Neocortex in the hippocampus: An anatomical and functional study of CA1 heterotopias after prenatal treatment with methylazoxymethanol in rats

Journal of Comparative Neurology

Volumn 394, Issue 4, 1998, Pages 520-536

  Chevassus Au Louis, N ^a   Rafiki, A ^a   Jorquera, I ^a   Ben Ari, Y ^a   Represa, A ^a  

^a INSERM   (France)

Author keywords

Cortical dysplasia; Epilepsy; Limbic system; Microcephaly; Neuronal migration

Indexed keywords

ANIMAL TISSUE; ARTICLE; DYSPLASIA; EPILEPSY; HETEROTOPIA; HIPPOCAMPUS; LIMBIC SYSTEM; MICROCEPHALY; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN MAPPING; BROMODEOXYURIDINE; CELL MOVEMENT; CHORISTOMA; FEMALE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; METHYLAZOXYMETHANOL ACETATE; MITOSIS; NEOCORTEX; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR;

EID: 0032543251     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980518)394:4<520::AID-CNE9>3.0.CO;2-3     Document Type: Article

References (95)

1. Alcantara, S., I. Ferrer, and E. Soriano (1993) Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat. Embryol. 188:63-73.
2. Altman, J. (1973) Experimental reorganization of the cerebellar cortex: III Regeneration of the external germinal layer and granule cells ectopia. J. Comp. Neurol. 149:123-152.
3. Angevine, J.B. and R.L. Sidman (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766-768.
4. Anton, E.S., R.S. Cameron, and P. Rakic (1996) Role of neuron-glial junctional domain proteins in the maintenance and termination of neuronal mígratíon across the embryonic cerebral wall. J. Neurosci. 16:2283-2293.
5. Baraban, S.C. and P.A. Schwartzkroin (1996) Flurothyl seizure susceptibility in rats following prenatal methylazoxymethanol treatment. Epilepsy Res. 23:189-194.
6. Barbe, M.F. and P. Levitt (1991) The early commitment of fetal neurons to the limbic cortex. J. Neurosci. 11:519-533.
7. Barbe, M.F. and P. Levitt (1995) Age-dependent specification of the cortico-cortical connections of cerebral grafts. J. Neurosci. 15:1819-1834.
8. Barkovitch, A.J. and B.O. Kjos (1992) Gray matter heterotopias: MR characteristics and correlation with developmental and neurological manifestations. Radiology 182:493-499.
9. Ben-Ari, Y. (1985) Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
10. Ben-Ari, Y., E. Tremblay, O.P. Ottersen, and B.S. Meldrum (1980) The role of epileptic activity in hippocampal and "remote" cerebral lesions induced by kainic acid. Brain Res. 191:79-97.
11. Ben-Ari, Y., E. Tremhlay, D. Riche, G. Ghilini, and R. Naquet (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6:1361-1391.
12. Berciano, M.T. and M. Lafarga (1988) Colony forming ectopic granule cells in the cerebellar primary fissure of normal adult rats: A morphologic and morphometric study. Brain Res. 439:169-178.
13. Bernardo, K.L. and T.A. Woolsey (1987) Axonal trajectories between mouse somatosensory thalamus and cortex. J. Comp. Neurol. 258:542-564.
14. Bernardo, K.L., P.M. Ma, and T.A. Woolsey (1986) In vitro labeling of axonal projections in the mammalian nervous system. J. Neurosci. Methods 16:89.
15. Berry, M., A.W. Rogers, and J.T. Eayrs (1964) Pattern of cell migration during cortical histogenesis. Nature 203:591-593.
16. Burkhalter, A. (1989) Intrinsic connections of rat primary visual cortex: Laminar organization of axonal projections. J. Comp. Neurol. 279:171-186.
17. Cattabeni, F. and M. Di Luca (1997) Developmental models of brain dysfunctions induced by targeted cellular ablations with methylazoxymethanol. Physiol. Rev. 77:199-215.
