLARAI, G. & SUTULA, T. P. (1992). Septotemporal variation of the supragranular projection of the mossy fiber pathway in the dentate gyrus of normal and kindled rats. Hippocampus 2, 363-372.
15. CELIO, M. R., BAIER, W., SCHÄRER, L., DE VIRAGH, P. A. & GERDAY, C. (1988). Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9, 81-86.
16. CHEN, K., BARAM, T. Z. & SOLTESZ, I. (1999). Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits. Nature Medicine 5, 888-894.
17. COULTER, D. A., RAFIQ, A., SHUMATE, M., GONG, Q. Z., DELORENZO, R. J. & LYETH, B. G. (1996). Brain injury-induced enhanced limbic epileptogenesis: anatomical and physiological parallels to an animal model of temporal lobe epilepsy. Epilepsy Research 6, 81-91.
18. DELLER, T., MARTINEZ, A., NITSCH, R. & FROTSCHER, M. (1990). A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. Journal of Neuroscience 16, 3322-3333.
19. DIXON, C. E., LYETH, B. G., POVLISHOCK, J. T., FINDLING, R. L., HAMM, R. J., MARMAROU, A., YOUNG, H. F. & HAYES, H. L. (1989). A fluid percussion model of experimental brain injury in the rat. Journal of Neurosurgery 67, 110-119.
20. EPSTEIN, P., MEANS, A. R. & BERCHTOLD, M. W. (1986). Isolation of a rat parvalbumin gene and full length cDNA. Journal of Biological Chemistry 261, 5886-5891.
21. ERLANDER, M. G., TILLAKARATNE, N. J. K., FELDBLUM, S., PATEL, N. & TOBIN, A. J. (1991). Two genes encode distinct glutamate decarboxylases. Neuron 7, 91-100.
22. FREUND, T. F. & BUZSÁKI, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 345-470.
23. FROTSCHER, M., SERESS, L., SCHWERDTFEGER, W. K. & BUHL., E. (1991). The mossy cells of the fascia dentata: a comparative study of their fine structure and synaptic connections in rodents and primates. Journal of Comparative Neurology 312, 145-163.
24. GRABER, K. D. & PRINCE, D. A. (1999). Tetrodotoxin prevents post-traumatic epileptogenesis in rats. Annals of Neurology 46, 234-242.
25. GRADY, M. S. & LAM, A. M. (1995). Management of acute head injury. In Anesthetic Management of Head Injury, ed. LAM, A. M., pp. 87-100. McGraw-Hill, Inc., NY, USA.
26. HOLLRIGEL, G. S. & SOLTESZ, I. (1997). Slow kinetics of miniature [PSCs during early postnatal development in granule cells of the dentate gyrus. Journal of Neuroscience 17, 5119-5128.
27. HOLLRIGEL, G. S., TOTH, K. & SOLTESZ, I. (1996). Neuroprotection by propofol in acute mechanical injury: role of GABAergic inhibition. Journal of Neurophysiology 76, 2412-2422.
28. HOUSER, C. K. & ESCLAPEZ, M. (1994). Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus 4, 530-545.
29. HSU, M. & BUZSÁKI, G. (1993). Vulnerability of mossy fiber targets in the rat hippocampus to forebrain ischemia. Journal of Neuroscience 13, 3964-3979.
30. JACKSON, M. B. & SCHARFMAN, H. E. (1990). Positive feedback from hilar mossy cells to granule cells in the dentate gyrus revealed by voltage-sensitive dye and microelectrode recording. Journal of Neurophysiology 76, 601-616.
31. JEFFERYS, J. G. R. & THAUB, R. D. (1998). 'Dormant' inhibitory neurons: do they exist and what is their functional impact? Epilepsy Research 32, 104-113.
32. JENG, J.-M., TOTH, Z. & SOLTESZ, I. (1998). Rapid increase in excitatory glutamatergic drive to dentate interneurons following head trauma. Society for Neuroscience Abstracts 129.9.
33. JENNET, B. (1975). Epilepsy After Non-missile Head Injuries. W. Heinemann Medical Books, UK.
34. JENNETT, H. & LEWIN, W. (1960). Traumatic epilepsy after closed head injuries. Journal of Neurology, Neurosurgery and Psychiatry 23, 295-301.
35. LERÁNTH, C., SZEIDEMANN, Z., HSU, M. & BUZSÁKI, G. (1996). AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most interneurons. Neuroscience 70, 631-652.
