Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T23:04:03.033Z Has data issue: false hasContentIssue false
  • English
  • Français

Pathogenesis of Mesial Temporal Sclerosis

Published online by Cambridge University Press:  18 September 2015

C. Elizabeth Pringle ,
T. Blume Warren ,
G. Munoz David  and
L. Stan Leung
C. Elizabeth Pringle*
Affiliation:
Department of Clinical Neurological Sciences (C.E.P., W.T.B.); Department of Pathology (Neuropathology) (D.G.M.); Department of Physiology (L.S.L.), University of WesternOntario, London
T. Blume Warren
Affiliation:
Department of Clinical Neurological Sciences (C.E.P., W.T.B.); Department of Pathology (Neuropathology) (D.G.M.); Department of Physiology (L.S.L.), University of WesternOntario, London
G. Munoz David
Affiliation:
Department of Clinical Neurological Sciences (C.E.P., W.T.B.); Department of Pathology (Neuropathology) (D.G.M.); Department of Physiology (L.S.L.), University of WesternOntario, London
L. Stan Leung
Affiliation:
Department of Clinical Neurological Sciences (C.E.P., W.T.B.); Department of Pathology (Neuropathology) (D.G.M.); Department of Physiology (L.S.L.), University of WesternOntario, London
*
University Hospital, 339 Windermere, London, Ontario, Canada N6A 5A5
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A relationship between epilepsy and damage to mesial temporal structures has long been recognized. Recent advances have clarified somewhat the issue of whether the pathological changes seen in mesial temporal sclerosis represent the cause or the effect of seizures. This paper reviews mesial temporal sclerosis from an historical perspective and summarizes recent developments in the fields of excitotoxicity, selective vulnerability, and synaptic reorganization as they pertain to the pathogenesis of mesial temporal sclerosis.

Type
Research Article
Information
Canadian Journal of Neurological Sciences , Volume 20 , Issue 3 , August 1993 , pp. 184 - 193
Copyright
Copyright © Canadian Neurological Sciences Federation 1993

References

REFERENCES

1.Earle, KA, Baldwin, M, Penfield, W. Incisural sclerosis and temporal lobe seizures produced by hippocampal herniation at birth. Arch Neurol Psychiat 1953; 69: 27–42.CrossRefGoogle ScholarPubMed
2.Margerison, JH, Corsellis, JAN. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy with particular reference to the temporal lobes. Brain 1966; 89: 499–530.CrossRefGoogle Scholar
3.Falconer, MA, Taylor, DC. Surgical treatment of drug-resistant epilepsy due to mesial temporal sclerosis. Arch Neurol 1968; 19: 353–361.CrossRefGoogle ScholarPubMed
4.Bruton, CJ. The Neuropathology of Temporal Lobe Epilepsy. New York: Oxford University Press 1988.Google Scholar
5.Broca, P. Anatomie comparée des circonvolutions cérébrales. Le grand lobe limbique et la scissure dans la série des mammifères. Rev Anthropol Paris 1878; 2: 285–498.Google Scholar
6.Papez, JW. A proposed mechanism of emotion. Arch Neurol Psychiatry 1937; 38: 725–743.CrossRefGoogle Scholar
7.MacLean, PD. Some psychiatric implications of physiological studies on frontotemporal portion of limbic system. Electro-encephalogr Clin Neurophysiol 1952; 4: 407–418.CrossRefGoogle ScholarPubMed
8.Lopes, da Silva FH, Witter, MP, Boeijinga, PH, Lohman, AHM. Anatomic organization and physiology of the limbic cortex. Physiological Reviews 1990; 70: 453–511.CrossRefGoogle Scholar
9.Lorente, de Nó R. Studies on the structure of the cerebral cortex II. Continuation of the study of the Ammonic system. J Psychol Neurol 1934; 46: 113–177.Google Scholar
