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PMID: 11756501 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains.

Bushong EA, Martone ME, Jones YZ, Ellisman MH

Abstract

Protoplasmic astrocytes are increasingly thought to interact extensively with neuronal elements in the brain and to influence their activity. Recent reports have also begun to suggest that physiologically, and perhaps functionally, diverse forms of these cells may be present in the CNS. Our current understanding of astrocyte form and distribution is based predominantly on studies that used the astrocytic marker glial fibrillary acidic protein (GFAP) and on studies using metal-impregnation techniques. The prevalent opinion, based on studies using these methods, is that astrocytic processes overlap extensively and primarily share the underlying neuropil. However, both of these techniques have serious shortcomings for visualizing the interactions among these structurally complex cells. In the present study, intracellular injection combined with immunohistochemistry for GFAP show that GFAP delineates only approximately 15% of the total volume of the astrocyte. As a result, GFAP-based images have led to incorrect conclusions regarding the interaction of processes of neighboring astrocytes. To investigate these interactions in detail, groups of adjacent protoplasmic astrocytes in the CA1 stratum radiatum were injected with fluorescent intracellular tracers of distinctive emissive wavelengths and analyzed using three-dimensional (3D) confocal analysis and electron microscopy. Our findings show that protoplasmic astrocytes establish primarily exclusive territories. The knowledge of how the complex morphology of protoplasmic astrocytes affects their 3D relationships with other astrocytes, oligodendroglia, neurons, and vasculature of the brain should have important implications for our understanding of nervous system function.

