Electron microscopic serial-sectioning/reconstruction study of parvalbumin-containing neurons in the external plexiform layer of the rat olfactory bulb

Neuroscience

Volumn 72, Issue 2, 1996, Pages 449-466

  Toida, K ^a   Kosaka, K ^a   Heizmann, C W ^b   Kosaka, T ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

electron microscopy; olfactory bulb; parvalbumin; reciprocal synapse; reconstruction; serial section

Indexed keywords

PARVALBUMIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXTERNAL PLEXIFORM LAYER; IMMUNOCYTOCHEMISTRY; MALE; MORPHOMETRICS; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RAT; SYNAPSE;

EID: 0029971433     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(95)00521-8     Document Type: Article

References (46)

1. Alonso J. R., Arévalo R., García-Ojeda E., Porteros A., Briñón J. G. and Ajión J. (1995) NADPH-diaphorase active and calbindin D-28k-immunoreactive neurons and fibers in the olfactory bulb of the hedgehog (Erinaceus europaeus). J. comp. Neurol. 351, 307-327.
2. Bogan N., Brecha N., Gall C. and Karten H. J. (1982) Distribution of enkephalin-like immunoreactivity in the rat main olfactory bulb. Neuroscience 7, 895-906.
3. Briñón J. G., Alonso J. R., Arévalo R., García-Ojeda E. and Ajión J. (1992) Calbindin D-28k-positive neurons in the rat olfactory bulb. An immunohistochemical study. Cell Tiss. Res. 269, 289-297.
4. Cameron H. A., Kaliszewski C. K. and Greer C. A. (1991) Organization of mitochondria in olfactory bulb granule cell dendritic spines. Synapse 8, 107-118.
5. Celio M. R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375-475.
6. Celio M. R. and Heizmann C. W. (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293, 300-302.
7. Gall C., Seroogy K. and Brecha N. (1986) Distribution of VIP-and NPY-like immunoreactives in rat main olfactory bulb. Brain Res. 374, 389-394.
8. Gulyas A. I., Miettinen R., Jacobowitz D. M. and Freund T. F. (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus - I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48, 1-27.
9. Halász N. and Shepherd G. M. (1983) Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10, 579-619.
10. Hirata Y. (1964) Some observations on the fine structure of the synapses in the olfactory bulb of the mouse, with particular reference to the atypical synaptic configurations. Arch. Histol. Jpn. 24, 293-302.
11. Hsu S.-M., Raine L. and Fanger H. (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. J. Histochem. Cytochem. 29, 577-580.
12. Jacobowitz D. M. and Winsky L. (1991) Immunocytochemical localization of calretinin in the forebrain of the rat. J. comp. Neurol. 304, 198-218.
13. 2+-binding parvalbumin in rat testis: characterization, localization, and expression during development. J. biol. Chem. 262, 7314-7320.
14. Kasa P., Hlavati I., Dobo E., Wolff A., Joo F. and Wolff J. R. (1995) Synaptic and non-synaptic cholinergic innervation of the various types of neurons in the main olfactory bulb of adult rat: immunocytochemistry of choline acetyltransferase. Neuroscience 67, 667-677.
15. Katsumaru H., Kosaka T., Heizmann C. W. and Hama K. (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Expl Brain Res. 72, 343-362.
16. Katsumaru H., Kosaka T., Heizmann C. W. and Hama K. (1988) Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Expl Brain Res. 72, 363-370.
17. Kawaguchi Y., Katsumaru H., Kosaka T., Heizmann C. W. and Hama, K. (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416, 369-374.
18. Kishi K., Mori K. and Ojima H. (1984) Distribution of local axon colaterals of mitral, displaced mitral, and tufted cells in the rabbit olfactory bulb. J. comp. Neurol. 225, 511-526.
19. Kita H., Kosaka T. and Heizmann C. W. (1990) Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res. 536, 1-15.
20. Kosaka K., Aika Y., Toida K., Heizmann C. W., Hunziker W., Jacobowitz D. M., Nagatsu I., Streit P., Visser T. J. and Kosaka T. (1995) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci. Res. 23, 73-88.
21. Kosaka, K., Hama K., Nagatsu I., Wu J.-L. and Kosaka T. (1988) Possible coexistence of amino acid (γ-aminobutyric acid), amine (dopamine) and peptide (substance P); neurons containing immunoreactivities for glutamic acid decarboxylase, tyrosine hydrolase and substance P in the hamster main olfactory bulb. Expl Brain Res. 71, 633-642.
