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Neurotransmitters, receptors, and neuropeptides in the accessory optic system: An immunohistochemical survey in the pigeon (Columba livia)

Published online by Cambridge University Press:  02 June 2009

Luiz R. G. Britto ,
Dania E. Hamassaki ,
Kent T. Keyser  and
Harvey J. Karten
Luiz R. G. Britto
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences Sāo PauloState University (USP), Sāo, Paulo, Brazil
Dania E. Hamassaki
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences Sāo PauloState University (USP), Sāo, Paulo, Brazil
Kent T. Keyser
Affiliation:
Department of Neurosciences, School of Medicine, University of California at San Diego, La Jolla
Harvey J. Karten
Affiliation:
Department of Neurosciences, School of Medicine, University of California at San Diego, La Jolla
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Abstract

Immunohistochemical techiniques were used to survey the distribution of several conventional transmitters, receptors, and neuropeptides in the pigeon nucleus of the basal optic root (nBOR), a component of the accessory optic ststem. Amongst the conventional neurotransmitts'modulators, the most intense labeling of fibers/terminals within the nBOR was obtained with antisera directed against glutamic acid decarboxylase (GAD) and serotonin (5-HT). Moderately dense fiber plexuses were seen to label with antibodies directed against tyrosine hydroxylase (TH) and choline acetltransferase (ChAT). GAD-like immunoractivity (GAD-L1) was found in many small and medium-size perikarya within the nBOR. Some of the medium-sized cells were occasionally positive for ChAT-L1. Cell body and dendritic staining was also commonly seen with the two tested antisera against receptors–anti-GABA-A receptor and anti-nicotinic acetylcholine receptor.

The antisera directed against various neuropetides produced only fiber labelling within the nBOR. The densest fiber plexus staining was observed with antiserum against neuropeptide Y (NPY-L1), while intermediate fiber densities were seen for substance P (SP-L1) and cholecystokinin (CCK-L1). A few varicose fibers were labeled with antisera against neurotensin (NT), leucine-enkephalin (L-KNK), and the vasoactive intestinal polypeptide (VIP).

Unilateral enucleation produced an almost complete elimination of TH-L1 in the contralateral nBOR. SP-L1 and CCK-L1 were also decreased after enucleation. No apparent changes were seen for all other substances.

These results indicate that a wide variety of chemically-specific systems arborize within the nBOR. Three of the immunohistochemically defined fiber systems (TH-LI, SP-LI, and CCK-LI fibers) were reduced after removal of the retina, which may indicate the presence of these substances in retinal ganglion cells. In contrast, the fibers exhibiting ChAT-LI, GAD-LI, 5-HT-Ll, NPY-Ll, NT-LI, L-ENK-LI, and VIP-LI appear to be of nonretinal origin. Two different populations of nBOR neurons exhibited GAD-LI and ChAT-LI. However, these two populations together constituted only about 20% of the nBOR neurons.

Keywords

Accessory optic systemImmunohistochemistryNeuropeptidesNeurotransmittersVisual system
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 5 , November 1989 , pp. 463 - 475
Copyright
Copyright © Cambridge University Press 1989

