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Columnar activity regulates astrocytic β-adrenergic receptor-like immunoreactivity in V1 of adult monkeys

Published online by Cambridge University Press:  02 June 2009

Chiye Aoki ,
Mona Lubin  and
Suzanne Fenstemaker
Chiye Aoki
Affiliation:
Center for Neural Science, New York University, New York Center for Neural Scienc and Biology Dept., New York University, New York
Mona Lubin
Affiliation:
Center for Neural Science, New York University, New York
Suzanne Fenstemaker
Affiliation:
Center for Neural Science, New York University, New York
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Abstract

Recent results indicate that astrocytic β-adrenergic receptors (βAR) participate in noradrenergic modulation of synaptic activity. In this study, we sought to examine whether neural activity can, in turn, regulate astrocytic βAR. To address this question, an antiserum that recognizes β-adrenergic receptors (βAR) specifically in astrocytes was used to assess the distribution of the receptors across ocular dominance columns in VI of two monocular and four visually intact adult monkeys. Cytochrome oxidase histochemistry (CO) was used to identify the position of the cortical laminae and of the ocular dominance columns receiving visual inputs from the intact and enucleated eyes. This stain revealed the expected pattern within V1 of monocular monkeys–i.e. darker and lighter bands of equal widths (ca. 500μm) spanning laminae 4–6, each associated with larger and smaller blobs, respectively, in lamina 2/3;. Alignment of CO sections with adjacent sections stained for astrocytic βAR by the immunoperoxidase method revealed intense βAR-like immunoreactivity (βAR-li) in the superficial laminae, a slightly weaker staining in the infragranular laminae and weakest staining in lamina 4C. Within lamina 4C., a prominent striped pattern was evident. The darker bands of the stripe closely matched widths and positions of the lighter CO columns associated with the enucleated eye. On the other hand, immunocytochemical staining for the astrocytic intermediate filament protein, GFAP, within V1 of monocular monkeys revealed no inter-columnar difference in the density of astrocytic cell bodies or processes. Nissl stain also revealed no overt inter-columnar differences in cell density. V1 of visually intact monkeys exhibited a similar laminar distribution pattern of βAR-li and of CO. Within lamina 4C., βAR-li was uniformly faint and CO staining was uniformly intense. This suggests that the striped pattern of βAR-li seen in lamina 4C of monocular monkeys results from elevation of the βAR-antigen within the inactive columns. The results indicate that astrocytic βAR density is regulated by local neural activity. The mechanisms regulating βAR density are likely to be independent of those regulating glial cell proliferation or GFAP synthesis. In vitro experimental results of others suggest that elevation of astrocytic βAR may be a mechanism compensating for chronic neural inactivity, since the coincident release of noradrenaline with visual stimulation would elevate neuropil excitability via the astrocytic mechanism of (1) decreasing the uptake of neuronally released L-glutamate; (2) increasing GABA uptake; and (3) stimulating glycogenolysis. Alternatively, the changes in βAR-li may reflect an up-regulation of the receptors within inactive columns due to reduced levels of noradrenaline release.

Keywords

AstrocytesCatecholamine receptorsActivity-dependent regulationMonocular deprivationV1
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 179 - 187
Copyright
Copyright © Cambridge University Press 1994

