Seminars in Ultrasound, CT and MRI
Volume 29, Issue 1 , Pages 2-14 , February 2008

Hippocampal Sclerosis: Histopathology Substrate and Magnetic Resonance Imaging

  • Ramón Palacios Bote, MD

      Affiliations

    • Department of Radiology, Infanta Cristina Hospital, Complejo Hospitalario Universitario de Badajoz (CHUB) Servicio Extremeño de Salud (SES), Badajoz, Spain.
    • Corresponding Author InformationAddress reprint requests to: Ramón Palacios Bote, MD, C/C/ Zurbarán no. 16 2nd C-Z, 06002 Badajoz, Spain.
    • ,
  • Lidia Blázquez-Llorca, BSc

      Affiliations

    • Departament of Neuroanatomy and Cell Biology, Instituto Cajal (CSIC), Madrid, Spain.
    • ,
  • M. Ángeles Fernández-Gil, MD

      Affiliations

    • Department of Radiology, Infanta Cristina Hospital, Complejo Hospitalario Universitario de Badajoz (CHUB) Servicio Extremeño de Salud (SES), Badajoz, Spain.
    • ,
  • Lidia Alonso-Nanclares, PhD

      Affiliations

    • Departament of Neuroanatomy and Cell Biology, Instituto Cajal (CSIC), Madrid, Spain.
    • ,
  • Alberto Muñoz, PhD

      Affiliations

    • Departament of Neuroanatomy and Cell Biology, Instituto Cajal (CSIC), Madrid, Spain.
    • Departament of Cell Biology, Faculty of Biology, Universidad Complutense, Madrid, Spain.
    • ,
  • Javier De Felipe, PhD

      Affiliations

    • Departament of Neuroanatomy and Cell Biology, Instituto Cajal (CSIC), Madrid, Spain.

