Summary
Patterns of myelination have been studied in the optic tract and the superior colliculus (SC), with special reference to the optic layer, in the opossum Didelphis marsupialis. Myelination in the optic tract starts far in precedence of eye opening and follows a rostrocaudal gradient. Myelination in the SC presents the following features: it proceeds according to a general inside-out pattern and follows both rostro-caudal and latero-medial gradients in the optic layer, and it accelerates in the SC optic layer soon after systematic exposure to visual input. The data presented here, together with other available information, suggest that myelination in the opossum optic tract starts in parallel with the stabilization in the number of optic fibers, and advances in the rostro-caudal mode common to most eutherian mammals, and also that myelogenesis in the SC neither correlates necessarily with, nor recapitulates, the sequence of acquisition of GFAP-positive astrocytes in a given set of layers. Changes in the rate of myelination in the optic layer after exposure to visual input are regionally-selective, and seem compatible with the recruitment of thin axons into the myelogenetic cycle rather than with the thickening of pre-existing myelin sheaths. It is concluded that the SC is a favorable structure for the study of the differentiation of glial cells, particularly in species with an extended time course of maturation such as the opossum.
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References
Allodi S, Reese BE, Cavalcante LA (1990) Observations on the arrangement of axons according to diameter in the optic tract of the opossum Didelphis marsupialis. Braz J Med Biol Res 23:439–442
Barradas PC, Cavalcante LA, Mendez-Otero R, Vieira AM (1989) Astroglial differentiation in the opossum superior colliculus. Glia 2:103–111
Bignami A, Dahl D (1973) Differentiation of astrocytes in the cerebellar cortex and pyramidal tracts of the newborn rat. An immunofluorescence study with antibodies to a protein specific to astrocytes. Brain Res 49:393–402
Bignami A, Dahl D (1975) Astroglial protein in the developing spinal cord of the chick embryo. Dev Biol 44:204–209
Blunt MJ, Baldwin F, Wendell-Smith CP (1972) Gliogenesis and myelination in kitten optic nerve. Z Zellforsch Mikrosk Anat 124:293–310
Bruckner G, Mares V, Biesold D (1976) Neurogenesis in the visual system of the rat. An autoradiographic investigation. J Comp Neurol 166:245–256
Cavalcante LA (1987) Postnatal neurogenesis and the formation of neural connections in the visual system of a marsupial. In: Chagas C, Linden R (eds) Developmental neurobiology of mammals. Pontifical Academy, Vatican, pp 1–29
Cavalcante LA, Rocha-Miranda CE (1978) Postnatal development of retinogeniculate, retinopretectal and retinotectal projections in the opossum. Brain Res 146:231–248
Cavalcante LA, Rocha-Miranda CE, Lent R (1975) Hypothalamic, tectal and accessory optic projections in the opossum. Brain Res 84:302–307
Cavalcante LA, Rocha-Miranda CE, Linden R (1984) Observations on neurogenesis of the superior colliculus and pretectum in the opossum. Dev Brain Res 13:241–249
Cooper ML, Rakic P (1981) Neurogenetic gradients in the superior and inferior colliculi of the rhesus monkey. J Comp Neurol 202:309–334
Dahl D (1981) The vimentin-GFA protein transition in rat neuroglia occurs at the time of myelination. J Neurosci Res 6:741–748
do Carmo MP (1976) Differential geometry of curves and surfaces. Prentice Hall, Englewood Cliffs, 503 pp
Friede RL, Hu KH (1967) Proximo-distal differences in myelin development in human optic fibers. Z Zellforsch Mikrosk Anat 79:259–264
Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209
Ghandour MS, Sko'ff RP (1988) Expression of galactocerebroside in developing normal and jimpy oligodendrocytes in situ. J Neurocytol 17:485–498
Hess DT, Merker BH (1983) Technical modifications of Gallyas silver stain for myelin. J Neurosci Methods 8:95–97
Hildebrand C, Waxman SG (1984) Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J Comp Neurol 224:25–37
Hirano M, Goldman JE (1988) Gliogenesis in rat spinal cord: evidence for origin of astrocytes and oligodendrocytes from radial precursors. J Neurosci Res 21:155–167
Hokoc JN, Oswaldo-Cruz E (1978) Quantitative analysis of the opossum's optic nerve: an electron microscopic study. J Comp Neurol 178:773–782
Huber GC, Crosby EC (1943) A comparison of the mammalian and reptilian tecta. J Comp Neurol 78:133–168
Kirby MA, Clift-Forsberg L, Wilson PD, Rapisardi SC (1982) Quantitative analysis of the optic nerve of the North American opossum (Didelphis virginiana): an electron microscopic study. J Comp Neurol 211:318–327
Kirby MA, Wilson PD, Fischer TM (1988) Development of optic nerve of the opossum (Didelphis virginiana). Dev Brain Res 44:37–48
