Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-16T05:21:35.177Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification and localization of 5-hydroxytryptamine receptor sites in macaque visual cortex

Published online by Cambridge University Press:  02 June 2009

David Parkinson ,
Elizabeth C. Coscia  and
Nigel W. Daw
David Parkinson
Affiliation:
Department of Cell Biology and Physiology and McDonnell Center for Higher Brain Function, Washington University Medical School, St. Louis
Elizabeth C. Coscia
Affiliation:
Department of Cell Biology and Physiology and McDonnell Center for Higher Brain Function, Washington University Medical School, St. Louis
Nigel W. Daw
Affiliation:
Department of Cell Biology and Physiology and McDonnell Center for Higher Brain Function, Washington University Medical School, St. Louis
Get access Rights & Permissions [Opens in a new window]

Abstract

The two main receptor subtypes for 5-hydroxytryptamine (5HT) were measured and localized in visual cortical areas of macaque monkey. [3H]5HT was used to label all 5HT-1 receptor subtypes and [3H]ketanserin was used to label 5HT-2 receptors. Both receptor types could be demonstrated in membranes prepared from macaque primary visual cortex. The specificity of these ligands for 5HT-1 or 5HT-2 receptors was demonstrated by the pharmacological profile of inhibitors of the specific binding. 5HT-1A receptor sites were detected by displacement experiments and by direct labeling with [3H]8-hydroxy-2(di-n-propylamino) tetralin 8OH-DPAT. Receptor autoradiography showed that the distribution of these receptor subtypes varied from one part of visual cortex to another. 5HT-1 receptors, labeled with [3H]5HT were present in several bands through layer IV of primary visual cortex with the densest band seen in and above layer IVA: another band was in lower layer VI. The band in layer VI was predominantly 5HT-1A sites. There were two main bands of 5HT-2 receptor sites, the most prominent around the IV/V boundary, and the other extending from layer IVA upwards. Adjacent areas showed 5HT receptors in a broad band corresponding to layer IV. 5HT-1A sites were found in superficial layers of adjacent areas, except V2. These layering patterns did not correspond precisely with cytoarchitectonic layering, nor with the pattern of 5HT-containing presynaptic fibres in published reports. It is important, therefore, in considering the role of the 5HT-containing neurons in cortical function to take account not only of the anatomy of the presynaptic terminals, but also of the postsynaptic receptors upon which the released transmitter will act, and their location within the cortex.

Keywords

5-hydroxytryptamineVisual cortexMacaque monkeyReceptor autoradiography
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 5 , May 1989 , pp. 515 - 525
Copyright
Copyright © Cambridge University Press 1989

