Structural and functional asymmetry in the normal and epileptic rat dentate gyrus

Journal of Comparative Neurology

Volumn 454, Issue 4, 2002, Pages 424-439

  Scharfman, Helen E ^a,b   Sollas, Anne L ^a   Smith, Karen L ^c   Jackson, Meyer B ^d   Goodman, Jeffrey H ^a  

^a HELEN HAYES HOSPITAL   (United States)

^b College of Physicians and Surgeons ^*  (United States)

^c WADSWORTH CENTER   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Brain derived neurotrophic factor (BDNF); Mossy fiber sprouting; Neuropeptide Y (NPY); Pilocarpine; Seizure; Voltage dependent dyes

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; KAINIC ACID; NEUROPEPTIDE Y; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; DENTATE GYRUS; EPILEPSY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; IMAGING; MALE; MICROELECTRODE; MOSSY FIBER; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENTATE GYRUS; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID AGONISTS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MALE; MOSSY FIBERS, HIPPOCAMPAL; MUSCARINIC AGONISTS; NEUROPEPTIDE Y; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; STATUS EPILEPTICUS; SYNAPSES;

EID: 0037164603     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10449     Document Type: Article

References (74)

1. Acsady L, Kamondi A, Sik A, Freund TF, Buzsaki G. 1998. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18:3386-3403.
2. Alger BE, Teyler TJ. 1976. Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res 110:463-480.
3. Amaral DG. 1978. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851-914.
4. Amaral DG, Campbell MJ. 1986. Transmitter systems in the primate dentate gyrus. Hum Neurobiol 5:169-180.
5. Baimbridge KG. 1992. Calcium-binding proteins in the dentate gyrus. Epilepsy Res Suppl 7:211-220.
6. Blackstad TW, Brink K, Hem J, Jeune B. 1970. Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods. J Comp Neurol 138:433-450.
7. Cadete-Leite A, Brandao F, Andrade JP, Ribeiro da Silva A, Paula-Barbosa MM. 1997. The GABAergic system of the dentate gyrus after withdrawal from chronic alcohol consumption: Effects of intracerebral grafting and putative neuroprotective agents. Alcohol 32:471-484.
8. Claiborne BJ, Amaral DG, Cowan WM. 1986. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J Comp Neurol 246:435-458.
9. Claiborne BJ, Amaral DG, Cowan WM. 1990. Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206-219.
10. Croll SD, Suri C, Compton DL, Simmons MV, Yancopoulos GD, Lindsay RM, Weigand SJ, Scharfman HE. 1999. Brain-derived neurotrophic factor (BDNF) transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93:1491-1506.
11. Czeh G, Seress L, Houser CR. 1997. Number and distribution of GAD65 mRNA-containing neurons in the rat hippocampal formation. Neurobiology (Bp) 5:116.
12. Deller T, Leranth C. 1990. Synaptic connections of neuropeptide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus. J Comp Neurol 300:433-447.
13. Demir R, Haberly LB, Jackson MB. 1998. Voltage imaging of epileptiform activity in slices from rat piriform cortex: Onset and propagation. J Neurosci 80:2727-2742.
14. Dietrich D, Clusmann H, Cral T, Steinhauser C, Blumcke I, Heinemann U, Schramm J. 1999. Two electrophysiologically distinct types of granule cells in epileptic human hippocampus. Neuroscience 90:1197-1206.
15. Dudek FE, Obenaus A, Schweitzer JS, Wuarin JP. 1994. Functional significance of hippocampal plasticity in epileptic brain: Electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus 4:259-265.
16. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA. 1995. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36:543-558.
17. Freund TF. 1992. GABAergic septal and serotonergic median raphe afferents preferentially innervate inhibitory interneurons in the hippocampus and dentate gyrus. Epilepsy Res Suppl 7:79-91.
18. Freund TF, Magloczky Z. 1993. Early degeneration of calretinin-containing neurons in the rat hippocampus after ischemia. Neuroscience 56:581-596.
19. Frotscher M, Zimmer J. 1983. 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.
20. Frotscher M, Soriano E, Leranth C. 1992. Cholinergic and GABAergic neurotransmission in the fascia dentata: Electron microscopic immunocytochemical studies in rodents and primates. Epilepsy Res Suppl 7:65-78.