10.Amaral, DG, Insausti, R. Hippocampal formation. In: Paxinos, G, ed. The Human Nervous System. San Diego: Academic Press 1990; 711–755.CrossRefGoogle Scholar
11.Rose, M. Der Allocortex bei tier und mensch. J Psychol Neurol 1926; 34: 1–99.Google Scholar
12.Lacaille, J-C, Schwartzkroin, PA. Stratum lacunosum-moleculare interneurons of hippocampal CA, region. I. Intracellular response characteristics, synaptic responses, and morphology. J Neurosci 1988; 8(4): 1400–1410.Google Scholar
13.Sloviter, RS. 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 1991; 1: 41–66.CrossRefGoogle ScholarPubMed
14.Sloviter, RS, Damiano, BP. On the relationship between kainic acid-induced epileptiform activity and hippocampal neuronal damage. Neuropharmacology 1981; 20: 1003–1011.CrossRefGoogle ScholarPubMed
15.Sloviter, RS. “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 1983; 10: 675–697.Google ScholarPubMed
16.Scharfman, HE, Schwartzkroin, PA. Electrophysiology of morphologically identified mossy cells of the dentate hilus recorded in guinea pig hippocampal slices. J Neurosci 1988; 8(10): 3812–3821.CrossRefGoogle ScholarPubMed
17.Scharfman, HE, Schwartzkroin, PA. 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 1990; 35: 491–504.CrossRefGoogle ScholarPubMed
18.Witter, MP. Connectivity of the rat hippocampus. In: Chan-Palay, V, Kôhler, C, eds. The Hippocampus—New Vistas Neurology and Neurobiology. New York: Liss 1989: 53–69.Google Scholar
19.Witter, MP, Amaral, DG, Van, Hoesen GW. The entorhinal-dentate projection in the macaque monkey: topographical organization along the longitudinal axis of the hippocampus. J Neurosci 1989: 9: 216–228.CrossRefGoogle Scholar
20.Ramón, y Cajal S. Estructura del asta de Amnion. Anat Soc Esp Histol Nat Madrid. 1893; 22: 53–114.Google Scholar
21.Blackstad, TW. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 1956; 105: 417–537.CrossRefGoogle ScholarPubMed
22.Rosene, DL, Van, Hoesen GW. The hippocampal formation of the primate brain. A review of some comparative aspects of cytoar-chitecture and connections. In: Jones, EG and Peters, A, eds. Cerebral Cortex, Vol. 6. New York: Plenum Press 1987; 345–456.CrossRefGoogle Scholar
23.Houser, CR, Miyashiro, JE, Swartz, BE, Walsh, GO, Rich, JR. Delgado-Escueta, AV. Altered patterns of dynorphin immunore-activity suggest mossy fibre reorganization in human hippocampal epilepsy. J Neurosci 1990; 10: 267–282.CrossRefGoogle Scholar
24.Bouchet, C, Cazauvieilh, JB. De l'epilepsie considérée dans ses rapports avec l'aliénation mentale. Arch Gen Med 1825; 9: 510–542.Google Scholar
25.Meynert, T. Studien über das pathologisch-anatomiche material der Weine Irren-Anstalt. Vierteljahrssch Psychiat 1868; 3: 381–402.Google Scholar
26.Sommer, W. Erkrankung des Ammonshorns als aetiologische moment der epilepsie. Arch Psychiat Nervenkr 1880; 10: 631–675.CrossRefGoogle Scholar
27.Pfleger, L. Beobachtungen über Schrumpfung und Sklerose des Ammonshorns bei Epilepsie. Allg Z Psychiat 1880; 36: 359–365.Google Scholar
28.Spielmeyer, W. Die Pathogenese des epileptischen Krampfanfalles Histopathologischer Teil. Z Dtsch Gesellsch Neurol Psychiat 1927; 109: 501–520.CrossRefGoogle Scholar
29.Scholz, W. Die Krampfschädigungen des Gehirns. Monographien Gesamtgeb Neurol Psychiat 1951; 75, Berlin: Springer.Google Scholar
30.Gastaut, H. Colloque sur les problèmes d'anatomie normale et pathologique poses par les décharges epileptiques. Bruxelles: Editions Acta Medica Bélgica 1956; 5–20.Google Scholar
