Neuronal Cell Death in a Rat Model for Mesial Temporal Lobe Epilepsy Is Induced by the Initial Status Epilepticus and Not by Later Repeated Spontaneous Seizures

Summary:  Purpose: To determine whether repeated seizures contribute to hippocampal sclerosis, we investigated whether cell loss in the (para) hippocampal region was related to the severity of chronic seizure activity in a rat model for temporal lobe epilepsy (TLE).

[1]  E. Chang,et al.  Neuronal injury and loss after traumatic brain injury: time course and regional variability , 2001, Brain Research.

[2]  J. S. Duncan,et al.  A Longitudinal Quantitative MRI Study of Community-Based Patients with Chronic Epilepsy and Newly Diagnosed Seizures: Methodology and Preliminary Findings , 2001, NeuroImage.

[3]  M Kokaia,et al.  Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Winblad,et al.  Immunohistochemical localization of interleukin-1β, interleukin-1 receptor antagonist and interleukin-1β converting enzyme/caspase-1 in the rat brain after peripheral administration of kainic acid , 1999, Neuroscience.

[5]  D. Fujikawa,et al.  Lithium‐pilocarpine‐induced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats , 1999, The European journal of neuroscience.

[6]  L. Schmued,et al.  Temporal progression of kainic acid induced neuronal and myelin degeneration in the rat forebrain , 2000, Brain Research.

[7]  J. Cavazos,et al.  Erratum: Progressive neuronal loss induced by kindling: A possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis (Brain Research, 527 (1990) 1-6) , 1991 .

[8]  R. Sapolsky,et al.  Neuronal apoptosis in acute necrotic insults: why is this subject such a mess? , 1999, Trends in Neurosciences.

[9]  A. Pitkänen,et al.  Status Epilepticus Causes Necrotic Damage in the Mediodorsal Nucleus of the Thalamus in Immature Rats , 2001, The Journal of Neuroscience.

[10]  Dirk Troost,et al.  Induction of neonatal sodium channel II and III α‐isoform mRNAs in neurons and microglia after status epilepticus in the rat hippocampus , 2001, The European journal of neuroscience.

[11]  K. Gale,et al.  Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus. , 2000, Brain research. Molecular brain research.

[12]  M. van Lookeren Campagne,et al.  Microwave-enhanced in situ end-labeling of fragmented DNA: parametric studies in relation to postmortem delay and fixation of rat and human brain. , 1995, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[13]  M. Ingvar,et al.  The nature and timing of excitotoxic neuronal necrosis in the cerebral cortex, hippocampus and thalamus due to flurothyl-induced status epilepticus , 2004, Acta Neuropathologica.

[14]  G. Holmes,et al.  Phenobarbital modifies seizure‐related brain injury in the developing brain , 1994, Annals of neurology.

[15]  G. Holmes,et al.  Comparison of valproate and phenobarbital treatment after status epilepticus in rats , 1998, Neurology.

[16]  M Ingvar,et al.  Status epilepticus in well–oxygenated rats causes neuronal necrosis , 1985, Annals of neurology.

[17]  Edward H Bertram,et al.  Self-sustaining limbic status epilepticus induced by ‘continuous’ hippocampal stimulation: electrographic and behavioral characteristics , 1989, Epilepsy Research.

[18]  A. M. Dam,et al.  Epilepsy and Neuron Loss in the Hippocampus , 1980, Epilepsia.

[19]  J. Cavazos,et al.  Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Frederick Andermann,et al.  Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy , 1999, Annals of neurology.

[21]  R. Sankar,et al.  Granule Cell Neurogenesis After Status Epilepticus in the Immature Rat Brain , 2000, Epilepsia.

[22]  C. Jack,et al.  Progressive hippocampal atrophy in chronic intractable temporal lobe epilepsy , 1999, Annals of neurology.

[23]  E. Lothman,et al.  Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat , 1993, Brain Research.

[24]  P. Gloor,et al.  Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures , 1994, Epilepsy Research.

[25]  L. Covolan,et al.  Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus , 2000, Epilepsy Research.

[26]  R. S. Sloviter,et al.  Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat , 1996, The Journal of comparative neurology.

[27]  Asla Pitkänen,et al.  Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy. , 2002, Progress in brain research.

[28]  R. Post,et al.  Apoptosis of hippocampal neurons after amygdala kindled seizures. , 1998, Brain research. Molecular brain research.

[29]  B. Hermann,et al.  Hippocampal malformation as a cause of familial febrile convulsions and subsequent hippocampal sclerosis. , 1999, Neurology.

[30]  A. Pitkänen,et al.  More evidence for seizure-induced neuron loss , 2001, Neurology.

[31]  L. Covolan,et al.  Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine‐ or kainate‐induced status epilepticus , 2000 .

[32]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. II. Motor seizure. , 1972, Electroencephalography and clinical neurophysiology.

[33]  A. Pitkänen,et al.  Recurrent seizures may cause hippocambal damage in temporal lobe epilepsy , 1998, Neurology.

[34]  A. Nehlig,et al.  Magnetic Resonance Imaging in the Study of the Lithium–Pilocarpine Model of Temporal Lobe Epilepsy in Adult Rats , 2002, Epilepsia.

[35]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[36]  Y. Koninck,et al.  Differential progression of Dark Neuron and Fluoro-Jade labelling in the rat hippocampus following pilocarpine-induced status epilepticus , 2000, Neuroscience.

[37]  William Slikker,et al.  Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration , 1997, Brain Research.

[38]  R. Schwarcz,et al.  Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  Thomas P. Sutula,et al.  Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis , 1990, Brain Research.

[40]  E. Aronica,et al.  Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin‐immunoreactive neurons , 2001, The European journal of neuroscience.

[41]  J. Price,et al.  Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: A histological study , 1980, Neuroscience.

[42]  T. Halonen,et al.  Status epilepticus-induced neuronal damage in the rat amygdaloid complex: distribution, time-course and mechanisms , 1999, Neuroscience.

[43]  R. Racine,et al.  Nerve Growth Factor Accelerates Seizure Development, Enhances Mossy Fiber Sprouting, and Attenuates Seizure-Induced Decreases in Neuronal Density in the Kindling Model of Epilepsy , 1997, The Journal of Neuroscience.

[44]  E. Bertram,et al.  The hippocampus in experimental chronic epilepsy: A morphometric analysis , 1990, Annals of neurology.

[45]  S. Ben‐Sasson,et al.  Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation , 1992, The Journal of cell biology.

[46]  G. Jackson,et al.  Hippocampal Sclerosis: Development in Adult Life , 1999, Developmental Neuroscience.

[47]  G. Paxinos.  The Rat nervous system , 1985 .

[48]  Luiz E. A. M. Mello,et al.  Spontaneous seizures preferentially injure interneurons in the pilocarpine model of chronic spontaneous seizures , 1996, Epilepsy Research.

[49]  T. Babb,et al.  The pathogenic and progressive features of chronic human hippocampal epilepsy , 1996, Epilepsy Research.

[50]  N. Kyprianou,et al.  Relationship between DNA fragmentation and apoptosis in the programmed cell death in the rat prostate following castration , 1989, The Prostate.

[51]  G. Holmes,et al.  Anticonvulsant action and long-term effects of gabapentin in the immature brain , 2001, Neuropharmacology.

[52]  S. Moshé,et al.  Hippocampal sclerosis revisited , 1998, Brain and Development.