21. Frotscher M, Soriano E, Misgeld U. 1994. Divergence of hippocampal mossy fibers. Synapse 16:148-160.
22. Gaarskjaer FB. 1981. The hippocampal mossy fiber system of the rat studied with retrograde tracing techniques. Correlation between topographic organization and neurogenetic gradients. J Comp Neurol 203:717-735.
23. Gariboldi M, Conti M, Cavaleri D, Samani R, Vezzani A. 1998. Anticonvulsant properties of BIBP3226, a non-peptide selective antagonist at neuropeptide Y Y1 receptors. Eur J Neurosci 10:757-759.
24. Goodman JH, Scharfman HE. 1999. Co-variation of hyperexcitability and mossy fiber sprouting along the septotemporal axis of the rat hippocampus. Soc Neurosci Abstr 25:847.
25. Gruber B, Greber S, Rupp E, Sperk G. 1994. Differential NPY mRNA expression in granule cells and interneurons of the rat dentate gyrus after kainic acid injection. Hippocampus 4:474-482.
26. Gulyas AI, Miettinen R, Jacobowitz DM, Freund TF. 1992. 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 48:1-27.
27. Gulyas AI, Hajos N, Freund TF. 1996. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
28. Hara H, Onodera H, Kogure K, Akaike N. 1990. The regional difference of neuronal susceptibility in the dentate gyrus to hypoxia. Neurosci Lett 115:189-194.
29. Heinemann U, Beck H, Dreier JP, Ficker E, Stabel J, Zhang CL. 1992. The dentate gyrus as a regulated gate for the propagation of epileptiform activity. Epilepsy Res Suppl 7:273-280.
30. Jackson MB, Scharfman HE. 1996. Positive feedback from hilar mossy cells to granule cells in the dentate gyrus revealed by voltage-sensitive dye and microelectrode recording. J Neurophysiol 76:601-616.
31. Jiang M, Swann JW. 1997. Expression of calretinin in diverse neuronal populations during development of rat hippocampus. Neuroscience 81:1137-1154.
32. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
33. Leranth C, Nitsch R, Deller T, Frotscher M. 1992. Synaptic connections of seizure-sensitive neurons in the dentate gyrus. Epilepsy Res Suppl 7:49-64.
34. Liu YB, Lio PA, Pasternak JF, Trommer BL. 1996. Developmental changes in membrane properties and postsynaptic currents of granule cells in rat dentate gyrus. J Neurophysiol 76:1074-1088.
35. Lothman EW, Stringer JL, Bertram EH. 1992. The dentate gyrus as a control point for seizures in the hippocampus and beyond. Epilepsy Res Suppl 7:301-313.
36. Martinez A, Ruiz M, Soriano E. 1999. Spiny calretinin-immunoreactive neurons in the hilus and CA3 region of the rat hippocampus: Local axon circuits, synaptic connections, and glutamate acid decarboxylase 65/67 mRNA expression. J Comp Neurol 404:438-448.
37. Miettinen R, Gulyas AI, Baimbridge KG, Jacobowitz DM, Freund TF. 1992. Calretinin is present in non-pyramidal cells of the rat hippocampus. II. Co-existence with other calcium binding proteins and GABA. Neuroscience 48:29-43.
38. Milner T, Veznedaroglu E. 1992. Ultrastructural localization of neuropeptide Y-like immunoreactivity in the rat hippocampal formation. Hippocampus 2:107-125.
39. Molnar P, Nadler JV. 1999. Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation. J Neurophysiol 82:1883-1894.
40. Nitsch R, Leranth C. 1993. Calretinin immunoreactivity in the monkey hippocampal formation. II. Intrinsic GABAergic and hypothalamic non-GABAergic systems: An experimental tracing and co-existence study. Neuroscience 55:797-812.
41. Nitsch R, Leranth C. 1996. GABAergic neurons in the rat dentate gyrus are innervated by subcortical calretinin-containing afferents. J Comp Neurol 625:425-438.
42. Okazaki MM, Evenson DA, Nadler JV. 1995. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin. J Comp Neurol 352:515-534.
43. Okazaki MM, Molnar P, Nadler JV. 1999. Recurrent mossy fiber pathway in rat dentate gyrus: Synaptic currents evoked in presence and absence of seizure-induced growth. J Neurophysiol 81:1645-1460.
44. Oleskevich S, Descarries L. 1990. Quantified distribution of the serotonin innervation in adult rat hippocampus. Neuroscience 34:19-33.
45. Oleskevich S, Descarries L, Lacaille JC. 1989. Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J Neurosci 9:3803-3015.
46. Patrylo PR, Dudek FE. 1998. Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J Neurophysiol 79:418-429.
47. Pollard H, Bugra K, Khrestchatisky M, Represa A, Ben-Ari Y. 1996. Seizure-induced molecular changes, sprouting and synaptogenesis of hippocampal mossy fibers. Epilepsy Res Suppl 12:355-363.