References 

  1. Falconer MA, Serafetinides EA, Corsellis JA. Etiology and pathogenesis of temporal lobe epilepsy. Arch Neurol. 1964;10:233–248
  2. Babb TL, Brown WJ. Pathological findings in epilepsy. In:  Engel J editors. Surgical Treatment of the Epilepsies. New York, NY: Raven Press; 1987;p. 511–540
  3. Falconer MA. Mesial temporal (Ammon’s horn) sclerosis as a common cause of epilepsy (Aetiology, treatment, and prevention). Lancet. 1974;2:767–770
  4. Houser CR. Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv Neurol. 1999;79:743–761
  5. Meldrum BS, Bruton CJ. Epilepsy. In:  Adams J,  Duchen LW editor. Greenffield’s Neuropathology. London: Arnold; 1992;p. 1246–1283
  6. Babb TL, Pretorius JK. Pathologic substrates of epilepsy. In:  Wyllie E editors. The Treatment of Epilepsy: Principles and Practice. Philadelphia, PA: Lea & Freiberg; 1993;p. 55–70
  7. Honavar M, Meldrum BS. Epilepsy. In:  Graham DI,  Lantos PL editor. Greenfield’s Neuropathology. London: Arnold; 1997;p. 931–971
  8. Wieser HG, Yasargil MG. Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy. Surg Neurol. 1982;17:445–457
  9. Wieser HG. Selective amygdalohippocampectomy: indications and follow-up. Can J Neurol Sci. 1991;18:617–627
  10. Wieser HG. Epilepsy surgery. Baillieres Clin Neurol. 1996;5:849–875
  11. Mayanagi Y, Watanabe E, Kaneko Y. Mesial temporal lobe epilepsy: clinical features and seizure mechanism. Epilepsia. 1996;37(suppl 3):57–60
  12. Alarcon G, Garcia Seoane JJ, Binnie CD, et al. Origin and propagation of interictal discharges in the acute electrocorticogram (Implications for pathophysiology and surgical treatment of temporal lobe epilepsy). Brain. 1997;120(Pt. 12):2259–2282
  13. DeFelipe J, Garcia Sola R, Marco P, et al. Selective changes in the microorganization of the human epileptogenic neocortex revealed by parvalbumin immunoreactivity. Cereb Cortex. 1993;3:39–48
  14. Marco P, Sola RG, Pulido P, et al. Inhibitory neurons in the human epileptogenic temporal neocortex (An immunocytochemical study). Brain. 1996;119(Pt. 4):1327–1347
  15. Arellano JI, Munoz A, Ballesteros-Yanez I, et al. Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain. 2004;127:45–64
  16. Jones-Gotman M, Zatorre RJ, Olivier A, et al. Learning and retention of words and designs following excision from medial or lateral temporal-lobe structures. Neuropsychologia. 1997;35:963–973
  17. Olivier A. Temporal resections in the surgical treatment of epilepsy. In:  Theodore WH editors. Surgical Treatment of Epilepsy. Amsterdam: Elsevier; 1992;p. 175–188
  18. Houser CR. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 1990;535:195–204
  19. Babb TL, Kupfer WR, Pretorius JK, et al. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 1991;42:351–363
  20. de Lanerolle NC, Kim JH, Robbins RJ, et al. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 1989;495:387–395
  21. Magloczky Z, Wittner L, Borhegyi Z, et al. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience. 2000;96:7–25
  22. Mathern GW, Babb TL, Pretorius JK, et al. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci. 1995;15:3990–4004
  23. Munoz A, Arellano JI, DeFelipe J. GABABR1 receptor protein expression in human mesial temporal cortex: changes in temporal lobe epilepsy. J Comp Neurol. 2002;449:166–179
  24. Munoz A, Mendez P, DeFelipe J, et al. Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia. 2007;48:663–673
  25. Sloviter RS, Sollas AL, Barbaro NM, et al. Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol. 1991;308:381–396
  26. Sutula T, Cascino G, Cavazos J, et al. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol. 1989;26:321–330
  27. Wittner L, Eross L, Szabo Z, et al. Synaptic reorganization of calbindin-positive neurons in the human hippocampal CA1 region in temporal lobe epilepsy. Neuroscience. 2002;115:961–978
  28. Avanzini G, Engel J, Fariello R, et al. Neurotransmitters in Epilepsy. Amsterdam: Elsevier; 1992;
  29. Bausch SB. Axonal sprouting of GABAergic interneurons in temporal lobe epilepsy. Epilepsy Behav. 2005;7:390–400
  30. Bernard C, Cossart R, Hirsch JC, et al. What is GABAergic inhibition? (How is it modified in epilepsy?). Epilepsia. 2000;41(suppl 6):S90–S95
  31. DeFelipe J. Chandelier cells and epilepsy. Brain. 1999;122(Pt. 10):1807–1822