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References

Atweh, S.F. & Kuhar, M.J. (1977). Autoradiographic localization of opiate receptors in rat brain, II: The brain stem. Brain Research 129, 1–12.CrossRefGoogle ScholarPubMed
Atweh, S.F., Murrin, L.C. & Kuhar, M.J. (1978). Presynaptic localization of opiate receptors in the vagal and accessory optic system: an autoradiographic study. Neuropharmacology 17, 655–71.CrossRefGoogle ScholarPubMed
Azevedo, T.A., Cukiert, A. & Britto, L.R.G. (1983). A pretectal projection upon the accessory optic nucleus in the pigeon: an anatomical and electrophysiological study. Neuroscience Letters 43, 13–18.CrossRefGoogle ScholarPubMed
Bagnoli, P. & Casini, G. (1985). Regional distribution of catecholaminergic terminals in the pigeon visual system. Brain Research 337, 277–286.CrossRefGoogle ScholarPubMed
Brauth, S.E., Kitt, C.A., Reiner, A. & Quirion, R. (1986). Neurotensin binding sites in the forebrain and midbrain of the pigeon. Journal of Comparative Neurology 253, 358–373.CrossRefGoogle ScholarPubMed
Brecha, N., Johnson, D., Bolz, J., Sharma, S., Parnavelas, J.G. & Lieberman, A.R. (1987). Substance P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit. Nature 327, 155–158.CrossRefGoogle ScholarPubMed
Brecha, N. & Karten, H.J. (1981). Organization of the avian accessory optic system. Annals of the New York Academy of Sciences 374, 215–229.CrossRefGoogle ScholarPubMed
Brecha, N., Karten, H.J. & Hunt, S.P. (1980). Projections of the nucleus of the basal optic root in the pigeon: an autoradiographic and horseradish peroxidase study. Journal of Comparative Neurology 189, 615–670.CrossRefGoogle ScholarPubMed
Britto, L.R.G. (1983). Retinal ganglion cells of the pigeon accessory optic system. Brazilian Journal of Medical and Biological Research 16, 357–363.Google ScholarPubMed
Britto, L.R.G., Keyser, K.T., Hamassaki, D.E. & Karten, H.J. (1988). Catecholominergic subpopulation of retinal displaced ganglion cells projects to the accessory optic nucleus in the pigeon (Columba livia). Journal of Comparative Neurology 269, 109–117.CrossRefGoogle Scholar
Britto, L.R.G., Natal, C.L., & Marcondes, A.M., (1981). The access sory optic system in pigeons: receptive field properties of identified neurons. Brain Research 206, 149–154.CrossRefGoogle Scholar
Card, J.P. & Moore, R.Y. (1982). Ventral lateral geniculated nucleus efferents to the suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity. Journal of Comparative Neurology 206, 390–398.CrossRefGoogle Scholar
Chronwall, B.M., DiMaggio, D.A., Massari, V.J., Pickel, V.M., Ruggiero, D.A. & O'Donohue, T.L. (1985). The anatomy of neuropeptide-Y containing neurons in rat brain. Neuroscience 15, 1159–1181.CrossRefGoogle ScholarPubMed
De, Quidt M.E. & Emson, P.C. (1986). Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system. II. Immunohistochemical analysis. Neuroscience 18, 546–618.Google Scholar
Dietl, M.M., Cortes, R. & Palacios, J.M. (1988 a). Neurotransmitter receptors in the avian brain. II. Muscarinic cholintergic receptors. Brain Research 439, 360–365.CrossRefGoogle ScholarPubMed
Dietl, M.M., Cortes, R. & Palacios, J.M. (1988 b). Neurotransmitter receptors in the avian brain. III. GABA- benzodiazepine receptors. Brain Research 439, 366–371.CrossRefGoogle ScholarPubMed
DiMaggio, D.A., Chronwall, B.M., Buchanan, K. & O'Donohue, T.L. (1985). Pancreatic polypetide immunoreactivity in rat brain is actually neurpeptide Y. Neuroscience 15, 1149–1157.CrossRefGoogle Scholar
Domenici, L., Waldvogel, H.J., Matute, C. & Streit, P. (1988). Distribution of GABA-like immunoreactivity in the pigeon brain. Neuroscience 25, 931–950.CrossRefGoogle ScholarPubMed
Ehrlich, D., Keyser, K.T. & Karten, H.J. (1987). The distribution of substance P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallus gallus). Journal of Comparative Neurology 266, 220–233.CrossRefGoogle ScholarPubMed