22. Kosaka K., Heizmann C. W. and Kosaka T. (1994) Calcium-binding protein parvalbumin immunoreactive neurons in the rat olfactory bulb 1. Distribution and structural features in adult rat. Expl Brain Res. 99, 191-204.
23. Kosaka T., Hataguchi Y., Hama K., Nagatsu I. and Wu J.-Y. (1985) Coexistence of immunoreactivites in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine. Brain Res. 343, 166-171.
24. Kosaka T., Kosaka K., Heizmann C. W., Nagatsu I., Wu J.-Y., Yanaihara N. and Hama K. (1987) An aspect of the organization of the GABAergic system in the rat main olfactory bulb: laminar distribution of immunohistochemically defined subpopulations of GABAergic neurons. Brain Res. 411, 373-378.
25. Kosaka T., Nagatsu I., Wu J.-Y. and Hama K. (1986) Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18, 975-990.
26. Macrides F. and Schneider S. P. (1982) Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J. comp. Neurol. 208, 419-430.
27. Martínez-Guijarro F. J., Soriano E., Del Río J. A., Blasco-Ibáñez J. M. and López-García C. (1993) Parvalbumin-containing neurons in the cerebral cortex of the lizard Podarcis hispanica: morphology, ultrastructure, and coexistence with GABA, somatostatin, and neuropeptide Y. J. comp. Neurol. 336, 447-467.
28. Mori K., Kishi K. and Ojima H. (1983) Distribution of dendrite of mitral, displaced mitral, tufted and granule cells in the rabbit olfactory bulb. J. comp. Neurol. 219, 339-355.
29. Orona E., Rainer E. C. and Scott J. W. (1984) Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb. J. comp. Neurol. 226, 346-356.
30. Pinching A. J. and Powell T. P. S. (1971) The neuron types of the glomerular layer of the olfactory bulb. J. Cell Sci. 9, 305-345.
31. Price J. L. and Powell T. P. S. (1970) The morphology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 91-123.
32. Price J. L. and Powell T. P. S. (1970) The synaptology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 125-155.
33. Price J. L. and Powell T. P. S. (1970) An electron-microscopic study of the termination of the afferent fibers to the olfactory bulb from the cerebral hemisphere. J. Cell Sci. 7, 157-187.
34. Price J. L. and Powell T. P. S. (1970) The mitral and short axon cells of the olfactory bulb. J. Cell Sci. 7, 631-651.
35. Rall W., Shepherd G. M., Reese T. S. and Brightman M. W. (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Expl Neurol. 14, 44-56.
36. Ramon y Cajal S. (1911) In Histologie du Système Nerveux de l'Homme et des Vertebrates, II (trans. Azoulay, L.), pp. 647-674. Maloine, Paris.
37. Ribak C. E., Seress L. and Leranth C. (1993) Electron microscopic immunocytochemical study of the distribution of parvalbumin-containing neurons and axon terminals in the primate dentate gyrus and Ammon's horn. J. comp. Neurol. 327, 298-321.
38. Sanides-Kohlrausch C. and Wahle P. (1990) VIP-and PHI-immunoreactivity in olfactory centers of the adult cat. J. comp. Neurol. 294, 325-339.
39. Schneider S. P. and Macrides F. (1978) Laminar distributions of interneurons in the main olfactory bulb of the adult hamster. Brain Res. Bull. 3, 73-82.
40. Seroogy K. B., Brecha N. and Gall C. (1985) Distribution of cholecystokinin-like immunoreactivity in the rat main olfactory bulb. J. comp. Neurol. 239, 378-391.
41. Shepherd G. M. and Greer C. A. (1990) Olfactory bulb. In The Synaptic Organization of the Brain, 3rd edn (ed. Shepherd G. M.), pp. 133-169. Oxford University Press, Oxford.
42. Small, J. V. (1968) Measurement of section thickness. In Abstracts of the Fourth European Regional Conference on Electron Microscopy, Rome, vol. 1, pp. 609-610.
43. Toida K., Kosaka K., Heizmann C. W. and Kosaka T. (1994) Synaptic contacts between mitral/tufted cells and GABAergic neurons containing calcium binding protein parvalbumin in the rat olfactory bulb, with special reference to reciprocal synapses between them. Brain Res. 650, 347-352.
44. Tsuruo Y., Hökfelt T. and Visser T. J. (1988) Thyrotropin-releasing hormone (TRH)-immunoreactive neuron populations in the rat olfactory bulb. Brain Res. 447, 183-187.
45. Woolf T. B., Shepherd G. M. and Greer C. A. (1991) Serial reconstructions of granule cell spines in the mammalian olfactory bulb. Synapse 7, 181-192.
46. Wouterlood F. G., Härtig W., Brückner G. and Witter M. P. (1995) Parvalbumin-immunoreactive neurons in the entorhinal cortex of the rat: localization, morphology, connectivity and ultrastructure. J. Neurocytol. 24, 135-153.