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Aberrant Synaptic Development: A Review

Aberrant Synaptic Development: A Review Abstract Recently, the use of the electron microscope has begun to reveal pathologic alterations of synapses accompanying certain neurologic disorders. For a thorough understanding of the significance of these alterations, synaptic morphology and development must be clarified. One useful tool in the armamentarium of synaptic morphologists is the ability to induce aberrant synaptic development, either through the use of various toxins, infectious agents, or, even more importantly, through the use of a large number of murine mutants such as "weaver." One of the more common forms of synaptic aberrations in these experimental models is the development and retention of dendritic spines of Purkinje cells unattached to their normal presynaptic mates. A review of the morphologic details of this phenomenon, as well as some theoretical considerations regarding their implications, forms the body of the present article. References 1. Gonatas NK, Goldensohn ES: Unusual neocortical presynaptic terminals in a patient with convulsions, mental retardation and cortical blindness: An electron microscopic study . J Neuropathol Exp Neurol 24:539-562, 1965.Crossref 2. Gonatas NK, Evangelista I, Walsh GO: Axonic and synaptic changes in a case of psychomotor retardation: An electron microscopic study . J Neuropathol Exp Neurol 26:179-199, 1967.Crossref 3. Hedley-Whyte ET, et al: Infantile neuroaxonal dystrophy: A disease characterized by altered terminal axons and synaptic endings . Neurology 18:891-906, 1968.Crossref 4. Herman MM, Huttenlocher PR, Bensch KG: Electron microscopic observations in infantile neuroaxonal dystrophy . Arch Neurol 20:19-34, 1969.Crossref 5. Sandbank U, Lerman P, Geifman M: Infantile neuroaxonal dystrophy: Cortical axonic and presynaptic changes . Acta Neuropathol 16:342-352, 1970.Crossref 6. Seitelberger F: Eine unbekannute Form von infantiler lipoidspeicher Krankheit des Gehirns, in Proceedings of the First International Congress of Neuropathology, Turin, Rosenberg & Sellier, 1952, vol 3, pp 323-333. 7. Seitelberger F: Eine eigenartige Stoffwech-selerkrankung der Ganglionzellen im Zentralnervensystem, in Proceedings of the Fifth International Neurological Congress, Lisbon, Comptes-Rendus, 1954, vol 3, pp 484-491. 8. Cowen D, Olmstead EV: Infantile neuroaxonal dystrophy . J Neuropathol Exp Neurol 22:175-236, 1963.Crossref 9. Crome L, Weller SDV: Infantile neuroaxonal dystrophy . Arch Dis Child 40:502-507, 1965.Crossref 10. Lyon G, See G: La dégénérescence neuroaxonale infantile (maladie de Seitelberger): Etude anatomique d'une observation . Rev Neurol 109:133-155, 1963. 11. Sandbank U: Infantile neuroaxonal dystrophy . Arch Neurol 12:155-159, 1965.Crossref 12. Takei Y: Infantile neuroaxonal dystrophy (Seitelberger's disease) . Acta Neuropathol 5:1-15, 1965.Crossref 13. Kamoshita S, Neustein HB, Landing BH: Infantile neuroaxonal dystrophy with neonatal onset: Neuropathologic and electron microscopic observation . J Neuropathol Exp Neurol 27:300-323, 1968.Crossref 14. Jellinger K, Seitelberger F: Infantile neuroaxonale Dystrophie: Frühform mit bevorzugtem Kleinhirnbefall . Acta Neuropathol 10:123-131, 1968.Crossref 15. Toga M, Berard-Badier M, Gambarelli-Dubois D: La dystrophie neuroaxonale infantile on maladie de Seitelberger . Acta Neuropathol 15:327-350, 1970.Crossref 16. Gonatas NK, Baird HW, Evangelista I: The fine structure of neocortical synapses in infantile amaurotic idiocy . J Neuropathol Exp Neurol 27:39-49, 1968.Crossref 17. Gonatas NK, Terry RD, Weiss M: Electron microscopy study in two cases of Jakob-Creutzfeldt disease . J Neuropathol Exp Neurol 24:575-598, 1965.Crossref 18. Bignami A, Forno LS: Status spongiosus in Jakob-Creutzfeldt disease: Electron microscopic study of a cortical biopsy . Brain 93:89-94, 1970.Crossref 19. Hirano A, et al: Argentophilic plaques in Creutzfeldt-Jakob disease . Arch Neurol 26:530-542, 1972.Crossref 20. Gonatas NK, Anderson W, Evangelista I: The contribution of altered synapses in the senile plaque: An electron microscopic study in Alzheimer's dementia . J Neuropathol Exp Neurol 26:25-39, 1967.Crossref 21. Gonatas NK, Gambetti P: The pathology of the synapse in Alzheimer's disease, in Wolstenholme GEW, O'Connor M (eds): Ciba Foundation Symposium on Alzheimer's Disease and Related Conditions, London, J & A Churchill Ltd, 1970, pp 169-183. 