36. LEROUX, P. D. & GRADY, M. S. (1995). Epidemology of head injury. In Anesthetic Management of Head Injury, ed. LAM, A. M., pp. 1-11. McGraw-Hill, Inc., NY, USA.
37. LISMAN, J. E. (1999). Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22, 233-242.
38. LORENTE DE No, R. (1934). Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. Journal of Psychology and Neurology Leipzig 46, 113-177.
39. LOWENSTEIN, D. H., THOMAS, M. J., SMITH, D. H. & MCINTOSH, T. K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. Journal of Neuroscience 12, 4846-4853.
40. LÜBKE, J., FROTSCHER, M. & SPRUSTON, N. (1998). Specialized electrophysiological properties of anatomically identified neurons in the hilar region of the rat fascia dentata. Journal of Neurophysiology 79, 1518-1034.
41. MCINTOSH, T. K., VINK, R., NOBLE, L., YAMAKAMI, I., FERNYAK, S., SOARES, H. & FADEN, A. L. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244.
42. MARGERISON, J. H. & CORSELLIS, J. A. (1966). Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89, 499-530.
43. POVLISHOCK, J. T., HAYES, R. L., MICHEL, M. E. & MCINTOSH, T. K. (1994). Workshop on animal models of traumatic brain injury. Journal of Neurotrauma 11, 723-732.
44. PRINCE, D. A. & JACOBS, K. (1998). Inhibitory function in two models of chronic epileptogenesis. Epilepsy Research 32, 83-92.
45. REMPEL-CLOWER, N. L., ZOLA, S. M., SQUIRE, L. R. & AMARAL, D. G. (1996). Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. Journal of Neuroscience 16, 5233-5255.
46. +-ATPase function and long-lasting amplification of inhibition in the dentate gyrus. Society for Neuroscience Abstracts 398.8.
47. SALAZAR, A. M. (1992). Traumatic brain injury: the continuing epidemic. In Challenges in Neurology, ed. HACHINSKI, V. C., pp. 55-67. Davis, Philadelphia, PA, USA.
48. SCHARFMAN, H. E. (1992). Differentiation of rat dentate neurons by morphology and electrophysiology in hippocampal slices: granule cells, spiny hilar neurons, and 'fast spiking' cells. Epilepsy Research, suppl. 7, 93-109.
49. SCHARFMAN, H. E. (1995). Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. Journal of Neurophysiology 74, 179-194.
50. SCHARFMAN, H. E. & SCHWARTZKROIN, P. A. (1989). Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246, 257-200.
51. 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.
52. SLOVITER, R. S. (1994). On the relationship between neuropathology and pathophysiology in the epileptic hippocampus of humans and experimental animals. Hippocampus 4, 250-253.
53. SOLTESZ, I., BOURASSA, J. & DESCHENES, M. (1993). The behavior of mossy cells of rat dentate gyrus during theta oscllations in vivo. Neuroscience 57, 555-564.
54. SOLTESZ, I. & MODY, I. (1994). Patch-clamp recordings reveal powerful GABAergic inhibition in dentate hilar neurons. Journal of Neuroscience 14, 2365-2370.
55. 2+-dependent plasticity of miniature inhibitory postsynaptic currents after amputation of dendrites in central neurons. Journal of Neurophysiology 73, 1763-1773.
56. SOLTESZ, I., SMETTERS, D. K. & MODY, I. (1995). Tonic inhibition originates from synapses close to the soma. Neuron 14, 1273-1283.
57. SORIANO, E. & FROTSCHER, M. (1994). Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus 4, 65-69.
58. STROWBRIDCE, B. W. & SCHWARTZKROIN, P. A. (1996). Transient potentiation of spontaneous EPSPs in rat mossy cells induced by depolarization of a single neurone. Journal of Physiology 494, 493-510.
59. STUART, G. J., DODT, H. U. & SAKMANN, B. (1993). Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Archiv 423, 511-518.
60. TOTH, Z., HOLLRIGEL, G. S., GORCS, T. & SOLTESZ, I. (1997). Instantaneous perturbation of interneuronal networks by a pressure wave-transient delivered to the neocortex. Journal of Neuroscience 17, 8106-8117.
61. WILLMORE, L. J. (1997). Prophylactic treatment. In Epilepsy: A Comprehensive Textbook, ed. ENGEL, J. & PEDLEY, T. A., pp. 1333-1337. Lippincott-Raven Publishers, Philadelphia, PA, USA.