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Tyrosine hydroxylase-like immunoreactive neurons in the olfactory bulb of the snake, Elaphe quadrivirgata, with special reference to the colocalization of tyrosine hydroxylase- and GABA-like immunoreactivities

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Summary

The distribution and structural features of tyrosine hydroxylase-like immunoreactive (TH-LI) neurons were studied in the olfactory bulb of a snake, Elaphe quadrivirgata, by using pre-and post-embedding immunocytochemistry at the light microscopic level. In contrast to rodent olfactory bulbs previously reported, many TH-LI neurons were seen not only in the main olfactory bulb (MOB) but also in the accessory olfactory bulb (AOB). With regard to the TH-like immunoreactivity, there appeared no appreciable differences between MOB and AOB. As in mammalian MOB, the majority of TH-LI neurons were clustered in the periglomerular region and appeared to send their dendritic branches into glomeruli, which as a whole make an intense TH-LI band in the glomerular layer (GML). In the external plexiform/mitral cell layer (EPL/ML) of MOB and AOB as well as in the outer sublamina of the internal plexiform layer (OSL) of AOB, an appreciable number of TH-LI neurons were scattered, extending dendritic processes which appeared to make a loose meshwork. TH-LI neurons in EPL/ML (including OSL) appeared to consist of at least two morphologically different types. The first had a small perikaryon and one or two smooth dendrites which usually extended to GML and were frequently confirmed to enter into glomeruli. The second had a larger perikaryon and 2–3 dendrites which branched into several varicose processes extending in EPL/ML/OSL but appeared not to enter into glomeruli. The TH-like immunoreactivity was rarely seen in the internal plexiform layer and internal granule cell layer. The colocalization of GABA-like and TH-like immunoreactivities was further studied. Almost all TH-LI neurons in both EPL/ ML/OSL and GML contained GABA-like immunoreactivity irrespectively of the type of TH-LI cells.

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Abbreviations

AOB:

accessory olfactory bulb

MOB:

main olfactory bulb

Hem:

hemisphere

ON:

olfactory nerve layer

VN:

vomeronasal nerve layer

GM:

glomerular layer

EP/M:

external plexiform layer/Mitral cell layer

IP:

internal plexiform layer

IG:

internal granular layer

OS:

outer sublamina of the IPL of AOB

MS:

middle sublamina of the IPL of AOB

IS:

inner sublamina of the IPL of AOB

References

  • Alonso JR, Coveñas R, Lara J, Arévalo R, de León M, Aijón J (1989) Tyrosine hydroxylase immunoreactivity in a subpopulation of granule cells in the olfactory bulb of teleost fish. Brain Behav Evol 34:318–324

    Google Scholar 

  • Andres KH (1970) Anatomy and ultrastructure of the olfactory bulb in fish, amphibia, reptiles, bird and mammals. In: Wolstenholme GEW, Knight J (eds) Taste and Smell in Vertebrates. A Ciba Foundation Symposium, Churchill, London, pp 177–196

    Google Scholar 

  • Crosby EC, Humphrey T (1939) Studies of the vertebrate telencephalon. I. The nuclear configuration of the olfactory and accessory olfactory formations and of the nucleus olfactorius anterior of certain reptiles, birds, and mammals. J Comp Neurol 71:121–213

    Google Scholar 

  • Davis BJ, Macrides F (1983) Tyrosine hydroxylase immunoreactive neurons and fibers in the olfactory system of the hamster. J Comp Neurol 214:427–440

    Google Scholar 

  • Dubé L, Parent A (1982) The organization of monoamine-containing neurons in the brain of the salamander, Necturus maculosus. J Comp Neurol 211:21–30

    Google Scholar 

  • Franzoni MF, Thibault J, Fasolo A, Martinoli MG, Scaranari F, Calas A (1986) Organization of tyrosine-hydroxylase immunoreactive neurons in the brain of the crested newt, Triturus cristatus carnifex. J Comp Neurol 251:121–134

    Google Scholar 

  • Gall CM, Hendry SHC, Seroogy KB, Jones EG, Haycock JW (1987) Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb. J Comp Neurol 266:307–318

    Google Scholar 

  • Halpern M (1987) The organization and function of the vomeronasal system. Ann Rev Neurosci 10:325–362

    Google Scholar 

  • Halpern M, Kubie JL (1984) The role of the ophidian vomeronasal system in species-typical behavior. Trends Neurosci 7:472–477

    Google Scholar 

  • ]Halász N, Shepherd GM (1983) Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10:579–619

    Google Scholar 

  • Halász N, Nowycky M, Hökfelt T, Shepherd GM, Markey K, Goldstein M (1982) Dopaminergic periglomerular cells in the turtle olfactory bulb. Brain Res Bull 9:383–389

    Google Scholar 

  • Hornby PJ, Piekut DT, Demski LS (1987) Localization of immunoreactive tyrosine hydroxylase in the goldfish brain. J Comp Neurol 261:1–14

    Google Scholar 

  • Hsu S-M, Raine L, Fanger H (1981) Use of avidin-biotin-perixidase complex (ABC) in immunoperoxidase techniques. J Histochem Cytochem 29:577–580

