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Differential timing for the appearance of neuronal and astrocytic β-adrenergic receptors in the developing rat visual cortex as revealed by light and electron-microscopic immunocytochemistry

  • Chiye Aoki (a1)

Abstract

The developing cerebral cortex is likely to exhibit synaptic circuitries differing from those in adulthood, due to the asynchronous maturation of the various neurotransmitter systems. Two antisera directed against mammalian β-adrenergic receptors (βAR), βAR248 and βAR404, were used to characterize the laminar, cellular, and subcellular distributions of βAR in postnatally developing visual cortex of rats. The antigenic sites were the receptor's third intracellular loop for βAR248 and the C-terminus for βAR404. During week 1, most of the βAR404- and βAR248-immunoreactive sites were dendritic. Morphologically identifiable synapses were rare, even in layer 1: yet, semiquantitative analysis revealed that βAR404-immunoreactive synapses comprise half of those in layer 1. During week 2, the two antisera began to diverge in their immunoreactivity patterns. With βAR248, there was an overall decline in immunoreactivity, while with βAR404, there was an increase in immunoreactive sites, primarily due to labeled astrocytic processes that increased 200-fold in areal density by week 3. In contrast, the areal density of synaptic labeling by βAR404 barely doubled, in spite of the 30-fold increase in areal density of synapses. These results suggest that βAR undergo conformational changes during early postnatal periods, causing alterations in their relative antigenicity to the two antisera. Furthermore, the first 2 weeks appear to be characterized by modulation of earliest-formed synapses, and the subsequent phase is marked by addition of astrocytic responses that would be more diffuse temporally and spatially. Activation of βAR is recognized to increase visually evoked activity relative to spontaneous activity. Moreover, astrocytic βAR are documented to regulate extracellular concentrations of glutamate, ATP, and neurotrophic factors important for the formation of binocular connections. Thus, neuronal and astrocytic responses may, together and in tandem, facilitate strengthening of intracortical synaptic circuitry during early life.