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

Andrade, R., Malenka, R.C. & Nicholl, R.A. (1986). A G protein couples serotonin and GABA-β receptors to the same channels in hippocampus. Science 234, 1261–1265.Google Scholar
Bremer, M.E. & Middlemiss, D.N. (1987). K+-evoked release of [3H]5HT from the guinea pig frontal cortex. Society for Neuroscience Abstracts 13, 345.Google Scholar
Conn, P.J. & Sanders-Bush, E. (1985). Serotonin-stimulated phosphoinositide turnover: mediation by the S2 binding site in rat cerebral cortex but not in subcortical regions. Journal of Pharmacology and Experimental Therapeutics 234, 195–203.Google Scholar
Draper, N.R. & Smith, H. (1981). Applied Regression Analysis. New York: John Wiley & Sons.Google Scholar
Engel, G., Gothert, M., Hoyer, D., Schucker, E. & Hillenbrand, K. (1986). Identity of inhibitory presynaptic 5-hydroxytryptamine (5HT) autoreceptors in the rat brain cortex with 5-HT1B binding sites. Naunyn-Schmiedeberg's Archives of Pharmacology 332, 1–7.Google Scholar
Foote, S.L. & Morrison, J.H. (1987). Extrathalamic modulation of cortical function. Annual Reviews of Neuroscience 10, 67–95.Google Scholar
Gozlan, H., El Mestikawy, S., Pichat, L., Glowinski, J. & Hamon, M. (1983). Identification of presynaptic serotonin autoreceptors using a new ligand: 3H-PAT. Nature 305, 140–142.Google Scholar
Heuring, R.E., Schlegel, J.R. & Peroutka, S.J. (1986). Species variations in RU 24969 interactions with non-5-HT1A binding sites. European Journal of Pharmacology 122, 279–282.Google Scholar
Heuring, R.E. & Peroutka, S.J. (1987). Characterization of a novel 3H-5-hydroxytryptamine binding site subtype in bovine brain membranes. Journal of Neuroscience 7, 894–903.Google Scholar
Hoyer, D., Engel, G. & Kalkman, H.O. (1985). Characterization of the 5-HT1B recognition site in rat brain: binding studies with (-)[123I]iodocyanopindolol. European Journal of Pharmacology 118, 1–12.Google Scholar
Hoyer, D., Pazos, A., Probst, A. & Palacios, J.M. (1986). Serotonin receptors in the human brain. I. Characterization and autoradiographic localization of 5-HT1A recognition sites. Apparent absence of 5-HT1B sites. Brain Research 376, 85–96.Google Scholar
Jones, R.S.G. (1982). Responses of cortical neurons to stimulation of the nucleus raphe medianus: a pharmacological analysis of the role of indoleamines. Neuropharmacology 21, 511–520.Google Scholar
Kanba, S. & Richelson, E. (1984). Histamine H1 receptors in human brain with [3H]doxepin. Brain Research 304 1–7.Google 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 cynomolgous monkey (Macaca fascicularis). Journal of Comparative Neurology 230, 168–178.Google Scholar
Leysen, J.E., Awoutens, F., Kennis, L., Laduron, P.M., Vandenberk, J. & Janssen, P.A.J. (1981). Receptor binding profile of R41 468. A novel antagonist at 5HT-2 receptors. Life Science 28, 1015–1022.Google Scholar
Leysen, J.E., Niemegeers, C.J.E., Van Neuten, J.M. & Laduron, P.M. (1982). [3H]ketanserin (R 41 468), a selective 3H-ligand for serotonin2 receptor binding sites. Molecular Pharmacology 21, 301–314.Google Scholar
Leysen, J.E., De Chaffoy de Courcelles, D., De Clerck, F., Niemegeers, C.J.E. & Van Neuten, J.M. (1984). Serotonin-S2 receptor binding sites and functional correlates. Neuropharmacology 23, 1493–1501.Google Scholar
Limberger, N., Bonanno, G., Spath, L. & Starke, K. (1986). Autoreceptors and α2-adrenoceptors at the serotonergic axons of rabbit brain cortex. Naunyn-Schmiedeberg's Archives of Pharmacology 332, 324–331.CrossRefGoogle Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.Google Scholar
Lum, J.T. & Piercey, M.F. (1988). Electrophysiological evidence that spiperone is an antagonist of 5HT-1A receptors in the dorsal raphenucleus. European Journal of Pharmacology 149, 9–15.Google Scholar
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Afacaca mulatto). Journal of Comparative Neurology 147, 455–496.Google Scholar
McPherson, G.A. (1985). Analysis of radioligand binding experiments. Journal of Pharmacological Methods 14, 213–228.Google Scholar
Miach, P.J., Dausse, J., Cardot, A. & Meye, P. (1980). [3-H]prazosin binds specifically to α-adrenoceptors in rat brain. Naunyn-Schmiedeberg's Archives of Pharmacology 312, 23–26.Google Scholar