Langworthy OR (1928) The behavior of pouch-young opossums correlated with the myelination of tracts in the nervous system. J Comp Neurol 46:201–240
Lent R, Cavalcante LA, Rocha-Miranda CE (1976) Retinofugal projections in the opossum. An anterograde degeneration and radioautographic study. Brain Res 107:9–26
Levine JM (1989) Neuronal influences on glial progenitor cell development. Neuron 3:103–113
Linden R, Rocha-Miranda CE (1978) Projections from the striate cortex to the superior colliculus in the opossum (Didelphis marsupialis aurita). In: Rocha-Miranda CE, Lent R (eds) Opossum neurobiology. Academia Brasileira de Ciencias, Rio de Janeiro, pp 137–150
Linden R, Rocha-Miranda CE (1983) Organization of the visual thalamus: corticothalamic projections from the primary visual area in the opossum. Braz J Med Biol Res 16:247–260
Linser PJ, Perkins M (1987) Gliogenesis in the embryonic avian optic tectum: neuronal-glial interactions influence astroglial phenotype maturation. Dev Brain Res 31:277–290
Looney GA, Elberger AJ (1986) Myelination of the corpus callosum in the cat: time course, topography, and functional implications. J Comp Neurol 248:336–347
Macri JJ, Perez M, Rama F, Rebollo MA (1966) Myelinization of the optic pathway in albino rats. An Fac Med Univ Repub (Montevideo) 51:45–59
Mc Crady E Jr (1938) The embryology of the opossum. Am Anat Memoirs 16, Wistar Institute, Philadelphia, 233 pp
Mendez-Otero R, Cavalcante LA, Rocha-Miranda CE, Bernardes RF, Barradas PCR (1985) Growth and restriction of the ipsilateral retinocollicular projection in the opossum. Dev Brain Res 18:199–210
Miller RH, David S, Patel R, Abney ER, Raff MC (1985) A quantitative immunohistochemical study of macroglial cell development in the rat optic nerve: in vivo evidence for two distinct astrocyte lineages. Dev Biol 111:35–41
Moore CL, Kalil R, Richards W (1976) Development of myelination in optic tract of the cat. J Comp Neurol 163:125–136
Mustari MJ, Lund RD, Graubard K (1979) Histogenesis of the superior colliculus of the albino rat. A tritiated thymidine study. Brain Res 164:39–52
Nakayama K (1967) Studies on myelination of human optic nerve. Jpn J Ophthalmol 11:18–26
Oblinger MM, Das GD (1981) Neurogenesis in the brain stem of the rabbit: an autoradiographic study. J Comp Neurol 197:45–62
Oswaldo-Cruz E, Rocha-Miranda CE (1968) The brain of the opossum (Didelphis marsupialis), Instituto de Biofisica da Universidade Federal do Rio de Janeiro, Rio de Janeiro, 99 pp
Raff MC (1989) Glial cell diversification in the rat optic nerve. Science 243:1450–1455
Raff MC, Mirsky R, Fields KL, Lisak RP, Dorfman SH, Silderberg DH, Gregson NA, Leibowitz S, Kennedy MC (1978) Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture. Nature 274:813–816
Ramon y Cajal S (1911) Histologie du système nerveux de l'homme et des vertébrés, vol II, Maloine, Paris
Ranscht B, Clapshaw PA, Price J, Noble M, Seifert W (1982) Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci USA 79:2709–2713
Rapaport DH, Wilson PD (1983) Retinal ganglion cell size groups projecting to the superior colliculus and the dorsal lateral geniculate nucleus in the North American opossum. J Comp Neurol 213:74–85
Rapaport DH, Wilson PD, Rowe MH (1981) The distribution of ganglion cells in the retina of the North American opossum (Didelphis virginiana). J Comp Neurol 199:465–480
Reynolds HC (1952) Studies of reproduction in the opossum. Univ Calif Publ Zool 52:233–294
Rocha-Miranda CE, Cavalcante LA, Gawryszewski LG, Linden R, Volchan E (1978) The vertical meridian representation and the pattern of retinotectal projections in the opossum. In: Rocha-Miranda CE, Lent R (eds) Opossum neurobiology. Academia Brasileira de Ciencias, Rio de Janeiro, pp 113–126
Skoff RP (1978) The pattern of myelination along the developing rat optic nerve. Neurosci Lett 7:191–196
Skoff RP, Toland D, Nast E (1980) Pattern of myelination and distribution of neuroglial cells along the developing optic system of the rat and rabbit. J Comp Neurol 191:237–253
Sterling P (1971) Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus. Vision Res [Suppl] 3:309–328
Volchan E, Gawryszewski LG, Rocha-Miranda CE (1982) Visuotopic organization of the superior colliculus of the opossum. Exp Brain Res 46:263–268
Yakovlev PI, Lecours A-R (1967) The myelogenetic cycles of regional maturation of the brain. In: Minkowski A (ed) Regional Development of the Brain in Early Life. William Clowes, London, pp 3–70
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Cavalcante, L.A., Barradas, P.C. & Martinez, A.M.B. Patterns of myelination in the opossum superior colliculus with additional reference to the optic tract. Anat Embryol 183, 273–285 (1991). https://doi.org/10.1007/BF00192215
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DOI: https://doi.org/10.1007/BF00192215