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Andrés, M.E., Bustos, G. & Gysling, K. (1993). Regulation of [3H]norepinephrine release by N-methyl-D-aspartate receptors in minislices from the dentate gyrus and the CA1-CA3 area of the rat hippocampus. Biochemical Pharmacology 46, 19831987.
Aoki, C. (1992). β-adrenergic receptors: Astrocytic localization in the adult visual cortex and their relation to catecholamine axon terminals as revealed by electron microscopic immunocytochemistry. Journal of Neuroscience 12, 781792.
Aoki, C. & Pickel, V.M. (1992). C-terminal tail of β-adrenergic receptors: Immunocytochemical localization within astrocytes and their relation to catecholaminergic neurons in N. tractus solitarii and area postrema. Brain Research 571, 3549.
Aoki, C. & Venkatesan, C. (1994). An antibody directed against the C-terminal tail of β-adrenergic receptor recognizes astrocytes in adult brain but neurons neonatally. Society for Neuroscience Abstracts 20, 877.
Aoki, C., Kaufman, D. & Rainbow, T.C. (1986). The ontogeny of the laminar distribution of β-adrenergic receptors in the visual cortex of cats, normally reared and visually deprived. Developmental Brain Research 27, 109116.
Aoki, C., Joh, T.H. & Pickel, V.M. (1987). Ultrastructural localization of β-adrenergic receptor-like immunoreactivity in the cortex and neostriatum of rat brain. Brain Research 437, 264282.
Aoki, C., Zemcik, B.A., Strader, C.D. & Pickel, V.M. (1989). Cytoplasmic loop of β-adrenergic receptors: Synaptic and intracellular localization and relation to catecholaminergic neurons in the nuclei of the solitary tracts. Brain Research 493, 331347.
Aoki, C., Venkatesan, C., Go, C.-G., Mong, J.A. & Dawson, T.M. (1994). Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. Journal of Neuroscience 14, 52025222.
Aston-Jones, G., Chiang, C. & Alexinsky, T. (1991). Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Progress in Brain Research 88, 501519.
Bear, M.F. & Singer, W. (1986). Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172176.
Berardi, N., Cellerino, A., Domenici, L., Fagiolini, M., Pizzorusso, T., Cattaneo, A. & Maffei, L. (1994). Monoclonal antibodies to nerve growth factor affect the postnatal development of the visual system. Proceedings of the National Academy of Sciences of the U.S.A. 91, 684688.
Bicknell, R.J., Luckman, S.M., Inenaga, K., Mason, W.T. & Hatton, G.I. (1989). Beta-adrenergic and opioid receptors on pituicytes cultured from adult rat neurohypophysis: Regulation of cell morphology. Brain Research Bulletin 22, 379388.
Blue, M.E. & Parnavelas, J.G. (1983 a). The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. Journal of Neurocytology 12, 599616.
Blue, M.E. & Parnavelas, J.G. (1983 b). The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. Journal of Neurocytology 12, 697712.
Bouvier, M., Hausdorff, W.P., De Blasi, A., O'Dowd, B.F., Kobilka, B.K., Caron, M.G. & Lefkowitz, R.J. (1988). Removal of phosphorylation sites from the β2-adrenergic receptor delays onset of agonist-promoted desensitization. Nature 333, 370373.
Carmignoto, G., Canella, R., Candeo, P, Comelli, M.C. & Maffei, L. (1993). Effects of nerve growth factor on neuronal plasticity of the kitten visual cortex. Journal of Physiology 464, 343360.
Chesselet, M.-F. (1984). Presynaptic regulation of neurotransmitter release in the brain. Neuroscience 12, 347375.
Coyle, J.T. & Molliver, M.E. (1977). Major innervation of newborn rat cortex by monoaminergic neurons. Science 196, 444447.
Cragg, B.G. (1975). The development of synapses in kitten visual cortex during visual deprivation. Experimental Neurology 46, 445451.
Descarries, L., Watkins, K.C. & Lapierre, Y. (1977). Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Research 133, 197222.
Dixon, R.A., Kobilka, B.K., Strader, D.J., Benovic, J.L., Dohlman, H.G., Frielle, T., Bolanowski, M.A., Bennett, C.D., Rands, E., Diehl, R.E., Mumford, R.A., Slater, E.E., Sigal, I.S., Caron, M.G., Lefkowitz, R.J. & Strader, C.D. (1986). Cloning of the gene and cDNA for mammalian β-adrenergic receptor and homology with rhodopsin. Nature 321, 7579.
Domenici, L., Parisi, V. & Maffei, L. (1992). Exogenous supply of nerve growth factor prevents the effects of strabismus in the rat. Neuroscience 51, 1924.
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. (1994). Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular deprivation. Vision Research 34, 709720.
Fink, K., Bönisch, H. & Göthert, M. (1990). Presynaptic NMDA receptors stimulate noradrenaline release in the cerebral cortex. European Journal of Pharmacology 185, 115117.
Goldman, J.E. & Abramson, B. (1990). Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Research 528, 189196.
Gordon, B., Mitchell, B., Mohtadi, K., Roth, E., Tseng, Y. & Turk, F. (1990). Lesion of nonvisual inputs affect plasticity, norepinephrine content, and acetylcholine content of visual cortex. Journal of Neurophysiology 64, 18511860.
Gray, E.G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex. Journal of Anatomy 93, 420433.
Hansson, E.A. (1992). Adrenergic receptor regulation of amino acid neurotransmitter uptake in astrocytes. Brain Research Bulletin 29, 297301.
Horton, J.C. & Hocking, D.R. (1996). An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. Journal of Neuroscience 16, 17911807.
Hsu, S.M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 21, 312332.
Kageyama, G.H. & Robertson, R.T. (1993). Development of geniculocortical projections to visual cortex in rat: Evidence for early ingrowth and synaptogenesis. Journal of Comparative Neurology 335, 123148.
Kasamatsu, T. (1991). Adrenergic regulation of visuocortical plasticity: A role of the locus coeruleus system. Progress in Brain Research 88, 599616.
King, J.C., Lechan, R.M., Kuigel, G. & Anthony, E.L.P. (1983). Acrolein: A fixative for immunocytochemical localization of peptides in the central nervous system. Journal of Histochemistry and Cytochemistry 31, 6268.
Lehmann, J., Valentino, R. & Robine, V. (1992). Cortical norepinephrine release elicited in situ by N-methyl-D-aspartate (NMDA) receptor stimulation: A microdialysis study. Brain Research 599, 171174.