Middlemiss, D.N. (1984). 8-hydroxy-2-(di-n-propylamino)tetralin is devoid of activity at the 5-hydroxytryptamine autoreceptor in rat brain. Implication for the proposed link between the autoreceptor and the [3H]5HT recognition site. Naunyn-Schmiedeberg's Archives of Pharmacology 327, 18–26.Google Scholar
Molliver, M.E. (1987). Serotonergic neuronal systems: what their anatomic organization tells us about function. Journal of Clinical Psychopharmacology 7, 3S–23S.Google Scholar
Munson, P.J. & Rodbard, D. (1980). Ligand: a versatile computerized approach for characterization of ligand-binding systems. Analytical Biochemistry 107, 220–239.Google Scholar
Orban, G.A. (1984). Neuronal Operations in the Visual Cortex. New York: Springer-Verlag.Google Scholar
Parkinson, D. & Callingham, B.A. (1979). Substrate and inhibitor selectivity of human heart monoamine oxidase. Biochemical Pharmacology 28, 1639–1643.Google Scholar
Pazos, A., Hoyer, D. & Palacios, J.M. (1984). The binding of serotonergic ligands to the porcine choroid plexus: characterization of a new type of serotonin recognition site. European Journal of Pharmacology 106, 539–546.CrossRefGoogle Scholar
Pedigo, N.W., Yamamura, H.I. & Nelson, D.L. (1981). Discrimination of multiple [3H]5-hydroxytryptamine sites by the neuroleptic spiperone in rat brain. Journal of Neurochemistry 36, 220–226.Google Scholar
Peroutka, S.J. (1987). 5-hydroxytryptamine receptor subtypes. Annual Reviews of Neuroscience 11, 45–60.Google Scholar
Peroutka, S.J. (1985). Selective labeling of 5-HT1A and 5-HT1B binding sites in bovine brain. Brain Research 344, 167–171.Google Scholar
Peroutka, S.J., Ison, P.J., Liu, D.U. & Barrett, R.W. (1986). Artifactual high-affinity and saturable binding of [3H]5-hydroxytryptamine induced by radioligand oxidation. Journal of Neurochemistry 47, 38–45.Google Scholar
Roberts, M.H.T. & Straughan, D.W. (1967). Excitation and depression of cortical neurons by 5-hydroxytryptamine. Journal of Physiology (London) 193, 264–294.Google Scholar
Sastry, B.S.R. & Phillis, J.W. (1977 a). Metergoline as a selective 5-hydroxytryptamine antagonist in the cerebral cortex. Canadian Journal of Physiology and Pharmacology 55, 130–133.Google Scholar
Sastry, B.S.R. & Phillis, J.W. (1977 b). Inhibition of cerebral cortical neurons by a 5-hydroxytryptaminergic pathway from median raphe nucleus. Canadian Journal of Physiology and Pharmacology 55, 737–743.Google Scholar
Schipper, J., van der Heyden, J.A.M. & Olivier, B. (1987). Species differences in serotonin autoreceptors. Society for Neuroscience Abstracts 13, 345.Google Scholar
Schlicker, E., Gothert, M. & Hillenbrand, K. (1985). Cyanopindolol is a highly potent and selective antagonist at the presynaptic serotonin autoreceptor in the rat brain cortex. Naunyn-Schmiedeberg's Archives of Pharmacology 331, 398–401.Google Scholar
Schnellman, R.G., Waters, J.J. & Nelson, S.J. (1984). [3H]5-hydroxytryptamine binding sites: species and tissue variation. Journal of Neurochemistry 42, 65–70.Google Scholar
Sills, M.A., Wolfe, B.B. & Frazer, A. (1984). Multiple states of the 5-hydroxytryptamine receptor as indicated by the effect of GTP on [3H]5-hydroxytryptamine binding in rat frontal cortex. Molecular Pharmacology 26, 10–18.Google Scholar
Sprouse, J.S. & Aghajanian, G.K. (1987). Electrophysiological responses of serotonergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1, 3–9Google Scholar
Takeuchi, Y. & Sano, Y. (1984). Serotonin nerve fibers in the primary visual cortex of the monkey. Anatomical Embryology 169, 1–8.Google Scholar
Toga, A.W., Goo, R.L., Murphy, R. & Collins, R.C. (1984). A neuroscience application of interactive image analysis. Optical Engineering 23, 279–282.Google Scholar
Tricklebank, M.D., Forler, C. & Fozard, J.R. (1985). The involvement of subtypes of the 5HT-1 receptor and of catecholaminergic systems in the behavioral response to 8-hydroxy-2-(di-n-propylamino)-tetralin in the rat. European Journal of Pharmacology 106, 271–282.Google Scholar
Van Essen, D.C. (1983). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3, ed. Peters, A. & Jones, E.G., pp. 259–329. New York: Plenum Press.Google Scholar