18. Cattaneo, E., B. Reinach, A. Caputi, F. Cattabeni, and M. Di Luca (1995) Selective in vitro blockade of neuroepithelial cells proliferation by methylazoxymethanol acetate, a molecule capable of inducing long lasting functional impairments. J. Neurosci. Res. 41:640-647.
19. Caviness, V.S., Jr. (1976) Patterns of cell and fiber distribution in the neocortex of the reeler mutant mice. J. Comp. Neurol. 170:435-448.
20. Chen, S. and D.E. Hillman (1986) Selective ablation of neurons by methylazoxymethanol during pre-and postnatal brain development. Exp. Neurol. 94:103-119.
21. Collier, P.A. and K.W.S. Ashwell (1993) Distribution of neuronal heterotopias following prenatal exposure to methylazoxymethanol. Neurotoxicol. Teratol. 15:439-444.
22. Dambska, M., R. Haddad, P.B. Kozlowski, M.H. Lee, and J. Shek (1982) Telencephalic cytoarchitectonics in the brains of rats with graded degrees of micrencephaly. Acta Neuropathol. (Berl.) 58:203-209.
23. De Feo, M.R., O. Mecarelli, and G.F. Ricci (1995) Seizure susceptibility in immature rats with micrencephaly induced by prenatal exposure to methylazoxymethanol acetate. Pharmacol. Res. 31:109-114.
24. Des Portes, V., J.-M. Pinard, P. Billuart, M.-C. Vinet, A. Kouiakoff, A. Carrié, A. Gélot, A. Dupuis, J. Motte, Y. Berwald-Netter, M. Catala, A. Kahn, C. Beldjord, and J. Chelly (1998) Identification of a novel CNS gene required for neuronal migration and involved in X-linked subcortical heterotopias and lissencephaly syndrome. Cell 92:51-61.
25. Dragunow, M. and R. Faull (1989) The use of c-Fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29:261-265.
26. Dubeau, F., D. Tampieri, N. Lee, E. Andermann, S. Carpenter, R. Leblanc, A. Olivier, R. Radtke, J.-G. Villemure, and F. Andermann (1995) Periventricular and subcortical nodular heterotopia. A study of 33 patients. Brain 118:1273-1287.
27. Ebrahimi-Gaillard, A. and M. Roger (1996) Development of spinal cord projections from neocortical transplants heterotopically placed in the neocortex of newborn hosts is highly dependant on the embryonic locus of origin of the graft. J. Comp. Neurol. 365:129-140.
28. Eksioglu, Y.Z., I.E. Scheffer, P. Cardenas, J. Knol, F. DiMario, G. Ramsby, M. Berg, K. Kamuro, S.F. Berkovic, G.M. Duyk, J. Parisi, PR. Huttenlocher, and C.A. Walsh (1996) Periventricular heterotopia: An X-linked dominant epilepsy locus causing aberrant cerebral cortical development. Neuron 16:77-87.
29. Feldman, M.L. and A. Peters (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J. Comp. Neurol. 179:761-794.
30. Ferrer, I., I. Fabregues, and G. Palacios (1982) An autoradiographic study of methylazoxymethanol acetate-induced cortical malformation. Acta Neuropathol. (Berl.) 57:313-315.
31. Ferrer, I., A. Xumetra, and J. Santamaria (1984) Cerebral malformation induced by prenatal X-irradiation: An autoradiographic and Golgi study. J. Anat. 138:81-93.
32. Ferrer, I., S. Alcantara, M.J. Zujer, and C. Cinos (1993) Structure and pathogenesis of cortical nodules induced by prenatal X-irradiation in the rat. Acta Neuropathol. (Berl. ) 85:205-212.
33. Ferri, R. and P. Levitt (1993) Cerebral cortical progenitors are fated to produce region-specific neuronal populations. Cereb. Cortex 3:187-198.
34. Freund, T.F. and G. Buzsaki (1996) Interneurons of the hippocampus. Hippocampus 6:347-370.
35. Gallyas, F., J.R. Wolff, H. Böttcher, and L. Zaborsky (1980) A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain. Technol. 55:299-306.
36. Garcia-Ladona, F.J., J. de Barry, C. Girard, and G. Gombos (1991) Ectopic granule cell layer in mouse cerebellum after methylazoxymethanol (MAM) treatment. Exp. Brain Res. 86:90-96.
37. Götz, M. and J. Price (1994) Cell fate and axonal projection from the cerebral cortex. Sem. Dev. Biol. 5:359-369.