31.Meyer, A, Falconer, MA, Beck, E. Pathological findings in temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 1954; 17: 276–285.CrossRefGoogle ScholarPubMed
32.Norman, RM. The neuropathology of status epilepticus. Med Sei Law 1964; 4: 46–51.CrossRefGoogle ScholarPubMed
33.Ounsted, C, Lindsay, J, Norman, R. Biological factors in temporal lobe epilepsy. Clin Dev Med. London: Heinemann Medical 1966; 22.Google Scholar
34.Veith, G. Anatomische Studie über die Ammonshornsklerose im epileptikergehirn. Deutsche Zeitschrift fur Nervenheilkunde 1970; 197: 293–314.Google Scholar
35.Rocca, WA, Sharbrough, FW, Hauser, WA, Annegers, JF, Schoenberg, BS. Risk factors for complex partial seizures: a population-based case-control study. Ann Neurol 1987; 21: 22–31.CrossRefGoogle ScholarPubMed
36.Sagar, HJ, Oxbury, JM. Hippocampal neuron loss in temporal lobe epilepsy: correlation with early childhood convulsions. Ann Neurol 1987; 22: 334–340.CrossRefGoogle ScholarPubMed
37.Mouritzen-Dam, A.Epilepsy and neuron loss in the hippocampus. Epilepsia 1980; 21: 617–629.Google Scholar
38.Babb, TL, Lieb, JP, Brown, WJ, Pretorius, J, Crandall, PH. Distribution of pyramidal cell density and hyperexcitability in the epileptic human hippocampal formation. Epilepsia 1984a; 25: 721–728.CrossRefGoogle ScholarPubMed
39.Babb, TL, Brown, WJ, Pretorius, J, Davenport, C, Lieb, JP, et al.Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 1984b; 25: 729–740.CrossRefGoogle ScholarPubMed
40.Meldrum, BS, Brierley, JB. Neuronal loss and gliosis in the hippocampus following repetitive epileptic seizures induced in adolescent baboons by allylglycine. Brain Res 1972; 48: 361–365.CrossRefGoogle ScholarPubMed
41.Meldrum, BS, Brierley, JB. Prolonged epileptic seizures in primates. Arch Neurol 1973; 28: 10–17.CrossRefGoogle ScholarPubMed
42.Meldrum, BS, Vigouroux, RA, Brierley, JB. Systemic factors and epileptic brain damage. Arch Neurol 1973; 29: 82–87.CrossRefGoogle ScholarPubMed
43.Meldrum, BS, Horton, RW, Brierley, JB. Epileptic brain damage in adolescent baboons following seizures induced by allylglycine. Brain 1974; 97: 407–418.CrossRefGoogle Scholar
44.Meldrum, BS, Nilsson, B. Cerebral blood flow and metabolic rate early and late in prolonged epileptic seizures induced in rats by bicuculline. Brain 1976; 99: 523–542.CrossRefGoogle ScholarPubMed
45.Meldrum, BS. Metabolic effects of prolonged epileptic seizures and the causation of epileptic brain damage. In: Rose, RC, ed. Metabolic Disorders of the Nervous System. London: Pitman 1981; 175–187.Google Scholar
46.Blennow, G, Brierley, JB, Meldrum, BS, Siesjo, BK. Epileptic brain damage: the role of systemic factors that modify cerebral energy metabolism. Brain 1978; 101: 687–700.CrossRefGoogle ScholarPubMed
47.Babb, TL, Brown, WJ. Pathological findings in epilepsy. In: Engel, J Jr, ed. Surgical Treatment of the Epilepsies. New York: Raven Press 1987; 22: 511–540.Google Scholar
48.Soderfeldt, B, Kalimo, H, Olsson, Y, Siesjo, BK. Histopathologic changes in the rat brain during bicuculline-induced status epilep-ticus. In: Delgado-Escueta, AV, Wasterlain, CG, Treiman, DM, Porter, RJ. eds. Advances in Neurology, Vol. 34: Status Epilepticus. New York: Raven Press 1983; 169–175.Google Scholar
49.Auer, RN, Siesjo, BK. Biological differences between ischaemia, hypoglycemia and epilepsy. Ann Neurol 1988; 24: 699–707.CrossRefGoogle ScholarPubMed
50.Howse, DC. Cerebral energy metabolism during experimental status epilepticus. In: Delgado-Escueta, AV, Wasterlain, CG, Treiman, DM, Porter, RJ, eds. Advances in Neurology, Vol. 34: Status Epilepticus. New York: Raven Press 1983; 209–216.Google Scholar