  32. Houser CR. GABA neurons in seizure disorders: a review of immunocytochemical studies. Neurochem Res. 1991;16:295–308
  33. Lloyd KG, Bossi L, Morselli PL, et al. Alterations of GABA-mediated Synaptic transmission in human epilepsy. In:  Delgado-Escueta AV,  Ward AA,  Woodbury DM, et al. editor. Basic Mechanisms of the Epilepsies. New York, NY: Raven Press; 1986;p. 1033–1044
  34. Prince DA, Connors BW. Mechanisms of interictal epileptogenensis. In:  Delgado-Escueta AV,  Ward AA,  Woodbury DM, et al. editor. Basic Mechanisms of the Epilepsies. New York, NY: Raven Press; 1986;
  35. Ribak C. Epilepsy and the cortex: Anatomy. In:  Peters A,  Jones EG editor. Cerebral Cortex (Normal and Altered States of Function). New York, NY: Plenum Press; 1991;p. 427–483
  36. 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
  37. Corsellis JA. The incidence of Ammon’s horn sclerosis. Brain. 1957;80:193–208
  38. Gloor P. Mesial temporal sclerosis: Historical background and overview from a modern perspective. In:  Lüders H editors. Epilepsy Surgery. New York, NY: Raven Press; 1991;p. 689–703
  39. Haymaker W, Pentschew A, Margoles C, et al. Occurrence of lesions in the temporal lobe in the absence of convulsive seizures. In:  Baldwin M,  Bailey P editor. Temporal Lobe Epilepsy. Springfield, IL: Charles C. Thomas; 1958;p. 166–202
  40. Cavazos JE, Das I, Sutula TP. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci. 1994;14:3106–3121
  41. Fujikawa DG, Itabashi HH, Wu A, Shinmei SS. Status epilepticus-induced neuronal loss in humans without systemic complications or epilepsy. Epilepsia. 2000;41:981–991
  42. Teitelbaum JS, Zatorre RJ, Carpenter S, et al. Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels. N Engl J Med. 1990;322:1781–1787
  43. Ribak CE, Seress L, Weber P, et al. Alumina gel injections into the temporal lobe of rhesus monkeys cause complex partial seizures and morphological changes found in human temporal lobe epilepsy. J Comp Neurol. 1998;401:266–290
  44. Buckmaster PS, Dudek FE. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol. 1997;385:385–404
  45. Mathern GW, Cifuentes F, Leite JP, et al. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr Clin Neurophysiol. 1993;87:326–339
  46. Nakajima S, Franck JE, Bilkey D, et al. Local circuit synaptic interactions between CA1 pyramidal cells and interneurons in the kainate-lesioned hyperexcitable hippocampus. Hippocampus. 1991;1:67–78
  47. Duchowny M. Febrile seizures. In:  Wyllie E editors. Childhood. Philadelphia, PA: Lea & Freiberg; 1993;
  48. Maher J, McLachlan RS. Febrile convulsions (Is seizure duration the most important predictor of temporal lobe epilepsy?). Brain. 1995;118(Pt. 6):1521–1528
  49. Mizrahi EM. Acute and chronic effects of seizures in the developing brain: lessons from clinical experience. Epilepsia. 1999;40(suppl 1):S42–S50discussion S64-S46
  50. Ramos Lizana J, Cassinello Garcia E, Carrasco Marina LL, et al. Seizure recurrence after a first unprovoked seizure in childhood: a prospective study. Epilepsia. 2000;41:1005–1013
  51. Niebauer M, Gruenthal M. Neuroprotective effects of early vs. late administration of dantrolene in experimental status epilepticus. Neuropharmacology. 1999;38:1343–1348
  52. Pitkanen A, Nissinen J, Jolkkonen E, et al. Effects of vigabatrin treatment on status epilepticus-induced neuronal damage and mossy fiber sprouting in the rat hippocampus. Epilepsy Res. 1999;33:67–85
  53. Tandon P, Yang Y, Das K, et al. Neuroprotective effects of brain-derived neurotrophic factor in seizures during development. Neuroscience. 1999;91:293–303
  54. Sapolsky RM, Stein BA. Status epilepticus-induced hippocampal damage is modulated by glucose availability. Neurosci Lett. 1989;97:157–162
  55. Niebauer M, Gruenthal M. Topiramate reduces neuronal injury after experimental status epilepticus. Brain Res. 1999;837:263–269
  56. McBride MC, Bronstein KS, Bennett B, et al. Failure of standard magnetic resonance imaging in patients with refractory temporal lobe epilepsy. Arch Neurol. 1998;55:346–348
  57. Von Oertzen J, Urbach H, Jungbluth S, et al. Standard magnetic resonance imaging is inadequate for patients with refractory focal epilepsy. J Neurol Neurosurg Psychiatry. 2002;73:643–647
  58. Jack CR, Rydberg CH, Krecke KN, et al. Mesial temporal sclerosis: diagnosis with fluid-attenuated inversion-recovery versus spin-echo MR imaging. Radiology. 1996;199:367–373
