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Postnatal development of neuropeptide Y-like immunoreactivity in area 17 of normal and visually deprived rhesus monkeys

Published online by Cambridge University Press:  02 June 2009

Margarete Tigges ,
Johannes Tigges ,
John K. McDonald ,
Michael Slattery  and
Alcides Fernandes
Margarete Tigges
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology and Ophthalmology, Emory University, Atlanta
Johannes Tigges
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology and Ophthalmology, Emory University, Atlanta
John K. McDonald
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology and Ophthalmology, Emory University, Atlanta
Michael Slattery
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology and Ophthalmology, Emory University, Atlanta
Alcides Fernandes
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology and Ophthalmology, Emory University, Atlanta
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Abstract

Immunocytochemical methods were used to examine neuropeptide Y (NPY) immunoreactive neurons and fibers in area 17 of rhesus monkeys during the first year of life. NPY-immunoreactive (+) neurons are nonpyramidal cells which are either multipolar, bipolar, or bitufted in shape. They occur most frequently in layer 6 and the subjacent white matter, are sparser in the supragranular layers, and absent from layer 4C. Labeled somata in the supragranular layers are smaller compared to those in layer 6 and the white matter. A typical axon originates from the NPY+ soma or from a primary dendrite and frequently is varicose. Distribution and morphologies of NPY+ neurons in area 17 of infants are similar to those of adult monkeys. Thus, it seems that NPY+ neurons in rhesus monkeys are mature from birth. NPY+ fibers occur in area 17 from birth; however, they differ in density and distribution from those of older infant and adult monkeys. At birth, a prominent fiber plexus is found in the deepest part of layer 1, and another in the white matter. Immunoreactive processes are sparse in the remaining cortical gray, except for some vertical fibers extending from pia to white matter. By 4 months of age, labeled fibers form a coarse network in layers 2, 3, 5, and 6. In addition, a distinct plexus extends through layers 4B, 4A, and the lowest aspect of layer 3. Also, a thin immunoreactive fiber band is found at the bottom of layer 4C. In the remainder of layer 4C, NPY+ fibers are scant. The supragranular layers also exhibit a unique immunoreactive “snarl” of fibers. Increases in density of NPY+ processes in the older infants are gradual so that between 7 and 13 months of age, NPY+ fibers appear to have achieved adultlike densities. These observations indicate that NPY+ fibers in area 17 of newborn rhesus monkeys undergo postnatal maturation which reaches a plateau around 4 months of age. After monocular visual deprivation from birth to 4 months of age, either by eyelid suture or by occlusion with an opaque contact lens, density and distribution of NPY+ neurons and fibers, including snarls, appear similar to those of age-matched undeprived infants. Thus, disruption of the normal binocular input does not seem to arrest the maturation of the NPY system in area 17 of rhesus monkeys during a sensitive period of early postnatal development.

Keywords

NPYArea 17Rhesus monkeyDevelopmentDeprivation
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 3 , March 1989 , pp. 315 - 328
Copyright
Copyright © Cambridge University Press 1989