51.Blennow, G, Nilsson, B, Siesjo, BK. Sustained epileptic seizures complicated by hypoxia, arterial hypotension or hyperthermia: effects on cerebral energy state. Acta Physiol Scand 1977; 100: 126–128.CrossRefGoogle ScholarPubMed
52.Chapman, A, Meldrum, BS, Siesjo, BK. Cerebral metabolic changes during prolonged epileptic seizures in rats. J Neurochem 1977; 28: 1025–1035.CrossRefGoogle ScholarPubMed
53.Olney, JW, Ho, OL, Rhee, V. Cytotoxic effects of acidic and sulphur-containing amino acids on the infant mouse CNS. Exp Brain Res 1972; 14: 61–76.Google Scholar
54.Olney, JW, Rhee, V, Ho, OL. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res 1974; 77: 507–512.CrossRefGoogle ScholarPubMed
55.Olney, JW. Neurotoxicity of excitatory amino acids. In: McGeer, EG, Olney, JW, McGeer, PL, eds. Kainic Acid as a Tool in Neurobiology. New York: Raven Press 1978; 95–121.Google Scholar
56.Buzsáki, G. Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 1984; 22: 131–153.CrossRefGoogle ScholarPubMed
57.Lomo, T. Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation. Exp Brain Res 1971; 12: 18–45.CrossRefGoogle Scholar
58.Eccles, JC. Excitatory and inhibitory mechanisms in brain. In: Jasper, HH, Ward, AA Jr, Pope, A, eds. Basic Mechanisms of the Epilepsies. Boston: Little, Brown and Company 1969; 229–252.Google Scholar
59.Cotman, CW, Monaghan, DT, Ottersen, OP, Storm-Mathisen, J. Anatomical organization of excitatory amino acid receptors and their pathways. Trends Neurosci 1987; 10: 273–280.CrossRefGoogle Scholar
60.Miller, RJ. The revenge of the kainate receptor. Trends Neurosci 1991; 14: 477–479.CrossRefGoogle ScholarPubMed
61.Lino, M, Ozawa, S, Tsuzuki, K. Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J Physiol 1990; 424: 151–165.Google Scholar
62.Andersen, P. Properties of glutamate excitation of hippocampal pyramidal cells. In: Roberts, PJ, Storm-Mathisen, J, Johnston, GAR, eds. Glutamate: Transmitter in the Central Nervous System. Chichester, UK: Wiley 1981; 25–33.Google Scholar
63.Fonnum, F. Glutamate: a neurotransmitter in mammalian brain. J Neurochem 1984; 42: 1–11.CrossRefGoogle ScholarPubMed
64.Hablitz, JJ, Langmoen, IA. Excitation of hippocampal pyramidal cells by glutamate in the guinea-pig and rat. J Physiol Lond 1982; 325: 317–331.CrossRefGoogle ScholarPubMed
65.Madison, DV, Lancaster, B, Nicoll, RA. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 1987; 7: 733–741.CrossRefGoogle ScholarPubMed
66.Haas, HL. Cholinergic disinhibition in hippocampal slices of the rat. Brain Res 1982; 233: 200–204.CrossRefGoogle ScholarPubMed
67.Krnjevic, K, Ropert, N, Casullo, J. Septohippocampal disinhibition. Brain Res 1988; 438: 182–192.CrossRefGoogle ScholarPubMed
68.Seress, L, Ribak, CE. GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp Brain Res 1983; 50: 173–182.Google ScholarPubMed
69.Alger, BE, Nicoll, RA. Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro. J Physiol Lond 1982; 328: 125–141.CrossRefGoogle ScholarPubMed
70.Crunelli, V, Assaf, SY, Kelly, JS. Intracellular recording from granule cells of the dentate gyrus in vitro. In: Seifert, W, ed. Neurobiology of the Hippocampus. London: Academic 1983; 197–214.Google Scholar
71.Wong, RKS, Watkins, DJ. Cellular factors influencing GABA response in hippocampal pyramidal cells. J Neurophysiol 1982; 48: 938–951.CrossRefGoogle ScholarPubMed
72.Numann, RE, Wong, RKS. Voltage-clamp study on GABA response desensitization in single pyramidal cells dissociated from the hippocampus of adult guinea pigs. Neurosci Lett 1984; 47: 289–294.CrossRefGoogle Scholar