  59. Bronen RA. Epilepsy: the role of MR imaging. AJR Am J Roentgenol. 1992;159:1165–1174
  60. Lee DH, Gao FQ, Rogers JM, et al. MR in temporal lobe epilepsy: analysis with pathologic confirmation. AJNR Am J Neuroradiol. 1998;19:19–27
  61. Jackson GD, Connelly A, Duncan JS, et al. Detection of hippocampal pathology in intractable partial epilepsy: increased sensitivity with quantitative magnetic resonance T2 relaxometry. Neurology. 1993;43:1793–1799
  62. Wieser HG. ILAE Commission Report (Mesial temporal lobe epilepsy with hippocampal sclerosis). Epilepsia. 2004;45:695–714
  63. Farina L, Bergqvist C, Zimmerman RA, et al. Acute diffusion abnormalities in the hippocampus of children with new-onset seizures: the development of mesial temporal sclerosis. Neuroradiology. 2004;46:251–257
  64. Killgore WD, Glosser G, Casasanto DJ, et al. Functional MRI and the Wada test provide complementary information for predicting post-operative seizure control. Seizure. 1999;8:450–455
  65. Kuzniecky R, de la Sayette V, Ethier R, et al. Magnetic resonance imaging in temporal lobe epilepsy: pathological correlations. Ann Neurol. 1987;22:341–347
  66. Bronen RA, Anderson AW, Spencer DD. Quantitative MR for epilepsy: a clinical and research tool?. AJNR Am J Neuroradiol. 1994;15:1157–1160
  67. Vattipally VR, Bronen RA. MR imaging of epilepsy: strategies for successful interpretation. Magn Reson Imaging Clin North Am. 2006;14:225–247
  68. Chan S, Erickson JK, Yoon SS. Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics. 1997;17:1095–1110
  69. Oppenheim C, Dormont D, Biondi A, et al. Loss of digitations of the hippocampal head on high-resolution fast spin-echo MR: a sign of mesial temporal sclerosis. AJNR Am J Neuroradiol. 1998;19:457–463
  70. Van Paesschen W, Connelly A, Johnson CL, et al. The amygdala and intractable temporal lobe epilepsy: a quantitative magnetic resonance imaging study. Neurology. 1996;47:1021–1031
  71. Miller LA, McLachlan RS, Bouwer MS, et al. Amygdalar sclerosis: preoperative indicators and outcome after temporal lobectomy. J Neurol Neurosurg Psychiatry. 1994;57:1099–1105
  72. Meiners LC, Witkamp TD, de Kort GA, et al. Relevance of temporal lobe white matter changes in hippocampal sclerosis (Magnetic resonance imaging and histology). Invest Radiol. 1999;34:38–45
  73. Papez JW. A proposed mechanism of emotion. 1937. J Neuropsychiatry Clin Neurosci. 1995;7:103–112
  74. Oikawa H, Sasaki M, Tamakawa Y, et al. The circuit of Papez in mesial temporal sclerosis: MRI. Neuroradiology. 2001;43:205–210
  75. Baldwin GN, Tsuruda JS, Maravilla KR, et al. The fornix in patients with seizures caused by unilateral hippocampal sclerosis: detection of unilateral volume loss on MR images. AJR Am J Roentgenol. 1994;162:1185–1189
  76. Mamourian AC, Cho CH, Saykin AJ, et al. Association between size of the lateral ventricle and asymmetry of the fornix in patients with temporal lobe epilepsy. AJNR Am J Neuroradiol. 1998;19:9–13
  77. Squire LR, Amaral DG, Press GA. Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia. J Neurosci. 1990;10:3106–3117
  78. Deasy NP, Jarosz JM, Elwes RC, et al. Thalamic changes with mesial temporal sclerosis: MRI. Neuroradiology. 2000;42:346–351
  79. Oppenheim C, Dormont D, Hasboun D, et al. Bilateral mesial temporal sclerosis: MRI with high-resolution fast spin-echo and fluid-attenuated inversion-recovery sequences. Neuroradiology. 1999;41:471–479
  80. Jack CR, Sharbrough FW, Cascino GD, et al. Magnetic resonance image-based hippocampal volumetry: correlation with outcome after temporal lobectomy. Ann Neurol. 1992;31:138–146
  81. Cendes F, Cook MJ, Watson C, et al. Frequency and characteristics of dual pathology in patients with lesional epilepsy. Neurology. 1995;45:2058–2064
  82. Li LM, Cendes F, Andermann F, et al. Surgical outcome in patients with epilepsy and dual pathology. Brain. 1999;122(Pt. 5):799–805
  83. Cendes F, Knowlton RC, Novotny E, et al. Magnetic resonance spectroscopy in epilepsy: clinical issues. Epilepsia. 2002;43(suppl 1):32–39

PII: S0887-2171(07)00101-1

doi: 10.1053/j.sult.2007.11.005

Seminars in Ultrasound, CT and MRI
Volume 29, Issue 1 , Pages 2-14 , February 2008

Article Tools

* Image Usage & Resolution