Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T21:08:02.640Z Has data issue: false hasContentIssue false
  • English
  • Français

Thalamic origin of neuropeptide Y innervation of the accessory optic nucleus of the pigeon (Columba livia)

Published online by Cambridge University Press:  02 June 2009

Dânia E. Hamassaki  and
Luiz R. G. Britto
Dânia E. Hamassaki
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences, São Paulo State University, Sāo Paulo, Brazil
Luiz R. G. Britto
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences, São Paulo State University, Sāo Paulo, Brazil
Get access Rights & Permissions [Opens in a new window]

Abstract

Immunohistochemical and tracing techniques were used in combination to reveal the source of a neuropeptide Y-like immunoreactive (NPY-LI) plexus in the nucleus of the basal optic root (nBOR) of the pigeon accessory optic system. Injections of rhodamine-labeled latex microspheres into nBOR produced retrograde labeling of a population of neurons interposed between the principal optic nucleus of the dorsolateral thalamus (equivalent to the mammalian dorsal lateral geniculate nucleus) and the ventral lateral geniculate nucleus. The retrogradely labeled neurons were distributed mainly in the immediate vicinity of the lateral, dorsal, and ventral aspects of the nucleus rotundus. Immunohistochemical methods revealed many NPY-containing somata within the same intergeniculate thalamic area. Double-labeling immunohistochemical and retrograde tracing experiments evidenced that many NPY-LI neurons in the intergeniculate area contained rhodamine microspheres that had been previously injected into the ipsilateral nBOR. The projection of that general thalamic area to the nBOR was then confirmed by means of anterograde transport of Phaseolus vulgaris leucoagglutinin. In these experiments, the intergeniculate region was demonstrated to project to all divisions of the nBOR and to every other retino-recipient structure, including the suprachiasmatic nucleus. Finally, electrolytic lesions of the intergeniculate area produced a dramatic reduction in the number of NPY-LI axons and terminals within the ipsilateral nBOR and also within other retino-recipient structures. These data indicate the existence of a thalamic NPY-LI projection to the pigeon nBOR of the accessory optic system. This chemically specific projection originates from the intergeniculate area, which was shown in this study to project to all other retino-recipient structures. Thus, NPY may have a role in the functional organization of the accessory optic system and also of the avian visual system as a whole.