48. Racine RJ. 1972. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
49. Represa A, Jorquera I, Le Gal La Salle G, Ben-Ari Y. 1993. Epilepsy induced collateral sprouting of hippocampal mossy fibers: Does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus 3:257-268.
50. Ribak CE, Peterson GM. 1991. Intragranular mossy fibers in rats and gerbils form synapses with the somata and proximal dendrites of basket cells in the dentate gyrus. Hippocampus 1:355-364.
51. Scharfman HE. 1997. Hyperexcitability in combined entorhinal/hippocampal slices of adult rat after exposure to brain-derived neurotrophic factor. J Neurophysiol 78:1082-1095.
52. Scharfman HE, Sarvey JM. 1985. Postsynaptic firing during repetitive stimulation is required for long-term potentiation in hippocampus. Brain Res 331:267-274.
53. Scharfman HE, Goodman JH, Sollas AL. 1999. Actions of BDNF in slices from rats with spontaneous seizures and mossy fiber sprouting in the dentate gyrus. J Neurosci 19:5619-5631.
54. Scharfman HE, Goodman JH, Sollas AL. 2000. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: Functional implications of seizure-induced neurogenesis. J Neurosci 20:6144-6158.
55. Schwarzer C, Williamson JM, Lothman EW, Vezzani A, Sperk G. 1995. Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience 69:831-845.
56. Seress L, Pokorny J. 1981. Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J Anat 133:181-195.
57. Simonyi A, Miller LA, Sun GY. 2000. Region-specific decline in the expression of metabotropic glutamate receptor mRNA in rat brain during aging. Mol Brain Res 82:101-106.
58. Sloviter RS. 1982. A simplified Timm stain procedure compatible with formaldehyde fixation and routine paraffin embedding of rat brain. Brain Res Bull 8:771-774.
59. Sloviter RS. 1989. Calcium-binding protein (Calbindin D28K) and parvalbumin immunocytochemistry: Localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizures activity. J Comp Neurol 280:183-196.
60. Sloviter RS. 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.
61. Sutula TP, Golarai G, Cavozos J. 1992. Assessing the functional significance of mossy fiber sprouting. Epilepsy Res Suppl 7:251-259.
62. Sutula T, Zhang P, Lynch M, Sayin U, Golarai G, Rod R. 1998. Synaptic 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.
63. Steward O, Scoville SA. 1976. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347-370.
64. Tamamaki N, Nojyo Y. 1993. Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus 3:471-480.
65. Tauck DL, Nadler JV. 1985. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
66. Turski L, Cavalheiro EA, Calderazzo-Filho LS, Bortolotto ZA, Klockgether T, Ikonomidou C, Turski WA. 1989. Review: Cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: A novel experimental model of intractable epilepsy. Synapse 3:154-171.
67. Vezzani A, Schwarzer C, Lothman EW, Williamson JM, Sperk G. 1996. Functional changes in somatostatin and neuropeptide Y containing neurons in the rat hippocampus in chronic models of limbic seizures. Epilepsy Res 26:267-279.
68. Vezzani A, Ravizza T, Moneta D, Conti M, Borroni A, Rizzi M, Samanin R, Maj R. 1999a. Brain-derived neurotrophic factor immunoreactivity in the limbic system of rats after acute seizures and during spontaneous convulsions: Temporal evolution of changes as compared to neuropeptide Y. Neuroscience 90:1445-1461.
69. Vezzani A, Sperk G, Colmers WF. 1999b. Neuropeptide Y: Emerging evidence for a functional role in seizure modulation. Trends Neurosci 22:25-30.
70. Wang S, Scott BW, Wojtowicz JM. 2000. Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257.
71. Wenzel HJ, Wooley CS, Robbins CA, Schwartzkroin PA. 2000. Kainic acid-induced mossy fiber sprouting and synapse formation in the dentate gyrus of rats. Hippocampus 10:244-260.
72. Woodson W, Nitecka L, Ben-Ari Y. 1989. Organization of the GABAergic system in the rat hippocampal formation: A quantitative immunocytochemical study. J Comp Neurol 280:254-271.
73. Wu JY, Cohen LB. 1993. Fast multisite optical measurements of membrane potential. In: Mason WT, editor. Fluorescent and Luminescent Probes for Biological Activity. London: Academic press. p 389-404.
74. Wuarin JP, Dudek FE. 1996. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 16:4438-4448.