73.Crawford, IL, Connor, JD. Localization and release of glutamic acid in relation to the hippocampal mossy fibre pathway. Nature 1973; 244: 442–443.CrossRefGoogle Scholar
74.Storm-Mathisen, J, Leknes, JAK, Bore, AT, Line, Vaaland J, Edminson, P, et al.First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 1983; 301: 517–520.CrossRefGoogle ScholarPubMed
75.Rofhman, SM, Thurston, JH, Hauhart, RE. Delayed neurotoxicity of excitatory amino acids in vitro. Neuroscience 1987; 22: 471–480.CrossRefGoogle Scholar
76.Sloviter, RS, Dempster, DW. “Epileptic” brain damage is replicated qualitatively in the rat hippocampus by central injection of glutamate or aspartate but not by GABA or acetylcholine. Brain Res Bull 1984; 15: 39–60.CrossRefGoogle Scholar
77.Monaghan, DT, Holets, VR, Toy, DW, Cotman, CW. Anatomical distributions of four pharmacologically distinct 3H-L-glutamate binding sites. Nature 1983; 306: 176–179.CrossRefGoogle ScholarPubMed
78.Rogers, BC, Barnes, MI, Mitchell, CL, Tilson, HA. Functional deficits after sustained stimulation of the perforant path. Brain Res 1989; 493: 41–50.CrossRefGoogle ScholarPubMed
79.Scheibel, ME, Crandall, PH, Scheibel, AB. The hippocanipal-dentate complex in temporal lobe epilepsy. Epilepsia 1974; 15: 55–80.CrossRefGoogle ScholarPubMed
80.Olney, JW, Fuller, T, deGubareff, T. Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res 1979; 76: 91–100.CrossRefGoogle Scholar
81.Nadler, JV, Perry, BW, Cotman, CW. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 1978; 271:676–677.CrossRefGoogle ScholarPubMed
82.Sloviter, RS, Damiano, BP. Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiologic effects and hippocampal damage in rats. Neurosci Lett 1981; 24: 279–284.CrossRefGoogle ScholarPubMed
83.Nadler, JV. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 1981; 29: 2031–2042.CrossRefGoogle Scholar
84.Ben-Ari, Y, Tremblay, E, Ottersen, OP, Meldrum, BS. The role of epileptic activity in hippocampal and ‘remote’ cerebral lesions induced by kainic acid. Brain Res 1980; 191: 79–97.CrossRefGoogle ScholarPubMed
85.Nadler, JV, Cuthbertson, GJ. Kainic acid neurotoxicity toward hip-pocampal formation: dependence on specific excitatory pathways. Brain Res 1980; 195: 47–56.CrossRefGoogle Scholar
86.Cavazos, J, Sutula, T. Progressive neuronal loss induced by kindling: a possible mechanism in mossy fibre reorganization and hippocampal sclerosis [Abstract], Epilepsia 1989; 30: 702.Google Scholar
87.Cavazos, JE, Sutula, TP. Progressive neuronal loss induced by kindling: a possible mechanism for mossy fibre synaptic reorganization and hippocampal sclerosis. Brain Res 1990; 527: 1–6.CrossRefGoogle Scholar
88.Turski, WA, Cavalheiro, EA, Schwarz, M, Czuczwar, SJ, Kleinrok, Z, et al.Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res 1983; 9: 315–335.CrossRefGoogle ScholarPubMed
89.Turski, WA, Cavalheiro, EA, Coimbra, C, da, Penha Berzaghi M, Ikonomidou-Turski, C, et al.Only certain antiepileptic drugs prevent seizures induced by pilocarpine. Brain Res Rev 1987; 12: 281–305.CrossRefGoogle Scholar
90.Nadler, JV, Perry, BW, Cotman, CW. Selective reinnervation of hippocampal area CA, and the fascia dentata after destruction of CA3 and CA4 afferents with kainic acid. Brain Res 1980; 182: 1–9.CrossRefGoogle Scholar
91.Frotscher, M, Zimmer, J. Lesion-induced mossy fibres to the molecular layer of the rat fascia dentata: identification of postsynaptic granule cells by the golgi-EM technique. J Comp Neurol 1983; 215: 299–311.CrossRefGoogle Scholar
