Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1983 Oct 1;97(4):1169–1178. doi: 10.1083/jcb.97.4.1169

Cytoplasmic organization in cerebellar dendritic spines

PMCID: PMC2112605  PMID: 6684661

Abstract

Three sets of filamentous structures were found to be associated with synaptic junctions in slices of cerebellar tissue prepared by rapid- freezing and freeze-etch techniques. The electron-dense fuzz subjacent to postsynaptic membranes corresponds to a web of 4-6-nm-diam filaments that were clearly visualized in rapid-frozen, freeze-etched preparations. Purkinje cell dendritic spines are filled with a meshwork of 5-7-nm filaments that were found to contact the spine membrane everywhere except at the synaptic junction, and extend through the neck of the spine into the parent dendrite. In addition, 8-10-nm microfilaments, possibly actin, were seen to be associated with the postsynaptic web and to extend into the body and neck of the spine. The arrangements and attachments of the filamentous elements in the Purkinje cell dendritic spine may account for its shape.

Full Text

The Full Text of this article is available as a PDF (5.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alger B. E., Teyler T. J. Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res. 1976 Jul 16;110(3):463–480. doi: 10.1016/0006-8993(76)90858-1. [DOI] [PubMed] [Google Scholar]
  2. Banker G., Churchill L., Cotman C. W. Proteins of the postsynaptic density. J Cell Biol. 1974 Nov;63(2 Pt 1):456–465. doi: 10.1083/jcb.63.2.456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blomberg F., Cohen R. S., Siekevitz P. The structure of postsynaptic densities isolated from dog cerebral cortex. II. Characterization and arrangement of some of the major proteins within the structure. J Cell Biol. 1977 Jul;74(1):204–225. doi: 10.1083/jcb.74.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Caceres A., Payne M. R., Binder L. I., Steward O. Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1738–1742. doi: 10.1073/pnas.80.6.1738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carlin R. K., Grab D. J., Cohen R. S., Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol. 1980 Sep;86(3):831–845. doi: 10.1083/jcb.86.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cohen R. S., Blomberg F., Berzins K., Siekevitz P. The structure of postsynaptic densities isolated from dog cerebral cortex. I. Overall morphology and protein composition. J Cell Biol. 1977 Jul;74(1):181–203. doi: 10.1083/jcb.74.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cotman C. W., Banker G., Churchill L., Taylor D. Isolation of postsynaptic densities from rat brain. J Cell Biol. 1974 Nov;63(2 Pt 1):441–455. doi: 10.1083/jcb.63.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DeRosier D. J., Tilney L. G., Egelman E. Actin in the inner ear: the remarkable structure of the stereocilium. Nature. 1980 Sep 25;287(5780):291–296. doi: 10.1038/287291a0. [DOI] [PubMed] [Google Scholar]
  9. Drenckhahn D., Kellner J., Mannherz H. G., Gröschel-Stewart U., Kendrick-Jones J., Scholey J. Absence of myosin-like immunoreactivity in stereocilia of cochlear hair cells. Nature. 1982 Dec 9;300(5892):531–532. doi: 10.1038/300531a0. [DOI] [PubMed] [Google Scholar]
  10. Fifková E., Delay R. J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol. 1982 Oct;95(1):345–350. doi: 10.1083/jcb.95.1.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Flock A., Cheung H. C. Actin filaments in sensory hairs of inner ear receptor cells. J Cell Biol. 1977 Nov;75(2 Pt 1):339–343. doi: 10.1083/jcb.75.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. GRAY E. G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat. 1959 Oct;93:420–433. [PMC free article] [PubMed] [Google Scholar]