38. Gressens, P., B.E. Kosofsky, and P. Evrard (1992) Cocaine-induced disturbances of corticogenesis in the developing murine brain. Neurosci. Lett. 140:113-116.
39. Griffin, W.S.T., M.A.E. Eriksson, M. del Cerro, D.J. Woodward, and N. Stampfer (1980) Naturally occurring alterations of cortical layers surrounding the fissura prima of cerebellum. J. Comp. Neurol. 192:109-118.
40. Harding, B. (1996) Gray matter heterotopia. In R. Guerrini, E. Andermann, R. Canapicchi, J. Roger, B. Zilfkin, and P. Pfanner (eds): Dysplasias of the Cerebral Cortex and Epilepsy. Philadelphia: Lippincott-Raven, pp. 81-88.
41. Hicks, S.P., C.J. D'Amato, and M.J. Lowe (1959) The development of the mammalian nervous system: I. Malformation of the brain, especially the cerebral cortex, induced in rats by radiation. II. Some mechanisms of the malformations of the cortex. J. Comp. Neurol. 113:435-469.
42. Jankovski, A., F. Rossi, and C. Sotelo (1996) Neuronal precursors in the postnatal mouse cerebellum are fully committed cells: Evidence from heterochronic transplantations. Eur. J. Neurosci. 8:2308-2319.
43. Jensen, F.E., I.R. Firkusny, and G.D. Mower (1993) Differences in c-Fos immunoreactivity due to age and mode of seizure induction. Mol. Brain Res. 17:185-193.
44. Jensen, K.F. and H.P. Killackey (1984) Subcortical projections from ectopic neocortical neurons. Proc. Natl.Acad. Sci. USA 81-964-968.
45. Johnston, M.V. and J.T. Coyle (1979) Histological and neurochemical effects of fetal treatment with metylazoxymethanol on rat neocortex in adulthood. Brain Res. 170:135-155.
46. Jones, E.G., K.L. Valentino, and J.W. Fleshman (1982) Adjustment of connectivity in rat neocortex after destruction of precursor cells of layers II-IV. Dev. Brain Res. 2:425-431.
47. Kasof, G.M., A. Mandelzys, S.D. Maika, R.E. Hammer, T. Currran, and J.I. Morgan (1995) Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-Fos-lacZ transgenic rats. J. Neurosci. 15:4238-4249.
48. Kennedy, H. and C. Dehay (1993) Cortical specification of mice and men. Cereb. Cortex 3:171-186.
49. Khrestchatisky, M., L. Ferhat, G. Charton, A. Bernard, H. Pollard, A. Represa, and Y. Ben-Ari (1995) Molecular correlates between reactive and developmental plasticity in the rat hippocampus. J. Neurobiol. 26:426-436.
50. Kotti, T., T. Halonen, J. Sirviö, P. Riekkinen, and R. Miettinen (1997) Comparison of NADPH diaphorase histochemistry, somatostatin immunohistochemistry, and silver impregnation in detecting structural and functional impairment in experimental status epilepticus. Neuroscience 80:105-117.
51. Lafarga, M. and M.T. Berciano (1985) A golgi and morphometric study of the ectopic granule cells of the molecular layer of the rat cerebellum. Brain Res. 345:398-401.
52. Larkman, A.U. and A. Mason (1990) Correlations between morphology and electrophysiology of pyramidal neurones in slices of rat visual cortex. I. Establishment of cell classes. J. Neurosci. 10:1407-1414.
53. Lee, K.S., F. Schottler, J.L. Collins, G. Lanzino, D. Couture, A. Rao, K.-I. Hiramatsu, Y. Goto, S.-C. Hong, H. Caner, H. Yamamoto, Z.-F. Chen, E. Bertram, S. Berr, R. Omary, H. Scrable, T. Jackson, J. Goble, and L. Eisenman (1997) A genetic model of human neocortical heterotopia associated with seizures. J. Neurosci. 17:6236-6242.
54. LeGal LaSalle, G. (1988) Long-lasting and sequential increase of c-Fos oncoprotein expression in kainic acid-induced status epilepticus. Neurosci. Lett. 88:127-130.
55. Levitt, P. (1984) A monoclonal antibody to limbic system neurons. Science 223:299-301.
56. Levitt, P. (1985) Relating molecular specificity to normal and anormal brain development. Ann. N.Y. Acad. Sci. 450:239-246.