92.Represa, A, Robain, O, Tremblay, E, Ben-Ari, Y. Hippocampal plasticity in childhood epilepsy. Neurosci Lett 1989; 99: 351–355.CrossRefGoogle ScholarPubMed
93.Sutula, T, Cascino, G, Cavazos, J, Parada, I, Ramirez, L. Mossy fibre synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989; 26: 321–330.CrossRefGoogle ScholarPubMed
94.de, Lanerolle NC, Kim, JH, Robbins, RJ, Spencer, D. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 1989; 495: 387–395.Google Scholar
95.Nadler, JV, Perry, BW, Gentry, C, Cotman, CW. Loss and reacquisition of hippocampal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res 1980; 191: 387–403.CrossRefGoogle ScholarPubMed
96.Represa, A, Tremblay, E, Ben-Ari, Y. Kainate binding sites in the hippocampal mpssy fibres: localization and plasticity. Neuroscience 1987; 20: 739–748.CrossRefGoogle ScholarPubMed
97.Sutula, T, Xiao-Xian, H, Cavazos, J, Scott, G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 1988; 239: 1147–1150.CrossRefGoogle ScholarPubMed
98.Tauck, DL, Nadler, JV. Evidence of functional mossy fibre sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 1985; 5: 1016–1022.CrossRefGoogle ScholarPubMed
99.Gall, CM, Isackson, PJ. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 1989; 245: 758–761.CrossRefGoogle ScholarPubMed
100.Springer, JE, Loy, R. Intrahippocampal injections of antiserum to nerve growth factor inhibit sympathohippocampal sprouting. Brain Res Bull 1985; 15: 629–634.CrossRefGoogle ScholarPubMed
101.Thoenen, H, Bandtlow, C, Heumann, R. The physiological function of nerve growth factor in the central nervous system: comparison with the periphery. Rev Physiol Biochem Pharmacol 1987; 109: 146–178.Google ScholarPubMed
102.Gahwiler, BH, Enz, A, Hefti, F. Nerve growth factor promotes development of the rat septo-hippocampal cholinergic projection in vitro. Neurosci Lett 1987; 75: 6–10.CrossRefGoogle ScholarPubMed
103.Goddard, GV, Mclntyre, DC, Leech, CK. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 1969; 25: 295–330.CrossRefGoogle ScholarPubMed
104.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 1991; 7: 165–l76.CrossRefGoogle ScholarPubMed
105.Gloor, P. Epilepsy: relationships between electrophysiology and intracellular mechanisms involving second messengers and gene expression. Can J Neurol Sci 1989; 16: 8–21.CrossRefGoogle ScholarPubMed
106.White, JD, Gall, CM, McKelvey, JF. Enkephalin biosynthesis and enkephalin gene expression are increased in hippocampal mossy fibres following a unilateral lesion of the hilus. J Neurosci 1987; 7: 753–759.CrossRefGoogle ScholarPubMed
107.Morris, BJ, Feasey, KJ, Bruggencate, GT, Herz, A, Höllt, V. Electrical stimulation in vivo increases the expression of pro-dynorphin m-RNA in rat hippocampal granule cells. Proc Natl Acad Sci USA 1988; 85: 3226–3230.CrossRefGoogle Scholar
108.Evans, M, Griffiths, T, Meldrum, BS. Early changes in the rat hippocampus following seizures induced by bicuculline or L-allyl-glycine: a light and electron microscopy study. Neuropathol Appl Neurobiol 1983; 9: 39–52.CrossRefGoogle ScholarPubMed
109.Griffiths, T, Evans, M, Meldrum, BS. Intracellular calcium accumulation in rat hippocampus during seizures induced by bicuculline or L-allylglycine. Neuroscience 1983; 10: 385–395.CrossRefGoogle ScholarPubMed
110.Rothman, S, Olney, J. Excitotoxicity and the NMDA receptor. Trends Neurosci 1987; 10: 299–302.CrossRefGoogle Scholar