22. Wiśniewski H, Terry RD: An experimental approach to the morphogenesis of neurofibrillary degeneration and the argyrophilic plaque, in Wolstenholme GEW, O'Connor M (eds): Ciba Foundation Symposium on Alzheimer's Disease and Related Conditions, London, J & A Churchill Ltd, 1970, pp 223-248. 23. Wiśniewski HM, Terry RD: Reexamination of the pathogenesis of the senile plaques , in Zimmerman HM (ed): Progress in Neuropathology , vol 2, New York, Grune & Stratton, Inc, to be published. 24. Robertson JD: The ultrastructure of synapses , in Schmitt FD (ed): The Neurosciences: Second Study Program , New York, Rockefeller University Press, 1970, pp 715-728. 25. Bloom FE: Correlating structure and function of synaptic ultrastructure , in Schmitt (ed): The Neurosciences: Second Study Program , New York, Rockefeller University Press, 1970, pp 729-746. 26. Peters A, Palay SL, Webster H deF: The Fine Structure of the Nervous System: The Cells and Their Processes . New York, Harper & Row, 1970. 27. McLennan H: Synaptic Transmission , ed 2. Philadelphia, WB Saunders Co, 1970. 28. Pappas GD, Purpura OP (eds): Structure and Function of Synapses . New York, Raven Press, 1972. 29. Gray EG: Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study . J Anat 93:420-432, 1959. 30. Gray EG: Electron microscopy of presynaptic organelles of the spinal cord . J Anat 97:101-106, 1963. 31. Gray EG: Tissue of the central nervous system , in Kurtz SM (ed): Electron Microscopic Anatomy , New York, Academic Press, 1964, pp 369-417. 32. Gray EG, Guillery RW: A note on the dendritic spine apparatus . J Anat 97:389-392, 1963. 33. Lampert P, Pentschew A: An electron microscopic study of spheroid and convoluted bodies in dystrophic terminal axons . Acta Neuropathol 4:158-168, 1964.Crossref 34. Lampert P, Blumberg JM, Pentschew A: An electron microscopic study of dystrophic axons in the Gracile and Cuneate nuclei of vitamin E-deficient rats . J Neuropathol Exp Neurol 23:60-77, 1964.Crossref 35. Fujisawa K: An unique type of axonal alteration (so-called axonal dystrophy) as seen in Goll s nucleus of 277 cases of controls: A contribution to the pathology of aging process . Acta Neuropathol 8:255-275, 1967.Crossref 36. Fujisawa K, Shiraki H, Katsui G: Early phase of axonal dystrophy in vitamin E-deficient rats, in Fourth International Congress of Neuropathology, Paris, Masson et Cie Editeurs, 1970, pp 99-100. 37. Prineas J: The pathogenesis of dying-back polyneurophathies: I. An ultrastructural study of experimental tri-ortho-cresyl phosphate intoxication in the cat . J Neuropathol Exp Neurol 28:571-597, 1969.Crossref 38. Gray EG: Electron microscopy of experimental degeneration in the brain, in Caveness WF, Walker AE (eds): Head Injury Conference Proceedings, Chicago, JB Lippincott Co, 1966, pp 455-462. 39. Barron KD, Doolin PF: Ultrastructural observations on retrograde atrophy of lateral geniculate body: II. The environs of the neuronal soma . J Neuropathol Exp Neurol 27:401-420, 1968.Crossref 40. Herndon RM: The interaction of axonal and dendritic elements in the developing and the mature synapse , in Pease DC (ed): Cellular Aspects of Normal Growth and Differentiation , Berkeley, Calif, University of Calif Press, 1971, pp 167-175. 41. Prineas J: The pathogenesis of dying-back polyneuropathies: II. An ultrastructural study of experimental acrylamide intoxication in the cat . J Neuropathol Exp Neurol 28:598-621, 1969.Crossref 42. Barron KD, et al: Subcellular accompaniments of axon reaction in cervical motoneurons of the cat , in Zimmerman HM (ed): Progress in Neuropathology , New York, Grune & Stratton, 1971, vol 1, pp 255-280. 43. Cornog JL Jr, Gonatas NK, Feierman BS: Effects of intracerebral injection of ouabain on the fine structure of rat cerebral cortex . Am J Pathol 51:573-590, 1967. 