57. Levitt, P., M.F. Barbe, and K.L. Eagleson (1997) Patterning and specification of the cerebral cortex. Annu. Rev. Neurosci. 20:1-24.
58. Marret, S., P. Gressens, and P. Evrard (1996) Arrest of neuronal migration by excitatory amino acids in hamster developing brain. Proc. Natl. Acad. Sci. USA 93:15463-15468.
59. Matsumoto, H., M. Spatz, and G.L. Laqueur (1972) Quantitative changes with age in the DNA content of methylazoxymethanol-induced microcephalic rat brain. J. Neurochem. 19:297-306.
60. Miller, M.W. (1986) Effects of alcohol on generation and migration of cerebral cortex neurons. Science 233:1308-1311.
61. Miller, M.W. (1987) Effect of prenatal exposure to alcohol on the distribution and time of origin of corticospinal neurons in the rat. J. Comp. Neurol. 257:372-382.
62. Morgan, J.I., D.R. Cohen, J.L. Hempstead, and T. Curran (1987) Mapping patterns of c-Fos expression in the central nervous system after seizure. Science 237:192-197.
63. Moshe, S.L., L. Velisek, and G.L. Holmes (1994) Developmental aspects of experimental generalized seizures induced by pentylenetetrazol, bicuculline and flurothyl. In A. Malafosse, P. Genton, E. Hirsch, C. Marescaux, D. Broglin, and R. Bernasconi (eds): Idiopathic Generalized Epilepsies: Clinical, Experimental and Genetic Aspects. London: John Libbey & Co Ltd., pp. 201-213.
64. Nadler, J.V. and D.A. Evenson (1983) Use of excitatory amino acids to make axon-sparing lesions of hypothalamus. Methods Enzymol. 103:393-400.
65. Nitsch, R., I. Bergmann, K Kuppers, M. Mueller, and M. Frotscher (1990) Late appearance of parvalbumin-immunoreactivity in the development of GABAergic neurons in the rat hippocampus. Neurosci. Lett. 118:147-150.
66. O'Leary, D. (1989) Do cortical areas emerge from a protocortex? Trends Neurosci. 12:400-406.
67. Popovici, T., A. Represa, V. Crépel, G. Barbin, M. Beaudoin, and Y. Ben-Ari (1990) Effects of kainic acid-induced seizures and ischemia on c-Fos like proteins in rat brain. Brain Res. 530:183-194.
68. Rafiki, A., N. Chevassus-au-Louis, Y. Ben-Ari, M. Khrestchatisky, and A. Represa (1998) Glutamate receptors in rat with diffuse cortical dysplasia: An in situ hybridization and immunohistochemical study. Brain Res. 782:141-154.
69. Rakic, P. (1988) Defects of neuronal migration and the pathogenesis of cortical malformations. Prog. Brain Res. 73:15-37.
70. Ramon y Cajal, S. (1911) Histologie du système nerveux central de l'homme et des vertébrés. Paris: Maloine.
71. Reinoso, B.S., A.F. Pimenta, and P. Levitt (1996) Expression of the mRNAs encoding the limbic system-associated membrane protein (LAMP): I. Adult rat brain. J. Comp. Neurol. 375:274-288.
72. Represa, A., J. Niquet, H. Pollard, and Y. Ben-Ari (1995) Cell death, gliosis and synaptic remodeling in the hippocampus of epileptic rats. J. Neurobiol. 26:413-425.
73. Robain, O., L. Lanfumey, J. Adrien, and E. Farkas (1985) Developmental changes in the cerebellar cortex after locus coeruleus lesion with 6-hydroxydopamine in the rat. Exp. Neurol. 88:150-164.
74. Rosen, G.D., G.F. Sherman, J.M. Richman, L.V. Stone, and A.M. Galaburda (1992) Induction of molecular layer ectopias by puncture wounds in newborn rats and mice. Dev. Brain Res. 67:285-291.
75. Sanchez, M.P., C. Frassoni, G. Alvarez-Bolado, R. Spreafico, and A. Fairen (1992) Distribution of calbindin and parvalbumin in the developing somatosensory cortex and its primordium in the rat: An immunocytochemical study. J. Neurocytol. 21:717-736.
76. Saper, C.B. (1996) Any way you count it: a new journal policy for the use of unbiased counting methods. J. Comp. Neurol. 364:5.
