Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T04:34:52.410Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

Chiye Aoki
Chiye Aoki
Affiliation:
Center for Neural Science and Biology, New York University, New York
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

SynaptogenesisUltrastructureImmunoelectron microscopyNorepinephrineNeuromodulationPresynaptic
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1129 - 1142
Copyright
Copyright © Cambridge University Press 1997

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

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, 1983–1987.CrossRefGoogle ScholarPubMed
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, 781–792.CrossRefGoogle ScholarPubMed
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, 35–49.CrossRefGoogle Scholar
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.Google Scholar
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, 109–116.CrossRefGoogle Scholar
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, 264–282.CrossRefGoogle ScholarPubMed
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, 331–347.CrossRefGoogle ScholarPubMed
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, 5202–5222.CrossRefGoogle ScholarPubMed
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, 501–519.CrossRefGoogle ScholarPubMed
Bear, M.F. & Singer, W. (1986). Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172–176.CrossRefGoogle ScholarPubMed
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, 684–688.CrossRefGoogle ScholarPubMed
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, 379–388.CrossRefGoogle ScholarPubMed
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, 599–616.CrossRefGoogle ScholarPubMed
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, 697–712.CrossRefGoogle ScholarPubMed
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, 370–373.CrossRefGoogle Scholar
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, 343–360.CrossRefGoogle ScholarPubMed
Chesselet, M.-F. (1984). Presynaptic regulation of neurotransmitter release in the brain. Neuroscience 12, 347–375.CrossRefGoogle ScholarPubMed
Coyle, J.T. & Molliver, M.E. (1977). Major innervation of newborn rat cortex by monoaminergic neurons. Science 196, 444–447.CrossRefGoogle ScholarPubMed
Cragg, B.G. (1975). The development of synapses in kitten visual cortex during visual deprivation. Experimental Neurology 46, 445–451.CrossRefGoogle ScholarPubMed
Descarries, L., Watkins, K.C. & Lapierre, Y. (1977). Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Research 133, 197–222.CrossRefGoogle ScholarPubMed
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, 75–79.CrossRefGoogle ScholarPubMed
Domenici, L., Parisi, V. & Maffei, L. (1992). Exogenous supply of nerve growth factor prevents the effects of strabismus in the rat. Neuroscience 51, 19–24.CrossRefGoogle ScholarPubMed
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, 709–720.CrossRefGoogle ScholarPubMed
Fink, K., Bönisch, H. & Göthert, M. (1990). Presynaptic NMDA receptors stimulate noradrenaline release in the cerebral cortex. European Journal of Pharmacology 185, 115–117.CrossRefGoogle ScholarPubMed
Goldman, J.E. & Abramson, B. (1990). Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Research 528, 189–196.CrossRefGoogle ScholarPubMed
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, 1851–1860.CrossRefGoogle ScholarPubMed
Gray, E.G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex. Journal of Anatomy 93, 420–433.Google ScholarPubMed
Hansson, E.A. (1992). Adrenergic receptor regulation of amino acid neurotransmitter uptake in astrocytes. Brain Research Bulletin 29, 297–301.CrossRefGoogle ScholarPubMed
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, 1791–1807.CrossRefGoogle ScholarPubMed
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, 312–332.Google Scholar
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, 123–148.CrossRefGoogle ScholarPubMed
Kasamatsu, T. (1991). Adrenergic regulation of visuocortical plasticity: A role of the locus coeruleus system. Progress in Brain Research 88, 599–616.CrossRefGoogle ScholarPubMed
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, 62–68.CrossRefGoogle ScholarPubMed
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, 171–174.CrossRefGoogle ScholarPubMed
Levitt, P. & Moore, R.Y. (1979). Development of the noradrenergic innervation of neocortex. Brain Research 162, 243–259.CrossRefGoogle ScholarPubMed
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, 73–82.CrossRefGoogle ScholarPubMed
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, 274–286.CrossRefGoogle ScholarPubMed
Madison, D.V. & Nicoll, R.A. (1986). Actions of noradrenalin recorded intracellularly in rat hippocampal CA1 pyramidal neurons, in vitro. Journal of Physiology 372, 221–244.CrossRefGoogle Scholar
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, 4651–4662.CrossRefGoogle ScholarPubMed
Molliver, M.E. & Kristt, D.A. (1975). The fine structural demonstration of monoaminergic synapses in immature rat neocortex. Neuroscience Letters 1, 305–310.CrossRefGoogle ScholarPubMed
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, 17–40.CrossRefGoogle ScholarPubMed
Müller, C.M. & Best, J. (1989). Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes. Nature 342, 427–430.CrossRefGoogle ScholarPubMed
Nakamura, S., Kimura, F. & Sakaguchi, T. (1987). Postnatal development of electrical activity in the locus coeruleus. Journal of Neurophysiology 58, 510–524.CrossRefGoogle Scholar
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, 271–280.CrossRefGoogle ScholarPubMed
Papadopoulos, G.C., Parnavelas, J.G. & Buijs, R.M. (1987). Monoaminergic fibers form conventional synapses in the cerebral cortex. Neuroscience Letters 7, 275–279.CrossRefGoogle Scholar
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, 1–10.CrossRefGoogle ScholarPubMed
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, 55–84.Google ScholarPubMed
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, 319–329.Google ScholarPubMed
Peters, A., Palay, S.L. & Webster, H. DeF. (1991). The Fine Structure of the Nervous System. New York: Oxford University Press.Google Scholar
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, 1585–1589.CrossRefGoogle Scholar
Rauschecker, J.P. (1991). Mechanisms of visual plasticity: Hebb synapses, NMDA receptors and beyond. Physiological Reviews 71, 587–615.CrossRefGoogle ScholarPubMed
Schliebs, R. & Godicke, C. (1988). Laminar distribution of noradrenergic markers in rat visual cortex. Neurochemistry International 13, 481–486.CrossRefGoogle ScholarPubMed
Schwartz, J.P. (1988). Stimulation of nerve growth factor mRNA content in C6 glioma cells by β-adrenergic receptor and cAMP. Glia 1, 282–285.CrossRefGoogle Scholar
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, 249–264.CrossRefGoogle ScholarPubMed
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, 693–699.CrossRefGoogle ScholarPubMed
Sternberger, L.A. (1986). lmmunocytochemistry, 3rd edition. New York: John Wiley.Google Scholar
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, 297–309.CrossRefGoogle ScholarPubMed
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, 4384–4388.CrossRefGoogle Scholar
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, 855–863.CrossRefGoogle Scholar
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, 79–95.3.0.CO;2-G>CrossRefGoogle Scholar
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, 5114–5118.CrossRefGoogle Scholar
Wang, J.K.T., Andrews, H. & Thukral, V. (1992). Presynaptic glutamate receptors regulate noradrenaline release from isolated nerve terminals. Journal of Neurochemistry 58, 204–211.CrossRefGoogle ScholarPubMed
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, 276–292.CrossRefGoogle ScholarPubMed
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, 349–352.CrossRefGoogle Scholar
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, 337–341.CrossRefGoogle ScholarPubMed
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, 333–339.CrossRefGoogle ScholarPubMed