44. Okada K, Ayala GF, Sung JH: Ultrastructure of penicillin-induced epileptogenic lesion of the cerebral cortex in cats . J Neuropathol Exp Neurol 30:337-353, 1971.Crossref 45. 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Bloom FE: The formation of synaptic junctions in developing rat brain , in Pappas GD, Purpura OP (eds): Structure and Function of Synapses , New York, Raven Press, 1972, pp 101-120. 52. Eccles JC, Ito M, Szentagothai J: The Cerebellum as a Neuronal Machine . New York, Springer-Verlag, 1967. 53. Fox CA, Hillman DE, Siegesmund KA: The primate cerebellar cortex: A Golgi and electron microscopic study , in Fox CA, Snider RS (eds): The Cerebellum: Progress in Brain Research , Amsterdam, Elsevier Publishing Co, 1967, vol 25, pp 174-225. 54. Gobel S: Electron microscopical studies of the cerebellar molecular layer . J Ultrastruct Res 21:430-458, 1968.Crossref 55. Larramendi LMH: Morphological characteristics of extrinsic and intrinsic nerve terminals and their synapses in the cerebellar cortex of the mouse , in Fields WS, Willis WD Jr (eds): The Cerebellum in Health and Disease , St. Louis, Warren H Green Inc, 1969, pp 63-110. 56. Llinás R (ed): Neurobiology of Cerebellar Evolution and Development: Proceedings of the First International Symposium of the Institute for Biomedical Research. Chicago, American Medical Association & Research Foundation, 1969. 57. Larramendi LMH: Analysis of synaptogenesis in cerebellum of the mouse , in Llinás RR (ed): Neurobiology of Cerebellar Evolution and Development , Chicago, American Medical Association Education & Research Foundation, 1969, pp 803-843. 58. Meller K, Glees P: The development of the mouse cerebellum: A Golgi and electron microscopical study , in Llinás RR (ed): Neurobiology of Cerebellar Evolution and Development , Chicago, American Medical Association Education & Research Foundation, 1969, pp 783-801. 59. Mugnaini E: Developmental aspects of synaptology with special emphasis upon the cerebellar cortex , in Pease DC (ed): Cellular Aspects of Neural Growth and Differentiation , Los Angeles, University of California Press, 1971, pp 141-165. 60. Woodward DJ, et al: The ontogenetic development of synaptic junctions, synaptic activation and responsiveness to neurotransmitter substances in rat cerebellar Purkinje cells . Brain Res 34:73-97, 1971.Crossref 61. Bloom FE: The formation of synaptic junctions in developing rat brain , in Pappas GD, Purpura OP (eds): Structure and Function of Synapses , New York, Raven Press, 1972, pp 101-120. 62. Margolis G, Kilham L: Rat virus, an agent with an affinity for the dividing cell , in Gajdusek DC, Gibbs CJ Jr, Alpers M (eds): National Institute of Neurological Diseases and Blindness Monograph No 2, Slow Latent and Temperate Virus Infections , Public Health Service publication 1378, 1965. 63. Margolis G, Kilham L: Virus-induced cerebellar hypoplasia , in Zimmerman HM (ed): Infections of the Nervous System: Proceedings, Association for Research in Nervous and Mental Diseases , Baltimore, Williams & Wilkins, 1968, vol 44, pp 113-146. 64. Margolis G, Kilham L: In pursuit of an ataxic hamster: Virus-induced cerebellar hypoplasia , in Bailey OT, Smith DE (eds): The Central Nervous System: Some Experimental Models of Neurological Diseases, International Academy of Pathology Monograph 9 , Baltimore, Williams & Wilkins, 1968, pp 157-183. 65. Margolis G, Kilham L, Johnson RH: The parvoviruses and replicating cells: Insights into the pathogenesis of cerebellar hypoplasia , in Zimmerman HM (ed): Progress in Neuropathology , New York, Grune & Stratton, 1971, vol 1, pp 168-201. 66. Herndon RM, Margolis G, Kilham L: The synaptic organization of the malformed cerebellum induced by perinatal infection with the feline panleukopenia virus (PLV): I. Elements forming the cerebellar glomeruli . J Neuropathol Exp Neurol 30:196-205, 1971.Crossref 67. Herndon RM, Margolis G, Kilham L: The synaptic organization of the malformed cerebellum induced by perinatal infection with the feline panleukopenia virus (PLV): II. The Purkinje cell and its afferents . J Neuropathol Exp Neurol 30:557-580, 1971.Crossref 68. Fischer DS, Jones AM: Cerebellar hypoplasia resulting from cytosine arabinoside treatment in the neonatal hamster . Clin Res 13:540, 1965. 