77. Schröder, R. and H.J. Luhmann (1997) Morphology, electrophysiology and pathophysiology of supragranular neurons in rat primary somatosensory cortex, Eur. J. Neurosci. 9:163-176.
78. Senba, E., K. Matsunaga, M. Tohyama, and K. Noguchi (1993) Stress-induced c-Fos expression in the rat brain: Activation mechanism of sympathetic pathway. Brain Res. Bull. 31:329-344.
79. Sharp, F.R., S.M. Sagar, K. Hicks, D. Lowenstein, and K. Hisanaga (1991) c-Fos mRNA, FOS, and Fos-related antigen induction by hypertonic saline and stress. J. Neurosci. 11:2321-2331.
80. Sherman, G.F, G.D. Rosen, L.V. Stone, D.M. Press, and A.M. Galaburda (1992) The organization of radial glial fibers in spontaneous ectopias of newborn New Zealand Black mice. Dev. Brain Res. 67:279-283.
81. Sievers, J., U. Mangold, and M. Berry (1985) 6-OHDA-induced ectopia of external granule cells in the subarachnoid space covering the cerebellum. III. Morphology and synaptic organization of ectopic cerebellar neurons: A scanning and transmission electron microscopic study. J. Comp. Neurol. 232:319-330.
82. Singh, S.C. (1977) Ectopic neurons in the hippocampus of the postnatal rat exposed to methylazoxymethanol during fetal development. Acta Neuropathol. (Berl.) 40:111-116.
83. Singh, S.C. (1978) Redirected perforant and commissural connections of eutopic and ectopic neurons in the hippocampus of methylazoxymethanol-acetate treated rats. Acta Neuropathol. (Berl.) 44:197-202.
84. Singh, S.C. (1980) Deformed dendrites and reduced spine numbers on ectopic neurones in the hippocampus of rats exposed to methylazoxymethanol-acetate. Acta Neuropathol. (Berl.) 49:193-198.
85. Smeyne, R.J., K. Schilling, L. Robertson, D. Luk, J. Oberdick, T. Curran, and J. Morgan (1992) Fos-lacZ transgenic mice: Mapping sites of gene induction in the central nervous system. Neuron 8:13-23.
86. Soriano, E., J.A. DelRio, I. Ferrer, C. Auladell, L. De Lecea, and S. Alcantara (1992) Late appearance of parvalbumin-immunoreactive neurons in the rodent cerebral cortex does not follow an inside-out sequence. Neurosci. Lett. 142:147-150.
87. Sotelo, C. and J.P. Rio (1980) Cerebellar malformation obtained in rats by early postnatal treatment with 6-aminonicotinamide: Role of neuron glia interaction in cerebellum development. Neuroscience 5:1737-1759.
88. Stoughton, R.L., M. DelCerro, J.R. Walker, and J.R. Swarz (1978) Presence of displaced neuronal elements within rat cerebellar fissures. Brain Res. 148:15-29.
89. Sun, X.-Z., M. Inouye, Y. Takagishi, S. Hayasaka, and T. Yamamura (1995) Follow-up study on histogenesis of microcephaly associated with ectopic gray matter induced by prenatal γ-irradiation in the mouse. J. Neuropathol. Exp. Neurol. 55:357-365.
90. Terashima, T., K. Inoue, Y. Inoue, and K. Mikoshiba (1987) Thalamic connectivity of the primary motor cortex of normal and reeler mutant mice. J. Comp. Neurol. 257:405-421.
91. Vicario-Abejon, C., M.G. Cunningham, and R.D.G. McKay (1995) Cerebellar precursors transplanted to the neonatal dentate gyrus express features characteristic of hippocampal neurons. J. Neurosci. 15:6351-6363.
92. Weiss, S., O. Cataltepe, and A.J. Cole (1996) Anatomical studies of DNA fragmentation in rat brain after systemic kainate administration. Neuroscience 74:541-551.
93. 14C-2-deoxyglucose uptake and Fos immunocytochemistry. J. Neurosci. 13:4787-4809.
94. Yurkewicz, L., K.L. Valentino, M.K. Floeter, J.W. Fleshman, and E.G. Jones (1984) Effects of cytotoxic deletions of somatic sensory cortex in fetal rats. Somatosen. Res. 1:303-327.
95. Zhang, L.L., P.A. Collier, and K.W.S. Ashwell (1995) Mechanisms in the induction of neuronal heterotopias following prenatal cytotoxic brain damage. Neurotoxicol. Teratol. 17:297-311.