MeSH Terms
Animals Astrocytes/cytology,metabolism,ultrastructure Cell Size Cytoplasm/ultrastructure Fluorescent Dyes Glial Fibrillary Acidic Protein/analysis,metabolism Hippocampus/anatomy & histology,metabolism,ultrastructure Immunohistochemistry Iontophoresis Isoquinolines Male Microscopy, Confocal Microscopy, Electron Oxidation-Reduction Photochemistry Rats Rats, Sprague-Dawley
Chemicals
Fluorescent Dyes Glial Fibrillary Acidic Protein Isoquinolines lucifer yellow
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Bushong Eric A
National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, California 92093-0608, USA.
Martone Maryann E
Jones Ying Z
Ellisman Mark H
References (35)
35 references, click to expand
  1. Functional specialization and topographic segregation of hippocampal astrocytes.
    J Neurosci. 1998 Jun 15;18(12):4425-38 PMID: 9614220
  2. Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells.
    Nat Neurosci. 1999 Feb;2(2):139-43 PMID: 10195197
  3. Astrocytic gap junctions remain open during ischemic conditions.
    J Neurosci. 1998 Apr 1;18(7):2520-37 PMID: 9502812
  4. Immunocytochemical evidence for a distinct GFAP-negative subpopulation of astrocytes in the adult rat hippocampus.
    Neurosci Lett. 1998 Dec 4;257(3):127-30 PMID: 9870336
  5. THE FINE STRUCTURE OF ASTROCYTES IN THE CEREBRAL CORTEX AND THEIR RESPONSE TO FOCAL INJURY PRODUCED BY HEAVY IONIZING PARTICLES.
    J Cell Biol. 1965 May 1;25(2):141-57 PMID: 19866658
  6. Factors determining the migration of astrocytes into the developing retina: migration does not depend on intact axons or patent vessels.
    J Comp Neurol. 1991 Jan 15;303(3):375-86 PMID: 2007655
  7. Seasonal changes in astrocytes parallel neuronal plasticity in the song control area HVc of the canary.
    Glia. 1999 Jul;27(1):88-100 PMID: 10401635
  8. Electron tomography of large, multicomponent biological structures.
    J Struct Biol. 1997 Dec;120(3):219-27 PMID: 9441927
  9. Glia-neuron intercommunications and synaptic plasticity.
    Prog Neurobiol. 1996 Jun;49(3):185-214 PMID: 8878303
  10. Studies on the 3-dimensional architecture of dendritic spines and varicosities in human cortex by confocal laser scanning microscopy and Lucifer yellow microinjections.
    J Neurosci Methods. 1995 Mar;57(1):55-61 PMID: 7791365
  11. Mechanisms of glial-guided neuronal migration in vitro and in vivo.
    Experientia. 1990 Sep 15;46(9):907-16 PMID: 2209800
  12. Control of synapse number by glia.
    Science. 2001 Jan 26;291(5504):657-61 PMID: 11158678
  13. Role of glial cells in the regulation of the brain ion microenvironment.
    Prog Neurobiol. 1989;33(4):309-33 PMID: 2479051
  14. Synaptic transmission in the hippocampus: critical role for glial cells.
    Glia. 1994 Apr;10(4):237-43 PMID: 7914511
  15. Fluorescence photooxidation with eosin: a method for high resolution immunolocalization and in situ hybridization detection for light and electron microscopy.
    J Cell Biol. 1994 Aug;126(4):901-10 PMID: 7519623
  16. Directed spatial potassium redistribution in rat neocortex.
    Glia. 2000 Feb 1;29(3):288-92 PMID: 10642755
  17. A demonstration of glial filament distribution in astrocytes isolated from rat cerebral cortex.
    Neuroscience. 1985 Sep;16(1):33-44 PMID: 2423916
  18. Contact spacing among astrocytes in the central nervous system: an hypothesis of their structural role.
    Glia. 1991;4(5):484-94 PMID: 1834565
  19. Interactions of living astrocytes in vitro: evidence of the development of contact spacing.
    Glia. 1994 May;11(1):57-63 PMID: 8070895
  20. Contact-spacing among astrocytes is independent of neighbouring structures: in vivo and in vitro evidence.
    J Comp Neurol. 1993 Jun 22;332(4):433-43 PMID: 8349842
  21. Intracellular injection in fixed slices in combination with neuroanatomical tracing techniques and electron microscopy to determine multisynaptic pathways in the brain.
    Microsc Res Tech. 1993 Jan 1;24(1):15-30 PMID: 8435499
  22. Distribution of glial fibrillary acidic protein and vimentin immunoreactivity during rat visual cortex development.
    J Neurocytol. 1991 Feb;20(2):97-108 PMID: 2027041
  23. Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter.
    Glia. 2000 Aug;31(2):95-103 PMID: 10878596
  24. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence.
    Brain Res. 1972 Aug 25;43(2):429-35 PMID: 4559710
  25. The oligodendrocyte precursor cell in health and disease.
    Trends Neurosci. 2001 Jan;24(1):39-47 PMID: 11163886
  26. Qualitative analysis of membrane currents in glial cells from normal and gliotic tissue in situ: down-regulation of Na+ current and lack of P2 purinergic responses.
    Neuroscience. 1997 Dec;81(3):847-60 PMID: 9316033
  27. Passive glial cells, fact or artifact?
    J Membr Biol. 1998 Dec 1;166(3):213-22 PMID: 9843595
  28. An acidic protein isolated from fibrous astrocytes.
    Brain Res. 1971 May 7;28(2):351-4 PMID: 5113526
  29. Immunohistochemistry of glial fibrillary acidic protein, vimentin and S-100 protein for study of astrocytes in hippocampus of rat.
    J Chem Neuroanat. 1990 May-Jun;3(3):179-92 PMID: 2363851
  30. Four-hour processing of clinical/diagnostic specimens for electron microscopy using microwave technique.
    J Vet Diagn Invest. 1997 Jan;9(1):61-7 PMID: 9087927
  31. Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats.
    J Neurosci. 1999 Apr 15;19(8):2876-86 PMID: 10191305
  32. Three-dimensional structure of astrocytes in the rat dentate gyrus.
    J Comp Neurol. 1986 Jul 8;249(2):242-60 PMID: 3525618
  33. Independent mechanisms of potassium clearance by astrocytes in gliotic tissue.
    J Neurosci Res. 1999 Jun 15;56(6):595-603 PMID: 10374814
  34. Tripartite synapses: glia, the unacknowledged partner.
    Trends Neurosci. 1999 May;22(5):208-15 PMID: 10322493
  35. Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus.
    Glia. 1994 Nov;12(3):180-95 PMID: 7851987
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-01-01
Pages
183-92
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6757596
Subset
IM
Grants
NCRR NIH HHS · P41 RR004050 · United States
NCRR NIH HHS · RR04050 · United States
NIDCD NIH HHS · DC03192 · United States
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