111.Fifkova, E, Van, Harreveld A. Long-lasting morphological changes in dendritic spines of dentate granule cells following stimulation of the entorhinal area. J Neurocytol 1977; 6: 211–230.CrossRefGoogle Scholar
112.Kandel, ER, Schwartz, JH. Directly gated transmission at central synapses. In: Kandel, ER, Schwartz, JH and jessel, TM, eds. Principles of Neuroscience, Third edition. New York: Elsevier, 1991; 153–172.Google Scholar
113.Choi, DW. Calcium mediated neurotoxicity: relationship to specific channel types and role in ischaemic damage. Trends Neurosci 1988; 11:465–469.CrossRefGoogle Scholar
114.Kudo, Y, Ito, K, Miyakawa, H, Izumi, Y, Ogura, A, et al.Cytoplasmic calcium elevation in hippocampal granule cells induced by perforant path stimulation and L-glutamate application. Brain Res 1987; 407: 168–172.CrossRefGoogle ScholarPubMed
115.Krnjevic, K, Morris, ME, Ropert, N. Changes in free calcium ion concentration recorded inside hippocampal pyramidal cells in situ. Brain Res 1986; 374: 1–11.CrossRefGoogle ScholarPubMed
116.Connor, JA, Wadman, WJ, Hockberger, PE, Wong, RKS. Sustained dendritic gradients of Ca2+ induced by excitatory amino acids in CA, hippocampal neurons. Science 1988; 240: 649–653.CrossRefGoogle Scholar
117.Sloviter, RS. Calcium binding protein (calbindin-D28K) and paralbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 1989; 280: 183–196.CrossRefGoogle Scholar
118.Baimbridge, KG, Mody, I, Miller, JJ. Reduction of rat hippocampal calcium-binding protein following commissural, amygdala, septal, perforant path and olfactory bulb kindling. Epilepsia 1985; 26: 460–465.CrossRefGoogle ScholarPubMed
119.Kamphuis, W, Huisman, E, Wadman, WJ, Heizmann, CW, Lopes, da Silva FH. Kindling-induced changes in parvalbumin immunore-activity in rat hippocampus and its relation to long-term decrease in GAB A immunoreactivity. Brain Res 1989; 479: 23–24.CrossRefGoogle Scholar
120.Iacangelo, A, Affolter, H-U, Eiden, LE, Herbert, E, Grimes, M. Bovine chromogranin-A: sequence and distribution of its messenger RNA in endocrine tissues. Nature 1986; 323: 82–86.CrossRefGoogle ScholarPubMed
121.Munoz, DG. The distribution of chromogranin A-like immunoreactivity in the human hippocampus coincides with the pattern of resistance to epilepsy-induced neuronal damage. Ann Neurol 1990; 27: 266–275.CrossRefGoogle ScholarPubMed
122.Ottersen, OP, Madsen, S, Meldrum, BS, Storm-Mathisen, J. Taurine in the hippocampal formation of the Sengalese baboon, Papio papio: an immunocytocherpical study with an antiserum against conjugated taurine. Exp Brain Res 1985; 59: 457–462.CrossRefGoogle Scholar
123.Storm-Mathisen, J, Iversen, LL. Uptake of [3H] glutamic acid in excitatory nerve endings: light “and electron microscopic observations in the hippocampal formation of the rat. Neuroscience 1979; 4: 1237–1253.CrossRefGoogle Scholar
124.Storm-Mathisen, J, Wold, JE. In vivo high affinity uptake and axonal transport of D-[2-3-3H]aspartate in excitatory neurons. Brain Res 1981; 230: 427–433.CrossRefGoogle Scholar
125.Taxt, T, Storm-Mathisen, J. Uptake of D-aspartate and L-glutamate in excitatory axon terminals in hippocampus: autoradiographic and biochemical comparison with GABA and other amino acids in normal rats and in rats with lesions. Neuroscience 1984; 11: 79–100.CrossRefGoogle ScholarPubMed
126.Heggli, DE, Aamodt, A, Malthe-Sorenssen. Kainic acid neurotoxicity: effect of systemic injection on neurotransmitter markers in different brain regions. Brain Res 1981; 230: 261–262.CrossRefGoogle ScholarPubMed
127.McNamara, JO.The neurobiological basis of epilepsy. Trends Neurosci 1992; 15:357–359.CrossRefGoogle ScholarPubMed