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References

Adrian, T.E., Allen, J.M., Bloom, S.R., Ghatei, M.A., Rossor, M.N., Roberts, G.W., Crow, T.J., Tatemoto, K. & Polak, J.M. (1983). Neuropeptide Y distribution in human brain. Nature 306, 584–586.CrossRefGoogle ScholarPubMed
Allen, Y.S., Adrian, T.E., Allen, J.M., Tatemoto, K., Crow, T.J., Bloom, S.R. & Polak, J.M. (1983). Neuropeptide Y distribution in the rat brain. Science 221, 877–879.CrossRefGoogle ScholarPubMed
Allen, J.M., Mcgregor, G.P., Woodhams, P.L., Polak, J.M. & Bloom, S.R. (1984). Ontogeny of a novel peptide, neuropeptide Y (NPY), in rat brain. Brain Research 303, 197–200.CrossRefGoogle ScholarPubMed
Beal, M.F., Mazurek, M.F., Chattha, G.K., Svendsen, C.V., Bird, E.D. & Martin, J.B. (1986). Neuropeptide Y immunoreactivity is reduced in cerebral cortex in Alzheimer's disease. Annals of Neurology 20, 282–288.CrossRefGoogle ScholarPubMed
Beal, M.F., Mazurek, M.F. & Martin, J.B. (1987). A comparison of somatostatin and neuropeptide Y distribution in monkey brain. Brain Research 405, 213–219.CrossRefGoogle ScholarPubMed
Chan-Palay, V., Allen, Y.S., Lang, W., Haesler, U. & Polak, J.M. (1985 a). I. Cytology and distribution in normal human cerebral cortex of neurons immunoreactive with antisera against neuropeptide Y. Journal of Comparative Neurology 238, 382–389.CrossRefGoogle ScholarPubMed
Chan-Palay, V., Lang, W., Allen, Y.S., Haesler, U. & Polak, J.M. (1985 b). II. Cortical neurons immunoreactive with antisera against neuropeptide Y are altered in Alzheimer's-type dementia. Journal of Comparative Neurology 238, 390–400.CrossRefGoogle Scholar
Chan-Palay, V., KÖHler, C., Haesler, U., Lang, W. & Yasargil, G. (1986). Distribution of neurons and axons immunoreactive with antisera against neuropeptide Y in the normal human hippocampus. Journal of Comparative Neurology 248, 360–375.CrossRefGoogle ScholarPubMed
Chan-Palay, V. & Yasargil, G. (1986). Immunocytochemistry of human brain tissue with a polyclonal antiserum against neuropeptide Y. Anatomy and Embryology 174, 27–33.CrossRefGoogle ScholarPubMed
Coons, A.H. (1956). Histochemistry with labeled antibody. International Review of Cytology 5, 1–23.CrossRefGoogle Scholar
Crawford, M.L.J. & Marc, R.E. (1976). Light transmission of cat and monkey eyelids. Vision Research 16, 323–324.CrossRefGoogle Scholar
Dawbarn, D., Hunt, S.P. & Emson, P.C. (1984). Neuropeptide Y: regional distribution, chromatographic characterization, and immu-nohistochemical demonstration in postmortem human brain. Brain Research 296, 168–173.CrossRefGoogle Scholar
Fernandes, A., Tigges, M., Tigges, J., Gammon, J.A. & Chandler, C. (1988). Management of extended-wear contact lenses in infant rhesus monkeys. Behavior Research Methods, Instruments, and Computers 20, 11–17.CrossRefGoogle Scholar
Fitzpatrick, D., Lund, J.S., Schmechel, D.E. & Towles, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Foote, S.L. & Morrison, J.H. (1984). Postnatal development of laminar innervation patterns by monoaminergic fibers in monkey (Macaca fascicularis) primary visual cortex. Journal of Neurosci-ence 4, 2667–2680.CrossRefGoogle ScholarPubMed
Foote, S.L. & Morrison, J.H. (1987). Development of the noradrener-gic, serotonergic, and dopaminergic innervation of neocortex. Current Topics in Developmental Biology 21, 391–423.CrossRefGoogle ScholarPubMed
Foster, G.A. & Schultzberg, M. (1984). Immunohistochemical analysis of the ontogeny of neuropeptide Y immunoreactive neurons in foetal rat brain. International Journal of Developmental Neurosci-ence 2, 387–407.CrossRefGoogle ScholarPubMed
Foster, G.A., Schultzberg, M. & Goldstein, M. (1984). Differential and independent manifestation within co-containing neurons of neuropeptide Y and tyrosine hydroxylase during ontogeny of the rat central nervous system. Neurochemistry International 6, 761–771.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P.S. & Brown, R.M. (1982). Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. Developmental Brain Research 4, 339–349.CrossRefGoogle Scholar