Levitt, P. & Moore, R.Y. (1979). Development of the noradrenergic innervation of neocortex. Brain Research 162, 243259.
Ling, E.A. & Leblond, C.P. (1973). Investigation of glial cells in semithin sections. II. Variations with age in the numbers of the various glial cell types in rat cortex and corpus callosum. Journal of Comparative Neurology 149, 7382.
Liu, Y., Jia, W., Strosberg, A.D. & Cynader, M. (1993). Development and regulation of β-adrenergic receptors in kitten visual cortex: An immunocytochemical and autoradiographic study. Brain Research 632, 274286.
Madison, D.V. & Nicoll, R.A. (1986). Actions of noradrenalin recorded intracellularly in rat hippocampal CA1 pyramidal neurons, in vitro. Journal of Physiology 372, 221244.
Maffei, L., Berardi, N., Domenici, L., Parisi, V. & Pizzorusso, T. (1992). Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. Journal of Neuroscience 12, 46514662.
Molliver, M.E. & Kristt, D.A. (1975). The fine structural demonstration of monoaminergic synapses in immature rat neocortex. Neuroscience Letters 1, 305310.
Morrison, J.H., Grzanna, R., Molliver, M.E. & Coyle, J.T. (1978). The distribution and orientation of noradrenergic fibers in neocortex of the rat: An immunofluorescence study. Journal of Comparative Neurology 181, 1740.
Müller, C.M. & Best, J. (1989). Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes. Nature 342, 427430.
Nakamura, S., Kimura, F. & Sakaguchi, T. (1987). Postnatal development of electrical activity in the locus coeruleus. Journal of Neurophysiology 58, 510524.
Olschowka, J.A., Molliver, M.E., Grzanna, R., Rice, F.L. & Coyle, J.T. (1981). Ultrastructural demonstration of noradrenergic synapses in the rat central nervous system by dopamine-beta-hydroxylase immunocytochemistry. Journal of Histochemistry and Cytochemistry 29, 271280.
Papadopoulos, G.C., Parnavelas, J.G. & Buijs, R.M. (1987). Monoaminergic fibers form conventional synapses in the cerebral cortex. Neuroscience Letters 7, 275279.
Papadopoulos, G.C., Parnavelas, J.G. & Buijs, R.M. (1989). Light and electron microscopic immunocytochemical analysis of the noradrenaline innervation of the rat visual cortex. Journal of Neurocytology 18, 110.
Parnavelas, J.G., Luder, R., Pollard, S.G., Sullivan, K. & Lieberman, A.R. (1983). A qualitative and quantitative ultrastructural study of glial cells in the developing visual cortex of the rat. Philosophical Transactions of the Royal Society B (London) 301, 5584.
Parnavelas, J.G., Moises, H.C. & Speciale, S.G. (1985). The monoaminergic innervation of the rat visual cortex. Proceedings of the Royal Society B (London) 223, 319329.
Peters, A., Palay, S.L. & Webster, H. DeF. (1991). The Fine Structure of the Nervous System. New York: Oxford University Press.
Rainbow, T.C., Parsons, B. & Wolfe, B.B. (1984). Quantitative autoradiography of beta 1- and beta2-adrenergic receptors in rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 81, 15851589.
Rauschecker, J.P. (1991). Mechanisms of visual plasticity: Hebb synapses, NMDA receptors and beyond. Physiological Reviews 71, 587615.
Schliebs, R. & Godicke, C. (1988). Laminar distribution of noradrenergic markers in rat visual cortex. Neurochemistry International 13, 481486.
Schwartz, J.P. (1988). Stimulation of nerve growth factor mRNA content in C6 glioma cells by β-adrenergic receptor and cAMP. Glia 1, 282285.
Séguéla, P., Watkins, K.C., Geffard, M. & Descarries, L. (1990). Noradrenaline axon terminals in adult rat neocortex: An immunocytochemical analysis in serial thin sections. Neuroscience 35, 249264.
Smithson, K.G., Suarez, I. & Hatton, G.I. (1990). β-adrenergic stimulation decreases glial and increases neural contact with the basal lamina in rat neurointermediate lobes incubated in vitro. Journal of Neuroendocrinology 2, 693699.
Sternberger, L.A. (1986). lmmunocytochemistry, 3rd edition. New York: John Wiley.
Stone, E.A. & Ariano, M.A. (1989). Are glial cells targets of the central noradrenergic system? A review of the evidence. Brain Research Reviews 14, 297309.
Strader, C.D., Sigal, I.S., Register, R.B., Candelore, M.R., Rands, E. & Dixon, R.A.F. (1987 a). Identification of residues required for ligand binding to the β-adrenergic receptor. Proceedings of the National Academy of Sciences of the U.S.A. 84, 43844388.
Strader, C.D., Sigal, I.S., Blake, A.D., Cheung, A.H., Register, B.S., Rands, E., Zemcik, B.A., Candelore, M.R. & Dixon, R.A.F. (1987 b). The carboxyl terminus of the hamster β-adrenergic receptor expressed in mouse L cells is not required for receptor sequestration. Cell 49, 855863.
Venkatesan, C., Song, X-A., Go, C.-G., Kurose, H. & Aoki, C. (1996). Cellular and subcellular distribution of α2A-adrenergic receptors in the visual cortex of neonatal and adult rats. Journal of Comparative Neurology 365, 7995.
Vos, P, Kaufmann, D., Hand, P.J. & Wolfe, B.B. (1990). β2-adrenergic receptors are colocalized and coregulated with "whisker barrels" in rat somatosensory cortex. Proceedings of the National Academy of Sciences of the U.S.A. 87, 51145118.
Wang, J.K.T., Andrews, H. & Thukral, V. (1992). Presynaptic glutamate receptors regulate noradrenaline release from isolated nerve terminals. Journal of Neurochemistry 58, 204211.
Waterhouse, B.D., Azizi, S.A., Burne, R.A. & Woodward, D.J. (1990). Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin microiontophoresis. Brain Research 514, 276292.
Wilkinson, M., Shaw, C., Khan, I. & Cynader, M. (1983). Ontogenesis of β-adrenergic binding sites in kitten visual cortex and the effects of visual deprivation. Developmental Brain Research 7, 349352.
Yu, S.S., Lefkowitz, R.J. & Hausdorff, W.P. (1993). β-Adrenergic receptor sequestration: A potential mechanism of receptor resensitization. Journal of Biological Chemistry 268, 337341.
Zemcik, B.A. & Strader, C.D. (1988). Fluorescent localization of the β-adrenergic receptor on DDT-1 cells: Down-regulation by adrenergic agonists. Biochemical Journal 251, 333339.

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