Eldred, W.D., Isayama, T., Reiner, A. & Carraway, R. (1988). Ganglion cells in the turtle retina contain the neurpeptide LANT-6. Journal of Neuroscience 8, 119–132.CrossRefGoogle ScholarPubMed
Fite, K.V. (1985). Pretectal and accessory optic visula nuclei of fish, amphibia and reptiles: theme and variations. Brain Behaviour and Evolution 26, 71–90.CrossRefGoogle Scholar
Fite, K.V., Brecha, N. & Karten, H.J. (1981). Displaced ganglion cells and the accessory optic system of pigeon. Journal of Comparative Neurology 195, 279–288.CrossRefGoogle ScholarPubMed
Fuxe, K. & Ljunggren, L. (1965). Cellular localization of monoamines in the upper brain stem of the pigeon. Journal of Comparative Neurology 125, 355–382.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R. & Cohen, D.H. (1988). Projections of the retinorecipient pretectal nucleri in the pigeon (Columba livia). Journal of Comparative Neurology 269, 18–46.CrossRefGoogle ScholarPubMed
Giolli, R.A., Blanks, R.H.I. & Torigoe, Y. (1984). Pretectal and brain stem projections of the medial terminal nucleus of the accessory optic system of the rabbit and rat as studied by anterograde and retrograde neuronal tracing methods. Journal of Comparative Neurology 227, 228–251.CrossRefGoogle ScholarPubMed
Giolli, R.A., Blanks, R.H.I., Torigoe, Y. & Williams, D.D. (1985 a). Projections of medial terminal accessory optic nucleus, ventral tegmental nuclei, and substantia nigra of rabbit and rat as studied by retrograde axonal transport of horseradish peroxidase. Journal of Comparative Neurology 232, 99–116.CrossRefGoogle ScholarPubMed
Giolli, R.A., Peterson, G.M., Ribak, C.E., McDonald, H.M., Blanks, R.H.I. & Fallon, J.H. (1985 b). GABAergic neurons comprise a major cell type in rodent visual relay nuclei: an immunocytochemical study of pretectal and accessory optic nuclei. Experimental Brain Research 61, 194–20.CrossRefGoogle Scholar
Giolli, R.A., Torigoe, Y. & Blanks, R.H.I. (1988). Nonretinal projections to the medial terminal accessory optic nucleus in rabbit and rat: a retrograde and anterograde transport study. Journal of Comparative Neurology, 269, 73–86.CrossRefGoogle Scholar
Goedert, M. (1984). Neurotensin–a status report. Trends in Neurosciences 7, 3–5.CrossRefGoogle Scholar
Gottlieb, M.D. & McKenna, O.C. (1986). Light and electron microscopic study of an avian pretectal nucleus, the lentiform nucleus of the mesencephalon, magnocellular division. Journal of Comparative Neurology 248, 133–145.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Cynader, M.S. (1986). Response properties of single units in the accessory optic system of the dark-reared cat. Developmental Brain Research 27, 199–210.CrossRefGoogle Scholar
Grasse, K.L. & Cynader, M.S. (1987). The accessory optic system of the monocularly deprived cat. Brain Research 428, 229–241.CrossRefGoogle ScholarPubMed
Hamassaki, D.E., Gasparotto, O.C., Nogueria, M.I. & Britto, L.R.G. (1988). Telencephalic and pretectal modulation of the directional selectivity of accessory optic neurons in the pigeon. Brazilian Journal of Medical and Biological Research 21, 649–652.Google ScholarPubMed
Herkenham, M. (1987). Mismatches between neurotransmitter and receptor localizations in brain: observations and implications. Neuroscience 23, 1–38.CrossRefGoogle ScholarPubMed
Johnson, C.D. & Epstein, M.L. (1986). Monoclonal antibodies and polyvalent antiserum to chicken choline acetyltransferase. Journal of Neurochemistry 46, 968–976.CrossRefGoogle ScholarPubMed
Karten, H.J. (1979). Visual lemniscal pathways in birds. In Neural Mechanisms of Behaviour in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 409–430. New York: Plenum PressGoogle Scholar