Harwerth, R.S., IIISmith, E.L., Duncan, G.C., Crawford, M.L.J. & Von Noorden, G.K. (1986). Multiple sensitive periods in the development of the primate visual system. Science 232, 235–238.CrossRefGoogle ScholarPubMed
Hayashi, M. & Oshima, K. (1986). Neuropeptides in cerebral cortex of macaque monkey (Macaca fuscata fuscata:) regional distribution and ontogeny. Brain Research 364, 360–368.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. (1985). Dots, stripes, and columns in monkey visual cortex. Trends in Neuroscience 8, 406–410.CrossRefGoogle Scholar
Hendrickson, A.E., Hunt, S.P. & Wu, J.-Y. (1981). Immunocyto-chemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292, 605–607.CrossRefGoogle Scholar
Hendrickson, A.E., Movshon, J.A., Eggers, H.M., Gizzi, M.S., Boothe, R.G. & Kiorpes, L. (1987). Effects of early unilateral blur on the macaque's visual system. II. Anatomical observations. Journal of Neuroscience 7, 1327–1339.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
Hendry, S.H.C., Schwark, H.D., Jones, E.G. & Yan, J. (1987). Numbers and proportions of Gaba-immunoreactive neurons in different areas of monkey cerebral cortex. Journal of Neuroscience 7, 1503–1519.CrossRefGoogle ScholarPubMed
HöKfelt, T., Lundberg, J.M., Lagercrantz, H., Tatemoto, K., Mutt, V., Lindberg, J., Terenius, L., Everitt, B.J., Fuxe, K., Agnati, L. & Goldstein, M. (1983). Occurrence of neuropeptide Y (NPY)-like immunoreactivity in catecholamine neurons in the human medulla oblongata. Neuroscience Letters 36, 217–222.CrossRefGoogle ScholarPubMed
Jeffery, G. & Parnavelas, J.G. (1987). Early visual deafferentation of the cortex results in an asymmetry of somatostatin-labeled cells. Experimental Brain Research 67, 651–655.CrossRefGoogle Scholar
Jones, E.G. & Hendry, S.H.C. (1986 a). Peptide-containing neurons of the primate cerebral cortex. In Neuropeptides in Neurologic and Psychiatric Disease, ed. Martin, J.B. & Barchas, J.D., pp. 163–178. New York: Raven Press.Google Scholar
Jones, E.G. & Hendry, S.H.C. (1986 b). Co-localization of Gaba and neuropeptides in neocortical neurons. Trends in Neuroscience 9, 71–76.CrossRefGoogle Scholar
Kosofsky, B.E., Molliver, M.E., Morrison, J.H. & Foote, S.L. (1984). The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey (Macaca fascicularis). Journal of Comparative Neurology 230, 168–178.CrossRefGoogle ScholarPubMed
Levay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191, 1–51.CrossRefGoogle ScholarPubMed
Levitt, P., Rakic, P. & Goldman-Rakic, P. (1984). Region-specific distribution of catecholamine afferents in primate cerebral cortex: a fluorescence histochemical analysis. Journal of Comparative Neurology 227, 23–36.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 a). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 a). Specificity of intrinsic connections in primate primary visual cortex. Journal of Neuroscience 4, 2830–2835.CrossRefGoogle ScholarPubMed
Mcdonald, J.K. (1988). NPY and related substances. In CRC Critical Reviews in Neurobiology, ed. Nelson, J., Boca Raton: CRC Press 4, 97–135.Google Scholar
Mcdonald, J.K., Dees, W.L., Ahmed, C.E., Noe, B.D. & Ojeda, S.R. (1987 a). Biochemical and immunocytochemical characterization of neuropeptide Y in the immature rat ovary. Endocrinology 120, 1703–1710.CrossRefGoogle ScholarPubMed
McDonald, J.K., Koenig, J.I., Gibbs, D.M., Collins, P. & Noe, B.D. (1987 b). High concentrations of neuropeptide Y in pituitary portal blood of rats. Neuroendocrinology 46, 538–541.CrossRefGoogle ScholarPubMed
McDonald, J.K., Parnavelas, J.G., Karamanlidis, A.N., Brecha, N. & Koenig, J.I. (1982 a). The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. I. Somatostatin. Journal of Neurocytology 11, 809–824.CrossRefGoogle Scholar