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References

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.Google Scholar
Aoki, C. (1992). C-terminal fragment of β-adrenergic receptors: Astrocytic localization in the visual cortex and their relation to catecholamine axon terminals. Journal of Neuroscience 12, 781–792.Google Scholar
Aoki, C. & Pickel, V.M. (1992 a). C-terminal tail of β-adrenergic receptors: Immunocytochemical localization within astrocytes and their relation to catecholaminergic neurons in tractus solitarii and area postrema. Brain Research 571, 35–49.Google Scholar
Aoki, C. & Pickel, V.M. (1992 b). Ultrastructural relations between β-adrenergic receptors and catecholaminergic neurons. Brain Research Bulletin 29, 257–263.CrossRefGoogle ScholarPubMed
Aronin, N. & DiFiglia, M. (1992). The subcellular localization of the G-protein Gjα in the basal ganglia reveals its potential role in both signal transduction and vesicle trafficking. Journal of Neuroscience 12, 3435–3444.Google Scholar
Barres, B.A., Chun, L.L.Y. & Corey, D.P.A. (1990). Ion channels in vertebrate glia. Annual Review of Neuroscience 13, 441–474.Google Scholar
Bicknell, R.J., Luckman, S.M., Inenaga, K. & Mason, W.T. (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
Burgess, S.K. & McCarthy, K.D. (1985). Autoradiographic quantitation of beta-adrenergic receptors on neural cells in primary cultures. I. Pharmacological studies of [125I]pindolol binding of individual astroglial cells. Brain Research 335, 1–9.Google Scholar
Chesselet, M.-F. (1984). Presynaptic regulation of neurotransmitter release in the brain: Facts and hypothesis. Neuroscience 12, 347–375.CrossRefGoogle ScholarPubMed
Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S. & Smith, S.J. (1990). Glutamate induces calcium waves in cultured astrocytes: Long-range glial signaling. Science 247, 470–473.CrossRefGoogle ScholarPubMed
Descarries, L., Seguela, P. & Watkins, K.C. (1991). Nonjunctional relationships of monoamine axon terminals in the cerebral cortex of adult rat. In Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission, ed. Fuxe, K. & Agnati, L.F., pp. 53–62. New York: Raven Press.Google Scholar
Fedoroff, S. & Vernadakis, A. (1986). Astrocytes, Vol. 1: Development, Morphology, and Regional Specialization of Astrocytes. New York: Academic Press.Google Scholar
Foote, S.L. & Morrison, J.H. (1987). Extrathalamic modulation of cortical function. Annual Review of Neuroscience 10, 67–95.Google Scholar
Hansson, E. (1988). Astroglia from defined brain regions as studied with primary cultures. Progress in Neurobiology 30, 369–397.Google Scholar
Hansson, E. (1990). Regional heterogeneity among astrocytes in the central nervous system. Neurochemistry International 16, 237–245.Google Scholar
Hansson, E. & Ronnback, L. (1992). Adrenergic receptor regulation of amino acid neurotransmitter uptake in astrocytes. Brain Research Bulletin 29, 297–302.Google Scholar
Harley, C. (1991). Noradrenergic and locus coeruleus modulation of the perforant path-evoked potential in rat dentate gyrus supports a role for the locus coeruleus in attentional and memorial process. Progress in Brain Research 88, 307–322.CrossRefGoogle Scholar
Hatton, G.I., Permutter, L.S., Salm, A.K. & Tweedle, C.D. (1984). Dynamic neuronal-glial interactions in hypothalamus and pituitary: Implications for control of hormone synthesis and release. Peptides 5, 121–138.Google Scholar
Hatton, G.I., Luckman, S.M. & Bicknell, R.J. (1991). Adrenaline activation of beta-2-adrenoceptors stimulates morphological changes in astrocytes (pituicytes) cultured from adult rat neurohypophysis. Brain Research Bulletin 26, 765–769.CrossRefGoogle Scholar
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of immunostained GABAergic neurons in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753.CrossRefGoogle Scholar
Hendry, S.H.C. & Jones, E.G. (1988). Activity dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron 1, 701–712.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Jones, E.G. & Burstein, N. (1988). Activity-dependent regulation of tachykinin-like immunoreactivity in neurons of monkey visual cortex. Journal of Neuroscience 8, 1225–1238.Google Scholar
Hevner, R.F. & Wong-Rtley, M.T.T. (1990). Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. Journal of Neuroscience 10, 1331–1340.CrossRefGoogle ScholarPubMed