Karten, H.J. & Kuijis, R.O. (1986). Lamination and peptidergic systems in the frog optic tectum. In Comparative Neurobiology: Modes of Communication in the Nervous System, ed. Cohen, M.J. & Strumwasser, F., pp. 213–224. New York: John Wiley & Sons, Inc.Google Scholar
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, Maryland: Johns Hopkins Press, 185 pp.Google Scholar
Karten, H.J., Reiner, A. & Brecha, N. (1982). Laminar Organization and origins of neuropeptides in the avian retina and optic tectum. In Cytochemical Methods in Neuroanatomy, ed. Chan, Palay V. & Palay, S.L., pp. 189–204. New York: Alan R. Liss, Inc.Google Scholar
Keyser, K.T., Hughes, T.E., Whiting, P.J., Lindstrom, J.M. &Karten, H.J. (1988). Cholinoceptive neurons in the retina of the chick: an immunohistochemical study of the nicotinic acetylcholine receptors.Visual Neuroscience 1, 349–366.CrossRefGoogle ScholarPubMed
Kiss, J.Z. & Peczely, P. (1987). Distribution of tyrosine-hydroxylase (TH)-immunoreactive neurons in the diencephalon of the pigeon (Columba livia domestica). Journal of Comparative Neurology 257,333–346.CrossRefGoogle ScholarPubMed
Kuljis, R.O. & Karten, H.J. (1983). Modifications in the laminar organization of peptide-like immunoreactivity in the anuran optic tecturn following retinal deafferentation. Journal of Comparative Neurology 217, 239–251.CrossRefGoogle ScholarPubMed
Kuljis, R.O. & Karten, H.J. (1986). Substance P-containing ganglion cells become progressively less detectable during retinotectal development in the frog Rana pipiens. Proceedings of the National Academy of Sciences of the U.S.A. 83, 5736–5740.CrossRefGoogle ScholarPubMed
Lindstrom, J.M., Schoeper, R. & Whiting, P. (1987). Molecular studies of the neuronal nicotinic acetylcholine receptor family. Molecular Neurobiology 1, 281–337.CrossRefGoogle ScholarPubMed
London, E.D., Dam, M. &Fanelli, R.J. (1988). Nicotine enhances cerebral glucose utilization in central components of the rat visual system. Brain Research Bulletin 20, 381–385.CrossRefGoogle ScholarPubMed
Mantyh, P.W. & Kemp, J.A. (1983). The distribution of putative neurotransmitters in the lateral geniculate nucleus of the rat. Brain Research 288, 344–348.CrossRefGoogle ScholarPubMed
McKenna, O.C. & Wallman, J. (1985). Accessory optic system and pretectum of birds: comparison with those of other vertebrates. Brain Behavior and Evolution 26, 91–116.CrossRefGoogle ScholarPubMed
Miceli, D., Reperant, J., Villalobos, J. & Dionnel, L. (1987). Extratelencephalic projections of the avian visual Wulst. A quantitative autoradiographic study in the pigeon (Columba livia). Journal für Hirnforschung 28, 45–57.Google Scholar
Morgan, B. & Frost, B.J. (1981). Visual response characteristics of neurons in nucleus of basal optic root of pigeons. Experimental Brain Research 42, 181–188.CrossRefGoogle ScholarPubMed
Natal, C.L. & Britto, L.R.G. (1987). The pretectal nucleus of the optic tract modulates the direction selectivity of accessory optic neurons in rats. Brain Research 419, 320–323.CrossRefGoogle ScholarPubMed
Natal, C.L. & Britto, L.R.G. (1988). The rat accessory optic system: effects of cortical lesions on the directional selectivity of units within the medial terminal nucleus. Neuroscience Letters 91, 154–159.CrossRefGoogle ScholarPubMed
Oertel, W.H., Schmechel, D.E., Tappaz, M.L. & Kopin, I. J. (1981). Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6, 2689–2700.CrossRefGoogle ScholarPubMed
Peduzzi, J.D. & Crossland, W.J. (1983). Anterograde transneuronal degeneration in the ectomamillary nucleus and ventral lateral geniculate nucleus of the chick. Journal of Comparative Neurology 213, 287–300.CrossRefGoogle ScholarPubMed
Penny, G.R., Conley, M., Schmechel, D.E. & Diamond, I.T. (1984). The distribution of glutamic acid decarboxylase immunoreactivity in the diencephalon of the opossum and rabbit. Journal of Comparative Neurology 228, 38–56.CrossRefGoogle ScholarPubMed
