Summary
Using techniques for enhanced microtubular preservation (albumin pretreatment of Gray) occipital and pyriform cortices of rats were studied by electron microscopy at various stages of development. A close structural relationship was seen between microtubules (mts), focal membrane densities, synaptic vesicles, and presynaptic dense projections (pre-dps) during maturation. Mts were seen in the neonates to be focused onto the inner surface of immature axonic profiles merging or sometimes fragmenting there. Focal densities occur at these attachment sites and thereafter synaptic vesicles clothe the mts and abut onto these presumed primordial pre-dps. Thus, mts may contribute to the initial formation of pre-dps as well as their maintenance in the adult and may act to channel the first synaptic vesicles to the site of eventual synaptic contact and transmitter release.
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References
Akert K, Pfenninger K, Sandri C, Moor H (1972) Freeze etching and cytochemistry of vesicles and membrane complexes in synapses of the central nervous system. In: Pappas GD, Purpura DP (eds) Structure and function of synapses. Raven Press, New York, pp 67–86
Binder L, Dentler W, Rosenbaum JL (1975) Assembly of chicken brain tubulin onto flagellar microtubules from Chlamydomonas and sea urchin sperm. Proc Natl Acad Sci USA 72:1122–1126
Bird MM (1976) Microtubule-synaptic vesicle associations in cultured rat spinal cord neurons. Cell Tissue Res 168:101–115
Bloom FE (1972) The formation of synaptic junctions in developing rat brain. In: Pappas GD, Purpura DP (eds) Structure and function of synapses. Raven Press, New York, pp 101–120
Burgoyne RD, Gray EG, Sullivan K, Barron J (1982) Depolymerization of dendritic microtubules following incubation of cortical slices. Neurosci Lett 31:81–85
Dustin P (1978) Microtubules. Springer, Berlin
Gray EG (1963) Electron microscopy of presynaptic organelles of the spinal cord. J Anat Lond 97:101–106
Gray EG (1975a) Presynaptic microtubules and their association with synaptic vesicles. Proc Roy Soc B 190:369–372
Gray EG (1975b) Synaptic fine structure and nuclear, cytoplasmic, and extracellular networks. J Neurocytol 4:315–339
Gray EG (1976) Problems of understanding the substructure of synapses. Prog Brain Res 45:207–234
Gray EG (1978) Synaptic vesicles and microtubules in frog motor end-plate. Proc Roy Soc B 203:219–227
Gray EG, Willis RA (1970) On synaptic vesicles, complex vesicles and dense projections. Brain Res 24:149–168
Gray EG, Westrum LE (1979) Marginal bundles of axoplasmic microtubules at nodes of Ranvier within muscle. Cell Tissue Res 199:281–288
Gray EG, Jones DH, Barron J (1979) Aggregation of synaptic vesicles on the exposed inner membrane of presynaptic mitochondria in brain. J Neurocytol 8:675–685
Gray EG, Westrum LE, Burgoyne RD, Barron J (1982a) Synaptic organization and neuronal microtubule distribution. Cell Tissue Res 226:579–588
Gray EG, Burgoyne RD, Westrum LE, Cumming R, Barron J (1982b) The enigma of microtubule coils in brain synaptosomes. Proc Roy Soc B, 216:385–396
Jones DG, Cullen AM (1979) A quantitative investigation of some presynaptic terminal parameters during synaptogenesis. Exp Neurol 64:245–258
Jones DG, Dittmer MM, Reading LC (1974) Synaptogenesis in guinea-pig cerebral cortex: a glutaraldehyde-PTA study. Brain Res 70:245–263
Kanaseki T, Kadota K (1969) The vesicle in a basket. J Cell Biol 42:202–220
Margolis RL, Wilson L (1981) Microtubule treadmills-possible molecular machinery. Nature Lond 293:705–711
Matus A, Bernhardt R, Hugh-Jones T (1981) High molecular weight microtubule-associated proteins are preferentially associated with dendritic microtubules in brain. Proc Natl Acad Sci USA 78:3010–3014
Peters A, Palay SL, Webster H deF (1976) The fine structure of the nervous system: The neurons and supporting cells. Saunders, Philadelphia, pp 132–135
Rees RP (1978) The morphology of interneuronal synaptogenesis — a review. Fed Proc 37:2000–2009
Westrum LE (1975) Electron microscopy of synaptic structures in olfactory cortex of early postnatal rats. J Neurocytol 4:713–732
Westrum LE, Gray EG (1977) Microtubules associated with postsynaptic “thickening.” J Neurocytol 6:505–518
Westrum LE, Jones DH, Gray EG, Barron J (1980) Microtubules, dendritic spines and spine apparatuses. Cell Tissue Res 208:171–181
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Dr. Westrum is an Affiliate of the CDMRC at the University of Washington and a recipient of a Wellcome Research Travel Grant from the Burroughs-Wellcome Fund. The research was also supported in part by NIH Grants NS09678, NS17111 (NINCDS) and DEO4942 (NIDR), DHHS
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Westrum, L.E., Gray, E.G., Burgoyne, R.D. et al. Synaptic development and microtubule organization. Cell Tissue Res. 231, 93–102 (1983). https://doi.org/10.1007/BF00215777
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DOI: https://doi.org/10.1007/BF00215777