69. Hirono I, Shibuya C: Induction of a neurological disorder by cycasin in mice . Nature 216:1311-1312, 1967.Crossref 70. Hirono I, Shibuya C, Hayashi K: Induction of a cerebellar disorder with cycasin in newborn mice and hamsters . Proc Soc Exp Biol Med 131:593-599, 1969.Crossref 71. Nonaka I: Electron microscopic study on granule cells of the cerebellum in experimental congenital Minamata disease . J Electron Microsc 17:87, 1968. 72. Altman J, Anderson WJ, Wright KA: Selective destruction of precursors of microneurons of the cerebellar cortex with fractionated low-dose x-rays . Exp Neurol 17:481-497, 1967.Crossref 73. Sidman RL, Green MC, Appel SH: Catalog of the Neurological Mutants of the Mouse . Cambridge, Mass, Harvard University Press, 1965. 74. Sidman RL: Development of interneuronal connection in brains of mutant mice , in Carlson FD (ed): Physiological and Biochemical Aspects of Nervous Integration , Englewood Cliffs, NJ, Prentice-Hall Inc, 1968, pp 164-193. 75. Whiting MG: Toxicity of cycads . Econ Bot 17:271-302, 1963.Crossref 76. Whiting MG: Food practices in ALS foci in Japan, the Marianas and New Guinea . Fed Proc 23:1343-1345, 1964. 77. Spatz M: Toxic and carcinogenic alkylating agents from cycads . Ann NY Acad Sci 163:848-859, 1969.Crossref 78. Kurland LT, Mulder DW: Epidemiologic investigations of amyotrophic lateral sclerosis: I. Preliminary report on geographic distribution, with special reference to the Mariana Islands, including clinical and pathologic observations . Neurology 4:355-438, 1954.Crossref 79. Hirano A, et al: Parkinsonism-dementia complex, an endemic disease on the island of Guam: I. Clinical features . Brain 84:642-661, 1961.Crossref 80. Hirano A, et al: A review of the pathologic findings in amyotrophic lateral sclerosis , in Norris FH Jr, Kurland LT (eds): Motor Neuron Diseases , New York, Grune & Stratton, 1969, pp 51-60. 81. Brody JA, Chen K: Changing epidemiologic patterns of amyotrophic lateral sclerosis and parkinsonism-dementia on Guam , in Norris FH, Kurland LT (eds): Motor Neuron Diseases , New York, Grune & Stratton, 1969, pp 61-79. 82. Hirano A: Progress in the pathology of motor neuron diseases , in Zimmerman HM (ed): Progress in Neuropathology , vol 2, New York, Grune & Stratton, to be published. 83. Hirano A, et al: Amyotrophic lateral sclerosis and parkinsonism-dementia complex on Guam: Further pathologic studies . Arch Neurol 15:35-51, 1966.Crossref 84. Jones M: Cycasin-induced cerebellar pathology in the postnatal Swiss albino mouse . Am J Pathol 63:6a, 1971. 85. Jones M, Yang M, Michelsen D: Effects of methylazoxymethanol glucoside and methylazoxymethanol acetate on the cerebellum of the postnatal Swiss albino mice . Fed Proc 31:1508-1511, 1972. 86. Jones M, Sweeley C, Yang M: Effects of methylazoxymethanol glucoside (cycasin) and methylazoxymethanol acetate on the postnatal mouse cerebellum and spinal cord . J Neuropathol Exp Neurol 31:191-192, 1972. 87. Sanger VL, Yang M, Mickelsen O: Cycasin induced central nervous system lesions in post-natal mice . Fed Proc 31:1524-1528, 1972. 88. Hirano A, Dembitzer HM, Jones M: An electron microscopic study of cycasin-induced cerebellar alterations . J Neuropathol Exp Neurol 31:113-125, 1972.Crossref 89. Hirano A, Jones M: The fine structure of cycasin-induced cerebellar alterations . Fed Proc 31:1517-1519, 1972. 90. Bloom FE, Aghajanian GK: Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid . J Ultrastruct Res 22:361-375, 1968.Crossref 91. 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Matsuyama H: Congenital anomalies in the central nervous system: Special reference to reaction to injury of human fetal tissues . Adv Neurol Sci 16:43-49, 1972. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Neurology American Medical Association

Aberrant Synaptic Development: A Review

Archives of Neurology , Volume 28 (6) – Jun 1, 1973

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American Medical Association
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Copyright © 1973 American Medical Association. All Rights Reserved.