Reiner, A., Brauth, S.E., Kitt, C.A. & Quirion, R. (1989). Distribution of Mu, Delta and Kappa opiate receptor types in the forebrain and midbrain of pigeons. Journal of Comparative Neurology 280, 359–382.CrossRefGoogle ScholarPubMed
Reiner, A., Eldred, W.D., Beinfeld, M.C. & Krause, J.E. (1985). The co-occurrence of a substance P-like peptide and cholecystokinin-8 in a fiber system of turtle cortex. Journal of Neuroscience 5, 1527–1544.CrossRefGoogle Scholar
Reiner, A., Krause, J.E., Keyser, K.T., Eldred, W.D. & McKelvy, J.F. (1984). The distribution of substance P in turtle nervous system: a radioimmunoassay and immunohistochemical study. Journal of Comparative Neurology 226, 50–75.CrossRefGoogle ScholarPubMed
Reubi, J.C. & Jessell, T.M. (1978). Distribution of substance P in the pigeon brain. Journal of Neurochemistry 31, 359–361.Google ScholarPubMed
Rio, J.P. (1979). The nucleus of the basal optic root in the pigeon: an electron microscope study. Archives d'Anatomie Microscopique et de Morphologie Experimentale 68, 17–27.Google ScholarPubMed
Rio, J.P., Villalobos, J., Miceli, D. & Reperant, J. (1983). Efferent projections of the visual Wulst upon the nucleus of the basal optic root in the pigeon. Brain Research 271, 145–251.CrossRefGoogle ScholarPubMed
Sako, H., Kojima, T. & Okado, N. (1986). Immunohistochemical study on the development of serotoninergic neurons in the chick: I. Distribution of cell bodies and fibers in the brain. Journal of Comparative Neurology 253, 61–78.CrossRefGoogle Scholar
Shen, C.L. & Baisden, R.H. (1986). Expansion of the ipsilateral retina projection to the medial terminal nucleus of the accessory optic system in rats with one eye removed. Experimental Neurology 93, 270–274.CrossRefGoogle Scholar
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian geniculate nucleus. Experimental Brain Research 63, 1–20.CrossRefGoogle ScholarPubMed
Shute, C.C.D. & Lewis, P.R. (1967). The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90, 497–520.CrossRefGoogle ScholarPubMed
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.CrossRefGoogle ScholarPubMed
Smeets, W.J. & Steinbusch, H.W. (1988). Distribution of serotonin immunoreactivity in the forebrain and midbrain of the lizard Gekko gecko. Journal of Comparative Neurology 271, 419–434.CrossRefGoogle ScholarPubMed
Swanson, L.W., Simmons, D.M., Whiting, P.J. & Lindstrom, J. (1987). Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. Journal of Neuroscience 7, 3334–3342.CrossRefGoogle ScholarPubMed
Thanos, S. & Bonhoeffer, F. (1983). Investigations on the development and topographical order of retinotectal axons: anterograde and retrograde staining of axons and perikarya with rhodamine in vivo. Journal of Comparative Neurology 219, 420–430.CrossRefGoogle ScholarPubMed
Thanos, S., Vidal-Sanz, M. & Aguayo, A.J. (1987). The use of rhodamine-B-isothiocyanate (RITC) as an anterograde and retrograde tracer in the adult rat visual system. Brain Research 406, 317–321.CrossRefGoogle ScholarPubMed
Vitorica, J., Park, D., Chin, G. & De Blas, A.L. (1988). Monoclonal antibodies and conventional antisera to the GABA-A receptor/benzodiazepine receptor/Cl–channel complex. Journal of Neuroscience 8, 615–622.CrossRefGoogle Scholar
Whiting, P. & Lindstrom, J. (1986). Purification and characterization of nicotinic acetyicholine receptor from chick brain. Biochemistry 25, 2082–2093.CrossRefGoogle Scholar
Wolters, J.G., Ten, Donkelaar H.J., Steinbusch, H.W.M. & Verhofstad, A.A.J. (1985). Distribution of serotonin in the brain stem and spinal cord of the lizard Varanus exanthematicus: an immunohistochemical study. Neuroscience 14, 169–193.CrossRefGoogle ScholarPubMed
Yucel, Y.H., Hindelang, C., Stoeckel, M.E., & Bonaventure, N. (1988). GAD immunoreactivity in pretectal and accessory optic nuclei of the frog mesencephalon. Neuroscience Letters 84, 1–6.CrossRefGoogle ScholarPubMed