Keywords

Accessory optic systemImmunohistochemistryIntergeniculate leafletNeuropeptide YSubcortical visual pathwaysVisual system
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 3 , September 1990 , pp. 249 - 259
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albers, H.E. & Ferris, D. F. (1984). Neuropeptide Y: role in light-dark cycle entrainment of hamster circadian rhythms. Neuroscience Letters 50, 163–168.CrossRefGoogle ScholarPubMed
Albers, H.E., Ferris, C.F., Leeman, S.E. & Goldman, B.D. (1984). Microinjections of neuropeptides into the suprachiasmatic region of the hypothalamus phase-shifts circadian activity rhythms of Syrian hamster. Science 223, 833–835.CrossRefGoogle Scholar
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
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., Hamassaki, D.E., Keyser, K.T. & Karten, H.J. (1989). Neurotransmitters, receptors and neuropeptides in the accessory optic system: an immunohistochemical survey in the pigeon (Columba livia). Visual Neuroscience 3, 463–475.CrossRefGoogle ScholarPubMed
Britto, L.R.G., Keyser, K.T., Hamassaki, D.E. & Karten, H.J. (1988). Catecholaminergic 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
Card, J.P. & Moore, R.Y. (1982). Ventral lateral geniculate nucleus efferents to the rat suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity. Journal of Comparative Neurology 206, 390–398.CrossRefGoogle Scholar
Card, J.P. & Moora, R.Y. (1989). Organization of lateral geniculatehypothalamic connections in the rat. Journal of Comparative Neurology 284, 135–147.CrossRefGoogle ScholarPubMed
Cassone, V.M. & Moore, R.Y. (1987). Retinohypothalamic projection and suprachiasmatic nucleus of the house sparrow. Passer domesticus. Journal of Comparative Neurology 266, 171–182.Google ScholarPubMed
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
Colmers, W.F., Lukowiak, K. & Pittman, Q.J. (1987). Presynaptic action of neuropeptide Y in area CA1 of the rat hippocampal slice. Journal of Physiology 383, 285–299.CrossRefGoogle ScholarPubMed
De, Quidt M.E. & Emson, P.C. (1986). Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system. 11. Immunohistochemical analysis. Neuroscience 18, 546–618.Google Scholar
DiMaggio, D.A., Chronwall, B.M., Buchanan, K. & O'Donohue, T.L. (1985). Pancreatic polypeptide immunoreactivity in rat brain is actually neuropeptide Y. Neuroscience 15, 1149–1157.CrossRefGoogle ScholarPubMed
Dinopoulos, A., Karamanlidis, A.N., Michaloudi, H., Antonopoulos, J. & Papadopoulos, G. (1987). Retinal projections in the hedgehog (Erinaceus europaeus). An autoradiographic and horseradish peroxidase study. Anatomy and Embryology 176, 65–70.CrossRefGoogle ScholarPubMed
Edvinsson, L., Ekblad, E., Hakanson, R. & Wahlestedt, C. (1984). Neuropeptide Y potentiates the effect of various vasoconstrictor agents on rabbit blood vessels. British Journal of Pharmacology 83, 519–525.CrossRefGoogle ScholarPubMed
Edvinsson, L., Emson, P., McCulloch, J., Tatemoto, K. & Uddman, R. (1983). Neuropeptide Y: cerebrovascular innervation and vasomotor effects in the cat. Neuroscience Letters 43, 79–84.CrossRefGoogle ScholarPubMed
Edwards, S.B., Rosenquist, A.C. & Palmer, L.A. (1974). An auto-radiographic study of ventral lateral geniculate projections in the cat. Brain Research 72, 282–287.CrossRefGoogle Scholar
Eldred, W.D., Isayama, T., Reiner, A. & Carraway, R. (1988). Ganglion cells in the turtle retina contain the neuropeptide LANT-6. Journal of Neuroscience 8, 119–132.CrossRefGoogle ScholarPubMed
Emmerton, J. (1983). Functional morphology of the visual system. In Physiology and Behavior of the Pigeon, ed. Abs, M., pp. 221–244. London: Academic Press.Google Scholar
Fite, K.V. (1985). Pretectal and accessory optic visual nuclei of fish, amphibia and reptiles: theme and variations. Brain Behavior and Evolution 26, 71–90.CrossRefGoogle ScholarPubMed
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
Flood, J.F., Hernandez, E.N. & Morley, J.E. (1987). Modulation of memory processing by neuropeptide Y. Brain Research 421, 280–290.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R. & Cohen, D.H. (1988 a). Retinal projections to the pretectum in the pigeon (Columba livia). Journal of Comparative Neurology 269, 1–17.CrossRefGoogle Scholar