  13. Grab D. J., Berzins K., Cohen R. S., Siekevitz P. Presence of calmodulin in postsynaptic densities isolated from canine cerebral cortex. J Biol Chem. 1979 Sep 10;254(17):8690–8696. [PubMed] [Google Scholar]
  14. Gray E. G., Guillery R. W. Synaptic morphology in the normal and degenerating nervous system. Int Rev Cytol. 1966;19:111–182. doi: 10.1016/s0074-7696(08)60566-5. [DOI] [PubMed] [Google Scholar]
  15. Gross H., Bas E., Moor H. Freeze-fracturing in ultrahigh vacuum at -196 degrees C. J Cell Biol. 1978 Mar;76(3):712–728. doi: 10.1083/jcb.76.3.712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gulley R. L., Landis D. M., Reese T. S. Internal organization of membranes at end bulbs of Held in the anteroventral cochlear nucleus. J Comp Neurol. 1978 Aug 15;180(4):707–741. doi: 10.1002/cne.901800405. [DOI] [PubMed] [Google Scholar]
  17. Gulley R. L., Reese T. S. Cytoskeletal organization at the postsynaptic complex. J Cell Biol. 1981 Oct;91(1):298–302. doi: 10.1083/jcb.91.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hall Z. W., Lubit B. W., Schwartz J. H. Cytoplasmic actin in postsynaptic structures at the neuromuscular junction. J Cell Biol. 1981 Sep;90(3):789–792. doi: 10.1083/jcb.90.3.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hanna R. B., Hirano A., Pappas G. D. Membrane specializations of dentritic spines and glia in the weaver mouse cerebellum: a freeze-fracture study. J Cell Biol. 1976 Mar;68(3):403–410. doi: 10.1083/jcb.68.3.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hasty D. L., Hay E. D. Freeze-fracture studies of the developing cell surface. II. Particle-free membrane blisters on glutaraldehyde-fixed corneal fibroblasts are artefacts. J Cell Biol. 1978 Sep;78(3):756–768. doi: 10.1083/jcb.78.3.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heuser J. E., Kirschner M. W. Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J Cell Biol. 1980 Jul;86(1):212–234. doi: 10.1083/jcb.86.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Heuser J. E., Reese T. S., Dennis M. J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol. 1979 May;81(2):275–300. doi: 10.1083/jcb.81.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Heuser J. E., Reese T. S., Landis D. M. Functional changes in frog neuromuscular junctions studied with freeze-fracture. J Neurocytol. 1974 Mar;3(1):109–131. doi: 10.1007/BF01111936. [DOI] [PubMed] [Google Scholar]
  24. Heuser J. E., Reese T. S., Landis D. M. Preservation of synaptic structure by rapid freezing. Cold Spring Harb Symp Quant Biol. 1976;40:17–24. doi: 10.1101/sqb.1976.040.01.004. [DOI] [PubMed] [Google Scholar]
  25. Heuser J. E., Reese T. S. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol. 1981 Mar;88(3):564–580. doi: 10.1083/jcb.88.3.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Heuser J. E., Salpeter S. R. Organization of acetylcholine receptors in quick-frozen, deep-etched, and rotary-replicated Torpedo postsynaptic membrane. J Cell Biol. 1979 Jul;82(1):150–173. doi: 10.1083/jcb.82.1.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Heuser J. Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol. 1980 Mar;84(3):560–583. doi: 10.1083/jcb.84.3.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hirokawa N., Heuser J. E. Internal and external differentiations of the postsynaptic membrane at the neuromuscular junction. J Neurocytol. 1982 Jun;11(3):487–510. doi: 10.1007/BF01257990. [DOI] [PubMed] [Google Scholar]