Hopkins, W.F. & Johnston, D. (1984). Frequency-dependent norad renergic modulation of long-term potentiation in the hippocampus. Science 226, 350–351.CrossRefGoogle Scholar
Hsu, S.M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin-per-oxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577–580.Google Scholar
Jones, E.G. (1984). Neurogliaform or spiderweb cells. In Cerebral Cortex, Vol. 1: Cellular Components of the Cerebral Cortex, ed. Peters, A. & Jones, E.G., pp. 409–418. New York: Plenum Press.CrossRefGoogle Scholar
Kettenmann, H., Backus, K.H. & Schachner, M. (1987). γ-amino-butyric acid opens Cl-channels in cultured astrocytes. Brain Research 404, 1–9.Google Scholar
Kimelberg, H.K. (1986). Catecholamine and serotonin uptake in astrocytes. In Astrocytes, Vol. 2: Biochemistry, Physiology and Pharmacology of Astrocytes, ed. Fedoroff, S. & Vernadakis, A., pp. 107–131. New York: Academic Press.Google Scholar
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 Histochemical Cytochemistry 31, 62–68.Google Scholar
Kuffler, S.W. & Nicholls, J.G. (1966). The physiology of neuroglial cells. Ergeb. physiol. 57, 1–90.Google Scholar
MacVicar, B.A., Tse, F.W.Y., Crichton, S.A. & Kettenmann, H. (1989). GABA-activated Cl− channels in astrocytes of hippocampal slices. Journal of Neuroscience 9, 3577–3583.Google Scholar
McCormick, D.A., Pare, H.-C. & Williamson, A. (1991). Actions of norepinephrine in the cerebral cortex and thalamus: Implications for function of the central noradrenergic system. Progress in Brain Research 88, 293–321.Google Scholar
Narumi, S., Kimelberg, H.K. & Bourke, R.L. (1978). Effects of norepinephrine on the morphology and some enzyme activities of primary monolayer cultures from rat brain. Journal of Neurochemistry 31, 1479–1480.Google Scholar
Neuman, R.S. & Harley, C.W. (1983). Long-lasting potentiation of the dentate gyrus population spike by norepinephrine. Brain Research 273, 162–165.Google Scholar
Palay, S.L. (1991). The meaning of synaptic architecture. In Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission, ed. Fuxe, K. & Agnati, L.F., pp. 49–52, New York: Raven Press.Google Scholar
Peters, A., Palay, S.L. & Webster, H.D. (1991). The Fine Structure of the Nervous System, 3rd edition. New York: Oxford Press.Google Scholar
Quach, T.T., Rose, C. & Schwartz, J.C. (1988). [3H]glycogen hydrolysis in brain slices: Responses to neurotransmitters and modulation of noradrenaline receptors. Journal of Neurochemistry 30, 1335–1341.Google Scholar
Salm, A.K. & McCarthy, K.D. (1992). The evidence for astrocytes as target for central noradrenergic activity: Expression of adrenergic receptors. Brain Research Bulletin 29, 265–276.Google Scholar
Segal, M., Markram, H. & Richter-Levtn, G. (1991). Actions of norepinephrine in the rat hippocampus. Progress in Brain Research 88, 323–341.Google Scholar
Seguela, 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
Stanton, P.K. & Sarvey, J.W. (1985). Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. Journal of Neuroscience 5, 2169–2176.CrossRefGoogle 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.Google Scholar
Strader, C.D., Sigal, I.S., Blake, A.D., Cheung, A.H., Register, B.S., Rands, E., Zemck, B.A., Candelore, M.R. & Dlxon, R.A.F. (1987 a). The carboxyl termnus of the hamster beta-adrenergic receptor expressed in mouse L cells is not required for receptor deques-tration. Cell 49, 855–863.Google Scholar
Strader, C.D., Sigal, I.S., Register, R.B., Candelore, M.R., Rands, E. & Dlxon, R.A.F. (1987 b). 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.Google Scholar
Sutin, J. & Shao, Y. (1992). Resting and reactive astrocytes express adrenergic receptors in the adult rat brain. Brain Research Bulletin 29, 277–284.Google Scholar
Tsumoto, T. (1990). Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral neocortex. Neuroscience Research 9, 79–102.Google Scholar
Tweedle, C.D. & Hatton, G.I. (1980). Evidence for dynamic interactions between pituicytes and neurosecretory axons in the rat. Neuroscience 5, 661–667.Google Scholar
Vaughn, D. W. (1984). The structure of neuroglial cells. In Cerebral Cortex, Vol. 2: Functional Properties of Cortical Cells, ed. Jones, E.G., & Peters, A., pp. 285–329. New York: Plenum Press.Google Scholar
Wong-Riley, M.T.T. (1979). Changes in the visual system of monocu-larly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.Google Scholar