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0003-9942
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1538-3687
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10.1001/archneur.1973.00490240019001
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Abstract

Abstract Recently, the use of the electron microscope has begun to reveal pathologic alterations of synapses accompanying certain neurologic disorders. For a thorough understanding of the significance of these alterations, synaptic morphology and development must be clarified. One useful tool in the armamentarium of synaptic morphologists is the ability to induce aberrant synaptic development, either through the use of various toxins, infectious agents, or, even more importantly, through the use of a large number of murine mutants such as "weaver." One of the more common forms of synaptic aberrations in these experimental models is the development and retention of dendritic spines of Purkinje cells unattached to their normal presynaptic mates. A review of the morphologic details of this phenomenon, as well as some theoretical considerations regarding their implications, forms the body of the present article. References 1. Gonatas NK, Goldensohn ES: Unusual neocortical presynaptic terminals in a patient with convulsions, mental retardation and cortical blindness: An electron microscopic study . J Neuropathol Exp Neurol 24:539-562, 1965.Crossref 2. Gonatas NK, Evangelista I, Walsh GO: Axonic and synaptic changes in a case of psychomotor retardation: An electron microscopic study . J Neuropathol Exp Neurol 26:179-199, 1967.Crossref 3. Hedley-Whyte ET, et al: Infantile neuroaxonal dystrophy: A disease characterized by altered terminal axons and synaptic endings . Neurology 18:891-906, 1968.Crossref 4. Herman MM, Huttenlocher PR, Bensch KG: Electron microscopic observations in infantile neuroaxonal dystrophy . Arch Neurol 20:19-34, 1969.Crossref 5. Sandbank U, Lerman P, Geifman M: Infantile neuroaxonal dystrophy: Cortical axonic and presynaptic changes . Acta Neuropathol 16:342-352, 1970.Crossref 6. Seitelberger F: Eine unbekannute Form von infantiler lipoidspeicher Krankheit des Gehirns, in Proceedings of the First International Congress of Neuropathology, Turin, Rosenberg & Sellier, 1952, vol 3, pp 323-333. 7. Seitelberger F: Eine eigenartige Stoffwech-selerkrankung der Ganglionzellen im Zentralnervensystem, in Proceedings of the Fifth International Neurological Congress, Lisbon, Comptes-Rendus, 1954, vol 3, pp 484-491. 8. Cowen D, Olmstead EV: Infantile neuroaxonal dystrophy . J Neuropathol Exp Neurol 22:175-236, 1963.Crossref 9. Crome L, Weller SDV: Infantile neuroaxonal dystrophy . Arch Dis Child 40:502-507, 1965.Crossref 10. Lyon G, See G: La dégénérescence neuroaxonale infantile (maladie de Seitelberger): Etude anatomique d'une observation . Rev Neurol 109:133-155, 1963. 11. Sandbank U: Infantile neuroaxonal dystrophy . Arch Neurol 12:155-159, 1965.Crossref 12. Takei Y: Infantile neuroaxonal dystrophy (Seitelberger's disease) . Acta Neuropathol 5:1-15, 1965.Crossref 13. Kamoshita S, Neustein HB, Landing BH: Infantile neuroaxonal dystrophy with neonatal onset: Neuropathologic and electron microscopic observation . J Neuropathol Exp Neurol 27:300-323, 1968.Crossref 14. Jellinger K, Seitelberger F: Infantile neuroaxonale Dystrophie: Frühform mit bevorzugtem Kleinhirnbefall . Acta Neuropathol 10:123-131, 1968.Crossref 15. Toga M, Berard-Badier M, Gambarelli-Dubois D: La dystrophie neuroaxonale infantile on maladie de Seitelberger . Acta Neuropathol 15:327-350, 1970.Crossref 16. Gonatas NK, Baird HW, Evangelista I: The fine structure of neocortical synapses in infantile amaurotic idiocy . J Neuropathol Exp Neurol 27:39-49, 1968.Crossref 17. Gonatas NK, Terry RD, Weiss M: Electron microscopy study in two cases of Jakob-Creutzfeldt disease . J Neuropathol Exp Neurol 