    CAS  PubMed  Google Scholar 

  • Kosaka K, Hama K, Nagatsu I, Wu J-Y, Ottersen OP, Storm-Mathisen J, Kosaka T (1987) Postnatal development of neurons containing both catecholaminergic and GABAergic traits in the rat main olfactory bulb. Brain Res 403:355–360

    Google Scholar 

  • Kosaka K, Hama K, Nagatsu I, Wu J-Y, 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 hydroxylase and substance P in the hamster olfactory bulb. Exp Brain Res 71:633–642

    Google Scholar 

  • Kosaka T (1980) Ruffed cell: a new type of neuron with a distinctive initial unmyelinated portion of the axon in the olfactory bulb of the goldfish (Carassius auratus). II. Fine structure of the ruffed cell. J Comp Neurol 193:119–145

    Google Scholar 

  • Kosaka T, Hama K (1979) Ruffed cell: a new type of neuron with a distinctive initial unmyelinated portion of the axon in the olfactory bulb of the goldfish (Carassius auratus) I. Golgi impregnation and serial thin sectioning studies. J Comp Neurol 186:301–320

    Google Scholar 

  • Kosaka T, Hama K (1980) Presence of the ruffed cell in the olfactory bulb of the catfish, Parasilurus asortus, and the sea eel, Conger myriaster. J Comp Neurol 193:103–117

    Google Scholar 

  • Kosaka T, Hama K (1981) Ruffed cell: a new type of neuron with a distinctive initial unmyelinated portion of the axon in the olfactory bulb of the goldfish (Carassius auratus). III. Threedimensional structure of the ruffed cell dendrite. J Comp Neurol 201:571–587

    Google Scholar 

  • Kosaka T, Hama K (1982–1983) Synaptic organization in the teleost olfactory bulb. J Physiol, Paris 78:707–719

    Google Scholar 

  • Kosaka T, Hataguchi Y, Hama K, Nagatsu I, Wu J-Y (1985a) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase 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

    Google Scholar 

  • Kosaka T, Kosaka K, Tateishi K, Hamaoka Y, Yanaihara N, Wu J-Y, Hama K (1985b) GABAergic neurons containing CCK-8like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J Comp Neurol 239:420–430

    Google Scholar 

  • Kosaka T, Nagatsu I, Wu J-Y, Hama K (1986) Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18:975–990

    Google Scholar 

  • Kosaka T, Kosaka K, Hataguchi Y, Nagatsu I, Wu J-Y, Ottersen OP, Strom-Mathisen J, Hama K (1987) Catecholaminergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 66:191–210

    Google Scholar 

  • Lane BP, Europa DL (1965) Differental staining of ultrathin sections of epon-embedded tissues for light microscopy. J Histochem Cytochem 13:579–582

    CAS  PubMed  Google Scholar 

  • Matute C, Streit P (1986) Monoclonal antibodies demonstrating GABA-like immunoreactivity. Histochemistry 86:147–157

    Google Scholar 

  • Meredith GE, Smeets WJAJ (1987) Immunocytochemical analysis of the dopamine system in the forebrain and midbrain of Raja radiata: evidence for a substantia nigra and ventral tegmental area in cartilaginous fish. J Comp Neurol 265:530–548

    Google Scholar 

  • Nagatsu I (1983) Immunohistocytochemistry of biogenic amines and immunoenzyme-histochemistry of catecholaminesynthesizing enzymes. In: Parvez S, Nagatsu T, Nagatsu I, Parvez H (eds) Methods in biogenic amine research. Elsevier/North-Holland, Amsterdam, pp 873–909

    Google Scholar 

  • Nagatsu I, Karasawa N, Kawakami Y, Yoshida M (1984) Studies on monoamine-containing neurons by immunoenzymehistocytochemistry and immunohistocytochemistry with special reference to goldfish brain. Acta Histochem Cytochem 17:151–160

    Google Scholar 

  • Northcutt RG, Reiner A, Karten HJ (1988) Immunohistocytochemical study of the telencephalon of the spiny dogfish, Squalus acanthias. J Comp Neurol 277:250–267

    Google Scholar 

  • Reiner A, Northcutt RG (1987) An immunohistochemical study of the telencephalon of the African lungfish, Protopterus annectens. J Comp Neurol 277:250–267

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry (2nd edn) Wiley, New York

    Google Scholar 

  • Wulle I, Wagner H-J (1990) GABA and tyrosine hydroxylase immunocytochemistry reveal different patterns of colocalization in retinal neurons of various vertebrates. J Comp Neurol 296:173–178

    Google Scholar 

  • Yoshida M, Nagatsu I, Kondo Y, Karasawa N, Ohno T, Spatz M, Nagatsu T (1983) Immunohistocytochemical localization of the neurons containing catecholamine-synthesizing enzymes and serotonin in the brain of bullfrog (Rana catesbiana). Acta Histochem Cytochem 16:245–258

    Google Scholar 

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Kosaka, T., Kosaka, K. & Nagatsu, I. Tyrosine hydroxylase-like immunoreactive neurons in the olfactory bulb of the snake, Elaphe quadrivirgata, with special reference to the colocalization of tyrosine hydroxylase- and GABA-like immunoreactivities. Exp Brain Res 87, 353–362 (1991). https://doi.org/10.1007/BF00231852

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  • DOI: https://doi.org/10.1007/BF00231852

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