Gamlin, P.D.R. & Cohen, D.H. (1988 b). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 18–46.CrossRefGoogle ScholarPubMed
Gerfen, C.R. & Sawchenko, P.F. (1984). An anterograde neuroanatomical tracing method that shows detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris-leucoagglutinm (PHA-L). Brain Research 290, 219–238.CrossRefGoogle ScholarPubMed
Giolli, R.A., Peterson, G.M., Ribak, C.E., McDonald, H.M., Blanks, R.H.I. & Fallon, J.H. (1985). 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, 194–203.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
Graybiel, A.M. (1974). Visuo-cerebellar and cerebello-visual connections involving the ventral lateral geniculate nucleus. Experimental Brain Research 20, 303–306.CrossRefGoogle ScholarPubMed
Harfstrand, A. (1987). Brain neuropeptide Y mechanisms. Basic aspects and involvement in cardiovascular and neuroendocrine regulation. Acta Physiologica Scandinavica 565, 11–83.Google ScholarPubMed
Harrington, M.E., Nance, D.M. & Rusak, B. (1985). Neuropeptide Y immunoreactivity in the hamster geniculo-suprachiasmatic tract. Brain Research Bulletin 15, 465–472.CrossRefGoogle ScholarPubMed
Harrington, M.E., Nance, D.M. & Rusak, B. (1987). Double-labeling of neuropeptide Y-immunoreactive neurons which project from the geniculate to the suprachiasmatic nuclei. Brain Research 410, 275–282.CrossRefGoogle Scholar
Harrington, M.E. & Rusak, B. (1986). Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. Journal of Biological Rhythms 1, 309–325.CrossRefGoogle ScholarPubMed
Harrington, M.E. & Rusak, B. (1989). Photic responses of geniculohypothalamic tract neurons in the Syrian hamster. Visual Neuroscience 2, 367–375.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G. & Emson, P.C. (1984). Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. Journal of Neuroscience 4, 2497–2517.CrossRefGoogle ScholarPubMed
Hickey, T.L. & Spear, P.D. (1976). Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Experimental Brain Research 24, 523–529.CrossRefGoogle ScholarPubMed
Johnson, R.F., Moore, R.Y. & Morin, L.P. (1989). Lateral geniculate lesions alter circadian activity rhythms in the hamster. Brain Research Bulletin 22, 411–422.CrossRefGoogle ScholarPubMed
Johnson, R.F., Smale, L., Moore, R.Y. & Morin, L.P. (1988). Lateral geniculate lesions block circadian phase-shift responses to a benzodiazepine. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5301–5304.CrossRefGoogle ScholarPubMed
Karten, H.J., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon (Columba livia). Proceedings of the National Academy of Sciences of the U.S.A. 74, 1753–1756.CrossRefGoogle Scholar
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia), pp. 185. Baltimore, Maryland: Johns Hopkins Press.Google Scholar
Katz, L.C., Burkhalter, A. & Dreyer, W.J. (1984). Fluorescent latex microespheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310, 498–500.CrossRefGoogle Scholar
Lehman, M.N., Silver, R., Gladstone, W.R., Kahn, R.M., Gibson, M. & Bittman, E.L. (1987). Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. Journal of Neuroscience 7, 1626–1638.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
McDonald, J.K., Han, C., Noe, B.D. & Abel, P.W. (1988). High levels of NPY in rabbit cerebrospinal fluid and immunohistochemical analysis of possible sources. Brain Research 463, 259–267.CrossRefGoogle ScholarPubMed
McDonald, J.K., Lumpkin, M.D., Samson, W.K. & McCann, S.M. (1985). Neuropeptide Y affects secretion of luteinizing hormone and growth hormone in ovariectomized rats. Proceedings of the National Academy of Sciences of the U.S.A. 82, 561–564.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. & Dionne, 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
Moore, R.Y. (1989). The geniculohypothalamic tract in monkey and man. Brain Research 486, 190–194.CrossRefGoogle ScholarPubMed
Moore, R.Y. & Card, J.P. (1985). Visual pathways and the entrainment of circadian rhythms. In The Medical and Biological Effects of Light, ed. Wurtman, R.J., Baum, M.J. & Potts, J.T. Jr, pp. 123–133. New York: Annals of the New York Academy of Sciences.Google Scholar