24:575-598, 1965.Crossref 18. Bignami A, Forno LS: Status spongiosus in Jakob-Creutzfeldt disease: Electron microscopic study of a cortical biopsy . Brain 93:89-94, 1970.Crossref 19. Hirano A, et al: Argentophilic plaques in Creutzfeldt-Jakob disease . Arch Neurol 26:530-542, 1972.Crossref 20. Gonatas NK, Anderson W, Evangelista I: The contribution of altered synapses in the senile plaque: An electron microscopic study in Alzheimer's dementia . J Neuropathol Exp Neurol 26:25-39, 1967.Crossref 21. Gonatas NK, Gambetti P: The pathology of the synapse in Alzheimer's disease, in Wolstenholme GEW, O'Connor M (eds): Ciba Foundation Symposium on Alzheimer's Disease and Related Conditions, London, J & A Churchill Ltd, 1970, pp 169-183. 22. Wiśniewski H, Terry RD: An experimental approach to the morphogenesis of neurofibrillary degeneration and the argyrophilic plaque, in Wolstenholme GEW, O'Connor M (eds): Ciba Foundation Symposium on Alzheimer's Disease and Related Conditions, London, J & A Churchill Ltd, 1970, pp 223-248. 23. Wiśniewski HM, Terry RD: Reexamination of the pathogenesis of the senile plaques , in Zimmerman HM (ed): Progress in Neuropathology , vol 2, New York, Grune & Stratton, Inc, to be published. 24. Robertson JD: The ultrastructure of synapses , in Schmitt FD (ed): The Neurosciences: Second Study Program , New York, Rockefeller University Press, 1970, pp 715-728. 25. Bloom FE: Correlating structure and function of synaptic ultrastructure , in Schmitt (ed): The Neurosciences: Second Study Program , New York, Rockefeller University Press, 1970, pp 729-746. 26. Peters A, Palay SL, Webster H deF: The Fine Structure of the Nervous System: The Cells and Their Processes . New York, Harper & Row, 1970. 27. McLennan H: Synaptic Transmission , ed 2. Philadelphia, WB Saunders Co, 1970. 28. Pappas GD, Purpura OP (eds): Structure and Function of Synapses . New York, Raven Press, 1972. 29. Gray EG: Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study . J Anat 93:420-432, 1959. 30. Gray EG: Electron microscopy of presynaptic organelles of the spinal cord . J Anat 97:101-106, 1963. 31. Gray EG: Tissue of the central nervous system , in Kurtz SM (ed): Electron Microscopic Anatomy , New York, Academic Press, 1964, pp 369-417. 32. Gray EG, Guillery RW: A note on the dendritic spine apparatus . J Anat 97:389-392, 1963. 33. Lampert P, Pentschew A: An electron microscopic study of spheroid and convoluted bodies in dystrophic terminal axons . Acta Neuropathol 4:158-168, 1964.Crossref 34. Lampert P, Blumberg JM, Pentschew A: An electron microscopic study of dystrophic axons in the Gracile and Cuneate nuclei of vitamin E-deficient rats . J Neuropathol Exp Neurol 23:60-77, 1964.Crossref 35. Fujisawa K: An unique type of axonal alteration (so-called axonal dystrophy) as seen in Goll s nucleus of 277 cases of controls: A contribution to the pathology of aging process . Acta Neuropathol 8:255-275, 1967.Crossref 36. Fujisawa K, Shiraki H, Katsui G: Early phase of axonal dystrophy in vitamin E-deficient rats, in Fourth International Congress of Neuropathology, Paris, Masson et Cie Editeurs, 1970, pp 99-100. 37. Prineas J: The pathogenesis of dying-back polyneurophathies: I. An ultrastructural study of experimental tri-ortho-cresyl phosphate intoxication in the cat . J Neuropathol Exp Neurol 28:571-597, 1969.Crossref 38. Gray EG: Electron microscopy of experimental degeneration in the brain, in Caveness WF, Walker AE (eds): Head Injury Conference Proceedings, Chicago, JB Lippincott Co, 1966, pp 455-462. 39. Barron KD, Doolin PF: Ultrastructural observations on retrograde atrophy of lateral geniculate body: II. The environs of the neuronal soma . J Neuropathol Exp Neurol 27:401-420, 1968.Crossref 40. 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Journal

Archives of NeurologyAmerican Medical Association

Published: Jun 1, 1973

References