McDonald, J.K., Parnavelas, J.G., Karamanlidis, A.N. & Brecha, N. (1982 b). The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. II. Vasoactive intestinal polypeptide. Journal of Neurocytology 11, 825–837.CrossRefGoogle ScholarPubMed
McDonald, J.K., Parnavelas, J.G., Karamanlidis, A.N. & Brecha, N. (1982 c). The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. III. Cholecystokinin. Journal of Neurocytology 11, 881–895.CrossRefGoogle ScholarPubMed
McDonald, J.K., Parnavelas, J.G., Karamanlidis, A.N. & Brecha, N. (1982 d). The morphology and distribution of peptide-contain-ing neurons in the adult and developing visual cortex of the rat. IV. Avian pancreatic polypeptide. Journal of Neurocytology 11, 985–995.CrossRefGoogle ScholarPubMed
McDonald, J.K., Tigges, J., Tigges, M. & Reich, C. (1988). Neuro-peptide Y-like immunoreactivity in the neurohypophysis and intermediate lobe of the rhesus monkey (Macaca mulatto). Cell and Tissue Research (in press).CrossRefGoogle Scholar
Mehra, R. & Hendrickson, A. (1987). Developmental studies of substance P and neuropeptide Y neurons in monkey visual cortex. Society for Neuroscience Abstracts 13, 358.Google Scholar
Movshon, J.A. & Van Sluyters, R.C. (1981). Visual neural development. Annual Review of Psychology 32, 477–522.CrossRefGoogle ScholarPubMed
Nakamura, S. & Vincent, S.R. (1986). Somatostatin- and neuropeptide Y-immunoreactive neurons in the neocortex in senile dementia of Alzheimer's type. Brain Research 370, 11–20.CrossRefGoogle ScholarPubMed
Noe, B.D., McDonald, J.K., Greiner, F., Wood, J.G. & Andrews, P.C. (1986). Anglerfish islets contain NPY immunoreactive nerves and produce the NPY analog aPY. Peptides 7, 147.CrossRefGoogle ScholarPubMed
Sabattno, F.D., Murnane, J.M., Hoffman, R.A. & McDonald, J.K. (1987). Distribution of neuropeptide Y-like immunoreactivity in the hypothalamus of the adult golden hamster. Journal of Comparative Neurology 257, 93–104.CrossRefGoogle Scholar
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738–855.CrossRefGoogle ScholarPubMed
Smith, Y., Parent, A., Kerkerian, L. & Pelletier, G. (1985). Distribution of neuropeptide Y immunoreactivity in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus). Journal of Comparative Neurology 236, 71–89.CrossRefGoogle ScholarPubMed
Sternberger, L.A. (1979). Immunocytochemistry, 2nd Edition. New York: John Wiley & Sons.Google ScholarPubMed
Tatemoto, K. (1982). Neuropeptide Y: complete amino-acid sequence of the brain peptide. Proceedings of the National Academy of Sciences of the U.S.A. 79, 5485–5489.CrossRefGoogle ScholarPubMed
Tatemoto, K., Carlquist, M. & Mutt, V. (1982). Neuropeptide Y— a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296, 659–660.CrossRefGoogle ScholarPubMed
Tigges, J., McDonald, J.K. & Tigges, M. (1987). Neuropeptide Y-like immunoreactivity in the hypothalamus of the young rhesus monkey (Macaca mulatto). Society for Neuroscience Abstracts 13, 1579.Google Scholar
Tigges, M., Hendrickson, A.E. & Tigges, J. (1984). Anatomical consequences of long-term monocular eyelid closure on lateral genic-ulate nucleus and striate cortex in squirrel monkey. Journal of Comparative Neurology 227, 1–13.CrossRefGoogle ScholarPubMed
Tigges, M. & Tigges, J. (1983). Cytochrome oxidase staining pattern in area 17: adult versus neonate monkeys. Investigative Ophthalmology and Visual Science (Suppl.) 24, 229.Google Scholar
Tigges, M., Tigges, J., Mcdonald, J.K., Fernandes, A., Gammon, J.A. & Slattery, M. (1987). Neuropeptide Y-like immunoreactivity in area 17 of normal and visually deprived infant rhesus monkeys. Investigative Ophthalmology and Visual Science (Suppl.) 28, 336.Google Scholar
Vincent, S.R., Johansson, O., HÖKfelt, T., Meyerson, B., Sachs, C, Elde, R.P., Terenius, L. & Kimmel, J. (1982). Neuropeptide coexistence in human cortical neurons. Nature 298, 65–67.CrossRefGoogle Scholar
Wahle, P. & Meyer, G. (1987). Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. Journal of Comparative Neurology 261, 165–192.CrossRefGoogle ScholarPubMed