Moore, R.Y., Gustafson, E.L. & Card, J.P. (1984). Identical immunoreactivity of afferents to the rat suprachiasmatic nucleus with antisera against avian pancreatic polypeptide, molluscan cardioexcitatory peptide and neuropeptide Y. Cell and Tissue Research 236, 41–46.CrossRefGoogle Scholar
Morin, L.P., Johnson, R.F. & Moore, R.Y. (1989). Two brain nuclei controlling circadian rhythms are identified by GFAP immunoreactivity in hamsters and rats. Neuroscience Letters 99, 55–60.CrossRefGoogle ScholarPubMed
Norgren, R.B. Jr & Silver, R. (1989). Retinohypothalamic projections and the suprachiasmatic nucleus in birds. Brain Behavior and Evolution 34, 73–83.CrossRefGoogle ScholarPubMed
Pickard, G.E. (1985). Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus. Neuroscience Letters 55, 211–217.CrossRefGoogle ScholarPubMed
Pickard, G.E., Ralph, M.R. & Menaker, M. (1987). The intergeniculate leaflet partially mediates effects of light on circadian rhythms. Journal of Biological Rhythms 2, 35–56.CrossRefGoogle ScholarPubMed
Ribak, C.E. & Peters, A. (1975). An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Research 92, 341–368.CrossRefGoogle ScholarPubMed
Rusak, B., Meijer, J.H. & Harrington, M.E. (1989). Hamster circadian rhythms are phase-shifted by electrical stimulation of the geniculo-hypothalamic tract. Brain Research 493, 283–291.CrossRefGoogle ScholarPubMed
Shen, C.L. (1987). Distribution of neuropeptide Y immunoreactivity in the forebrain of the rat. Proceedings of the National Sciences Council of the Republic of China 11, 115–127.Google ScholarPubMed
Shibata, S. & Moore, R.Y. (1989). Neuropeptide Y (NPY) produces circadian phase changes of suprachiasmatic nucleus (SCN) neuron firing rate rhythm in vitro. Society for Neuroscience Abstracts 15, 24.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.CrossRefGoogle ScholarPubMed
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988). The pretectal nuclear complex and the accessory optic system. In Neuroanatomy of the Oculomotor System, ed. Buettner-Ennever, J.A., pp. 335–364. Amsterdam: Elsevier Science Publishers.Google Scholar
Stanley, B.G. & Leibowitz, S.F. (1984). Neuropeptide Y: stimulation of feeding and drinking by injection into the paraventricular nucleus. Life Sciences 35, 2635–2642.CrossRefGoogle ScholarPubMed
Stanley, B.G. & Leibowitz, S.F. (1985). Neuropeptide Y injected in the paraventricular hypothalamus: a powerful stimulant of feeding behavior. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3940–3943.CrossRefGoogle ScholarPubMed
Swanson, L.W., Cowan, W.M. & Jones, E.G. (1974). An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. Journal of Comparative Neurology 156, 143–164.CrossRefGoogle ScholarPubMed
Takatsuji, K. & Tohyama, M. (1989). The organization of the rat lateral geniculate body by immunohistochemical analysis of neuroactive substances. Brain Research 480, 198–209.CrossRefGoogle ScholarPubMed
Tigges, M., Tigges, J., McDonald, J.K., Slattery, M. & Fernandes, A. (1989). Postnatal development of neuropeptide Y-like immunoreactivity in area 17 of normal and visually deprived rhesus monkeys. Visual Neuroscience 2, 315–328.CrossRefGoogle ScholarPubMed
Tseng, C.-J., Mosquenda-Garcia, R., Appalsamy, M. & Robertson, D. (1988). Cardiovascular effects of neuropeptide Y in rat brainstem nuclei. Circulation Research 64, 55–61.CrossRefGoogle Scholar
Vallejo, M., Carter, D.A., Biswas, S. & Lightman, S.L. (1987 a). Neuropeptide Y alters monoamine turnover in the rat brain. Neuroscience Letters 73, 155–160.CrossRefGoogle ScholarPubMed
Vallejo, M., Carter, D.A., Diez-Guerra, F.J., Emson, P.C. & Lightman, S.L. (1987 b). Neonatal administration of a specific neuropeptide Y antiserum alters the vasopressin response to haemorrhage and the hypothalamic content of noradrenaline in rats. Neuroendocrinology 45, 507–509.CrossRefGoogle ScholarPubMed
Watts, A.G. & Swanson, L.W. (1987). Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. Journal of Comparative Neurology 258, 230–252.CrossRefGoogle ScholarPubMed
Watts, A.G., Swanson, L.W. & Sanchez-Watts, G. (1987). Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. Journal of Comparative Neurology 258, 204–229.CrossRefGoogle ScholarPubMed
Weber, J.T. (1985). Pretectal complex and accessory optic system of primates. Brain Behavior and Evolution 26, 117–140.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