  29. Hirokawa N., Heuser J. E. Quick-freeze, deep-etch visualization of the cytoskeleton beneath surface differentiations of intestinal epithelial cells. J Cell Biol. 1981 Nov;91(2 Pt 1):399–409. doi: 10.1083/jcb.91.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kelly P. T., Cotman C. W. Synaptic proteins. Characterization of tubulin and actin and identification of a distinct postsynaptic density polypeptide. J Cell Biol. 1978 Oct;79(1):173–183. doi: 10.1083/jcb.79.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Landis D. M., Reese T. S. Differences in membrane structure between excitatory and inhibitory synapses in the cerebellar cortex. J Comp Neurol. 1974 May 1;155(1):93–125. doi: 10.1002/cne.901550107. [DOI] [PubMed] [Google Scholar]
  32. Landis D. M., Reese T. S. Structure of the Purkinje cell membrane in staggerer and weaver mutant mice. J Comp Neurol. 1977 Jan 15;171(2):247–260. doi: 10.1002/cne.901710208. [DOI] [PubMed] [Google Scholar]
  33. Lee K. S., Schottler F., Oliver M., Lynch G. Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J Neurophysiol. 1980 Aug;44(2):247–258. doi: 10.1152/jn.1980.44.2.247. [DOI] [PubMed] [Google Scholar]
  34. Moshkov D. A., Petrovskaia L. L., Bragin A. G. Posttetanicheskie izmeneniia v ul'trastrukture gigantskikh shipikovskikh sinapsov polia CA3 gippokampa. Dokl Akad Nauk SSSR. 1977;237(6):1525–1528. [PubMed] [Google Scholar]
  35. Moshkov D. A., Petrovskaia L. L., Bragin A. G. Ul'trastrukturnoe izuchenie osnov posttetanicheskoi potentsiatsii v srezakh gippokampa metodom zamorazhivaniia-zameshcheniia. Tsitologiia. 1980 Jan;22(1):20–26. [PubMed] [Google Scholar]
  36. PAPPAS G. D., PURPURA D. P. Fine structure of dendrites in the superficial neocortical neuropil. Exp Neurol. 1961 Dec;4:507–530. doi: 10.1016/0014-4886(61)90049-8. [DOI] [PubMed] [Google Scholar]
  37. Pumplin D. W., Reese T. S., Llinás R. Are the presynaptic membrane particles the calcium channels? Proc Natl Acad Sci U S A. 1981 Nov;78(11):7210–7213. doi: 10.1073/pnas.78.11.7210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rash J. E., Ellisman M. H. Studies of excitable membranes. I. Macromolecular specializations of the neuromuscular junction and the nonjunctional sarcolemma. J Cell Biol. 1974 Nov;63(2 Pt 1):567–586. doi: 10.1083/jcb.63.2.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sampedro M. N., Bussineau C. M., Cotman C. W. Postsynaptic density antigens: preparation and characterization of an antiserum against postsynaptic densities. J Cell Biol. 1981 Sep;90(3):675–686. doi: 10.1083/jcb.90.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Schnapp B. J., Reese T. S. Cytoplasmic structure in rapid-frozen axons. J Cell Biol. 1982 Sep;94(3):667–669. doi: 10.1083/jcb.94.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sleytr U. B., Robards A. W. Plastic deformation during freeze-cleavage: a review. J Microsc. 1977 May;110(1):1–25. doi: 10.1111/j.1365-2818.1977.tb00009.x. [DOI] [PubMed] [Google Scholar]
  42. Teyler T. J. Plasticity in the hippocamus: a model systems approach. Adv Psychobiol. 1976;3:301–326. [PubMed] [Google Scholar]
  43. Tilney L. G., Derosier D. J., Mulroy M. J. The organization of actin filaments in the stereocilia of cochlear hair cells. J Cell Biol. 1980 Jul;86(1):244–259. doi: 10.1083/jcb.86.1.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Ueda T., Greengard P., Berzins K., Cohen R. S., Blomberg F., Grab D. J., Siekevitz P. Subcellular distribution in cerebral cortex of two proteins phosphorylated by a cAMP-dependent protein kinase. J Cell Biol. 1979 Nov;83(2 Pt 1):308–319. doi: 10.1083/jcb.83.2.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. VANHARREVELD A., CROWELL J., MALHOTRA S. K. A STUDY OF EXTRACELLULAR SPACE IN CENTRAL NERVOUS TISSUE BY FREEZE-SUBSTITUTION. J Cell Biol. 1965 Apr;25:117–137. doi: 10.1083/jcb.25.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Van Harreveld A., Fifkova E. Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp Neurol. 1975 Dec;49(3):736–749. doi: 10.1016/0014-4886(75)90055-2. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES