Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-30T20:36:46.102Z Has data issue: false hasContentIssue false

Effects of angiotensin II on visual neurons in the superficial laminae of the hamster's superior colliculus

Published online by Cambridge University Press:  02 June 2009

Richard D. Mooney
Affiliation:
Department of Anatomy, Medical College of Ohio, Toledo
Yi Zhang
Affiliation:
Department of Anatomy, Medical College of Ohio, Toledo
Robert W. Rhoades
Affiliation:
Department of Anatomy, Medical College of Ohio, Toledo

Abstract

Superficial layer superior colliculus (SC) neurons were recorded extracellularly with multibarreled recording/ejecting micropipettes. Angiotensin II was delivered via micropressure ejection during visual stimulation (n = 215 cells), or during electrical stimulation of either the optic chiasm (OX; n = 150 cells) or visual cortex (CTX; n = 42 cells). Application of angiotensin II decreased visual responses of SC cells to 43.8% ± 30.7% (mean ± S.D.) and reduced responses to electrical stimulation of the OX and CTX to 58.6% ± 34.1% and 43.8% ± 30.7% of control values, respectively. Angiotensin II enhanced responses by at least 30% in only 6 cells (1.5%). Of the 35 neurons tested with both OX and CTX stimulation, the correlation of evoked response suppression by angiotensin II was highly significant (r = 0.69; P < 0.001). This suggests that the suppressive effects of angiotensin II were common to both pathways. To test whether the inhibitory effects of angiotensin II were presynaptic or postsynaptic, Mg2+ ions were ejected iontophoretically to abolish synaptic responses, and the neurons were activated by iontophoresis of glutamate and then tested with angiotensin II. Angiotensin II reduced the glutamate-evoked responses to an average 29.1% ± 21.1% of control values (n = 9 cells). This suggests that the site of action of angiotensin II is most likely postsynaptic. To identify which receptors were involved in these effects, angiotensin II was ejected concurrently with the AT1 antagonist Losartan (DUP753) or with either of two AT2 antagonists, CGP42112A or PD123177. Losartan antagonized the action of angiotensin II in 65.6% of the cells tested (n = 99) and CGP42112A and PD123177 had antagonistic effects in 58% (n = 65) and 60% (n = 5), respectively. Both classes of antagonists were tested in 29 cells; and there was no significant correlation between their effectiveness. These results suggest that both AT1, and AT2 receptors may independently mediate the suppressive effects of angiotensin II, and that collicular neurons may have either or both receptor subtypes.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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

Aguirre, J.A., Covnas, R., Croix, D., Alonso, J.R., Narvaez, J.A., Tramu, G. & Gonzalez-Baron, S. (1989). Immunocytochemical study of angiotensin II fibers and cell bodies in the brainstem respiratory areas of the cat. Brain Research 489, 311317.CrossRefGoogle ScholarPubMed
Albano, J.E., Mishkin, M., Westbrook, L.E. & Wurtz, R.H. (1982). Visuomotor deficits following ablation of monkey superior colliculus. Journal of Neurophysiology 48, 338351.CrossRefGoogle ScholarPubMed
Ashby, C.R. Jr., Minabe, Y., Edwards, E. & Wang, R.Y. (1991). 5-HT3-like receptors in the rat medial prefrontal cortex: An electrophysiological study. Brain Research 550, 181191.CrossRefGoogle ScholarPubMed
Barnes, K.L., Diz, D.I. & Ferrario, C.M. (1991). Functional interactions between angiotensin II and substance P in the dorsal medulla. Hypertension 17, 11211126.CrossRefGoogle ScholarPubMed
Barnes, K.L., Knowles, W.D. & Ferrario, C.M. (1990). Angiotensin II and angiotensin (1–7) excite neurons in the canine medulla in vitro. Brain Research Bulletin 24, 275280.CrossRefGoogle ScholarPubMed
Barnes, K.L., Qu, L. & McQueeney, A.J. (1992). Are angiotensin II and substance P receptors on medial NTS neurons pre- or postsynaptic? Society for Neuroscience Abstracts 18, 755.Google Scholar
Besson, J., Sarrieau, A., Vial, M., Marie, J. -C., Rosselin, G. & Rostene, W. (1986). Characterization and autoradiographic distribution of vasoactive intestinal peptide binding sites in the rat central nervous system. Brain Research 398, 329336.CrossRefGoogle ScholarPubMed
Born, J. & Fehm, H.L. (1988). The hormonal modulation of stimulus processing in humans. German Journal of Psychology 4, 315331.Google Scholar
Braszko, J.J., Wlasienko, J., Koziolkiewicz, W., Janecka, A. & Wisniewski, K. (1991). The 3–7 fragment of angiotensin II is probably responsible for its psychoactive properties. Brain Research 542, 4954CrossRefGoogle ScholarPubMed
Brownfield, M.S., Reid, I.A., Ganten, D. & Ganong, W.F. (1982). Differential distribution of immunoreactive angiotensin and angiotensin-converting enzyme in rat brain. Neuroscience 1, 17591769.CrossRefGoogle Scholar
Bunnemann, B., Fuxe, K. & Ganten, D. (1992). The brain renin-angiotensin system: Localization and general significance. Journal of Cardiovascular Pharmacology 19 (Suppl. 6), S51–S62.CrossRefGoogle ScholarPubMed
Bunsey, M., Kramer, D., Kesler, M. & Strupp, B.J. (1990). A vasopressin metabolite increases attentional selectivity. Behavioral Neuroscience 104, 277287.CrossRefGoogle ScholarPubMed
Castel, M.-N., Stutzmann, J.-M., Lucas, M., Lafforgue, J. & Blanchard, J.-C. (1989). Effects of ICV administration of neurotensin and analogs, on EEG in rats. Peptides 10, 95101.CrossRefGoogle ScholarPubMed
Chai, S.Y., McKenzie, J.S., McKinley, M.J. & Mendelsohn, F.A.O. (1990). Angiotensin converting enzyme in the human basal forebrain and midbrain visualized by in vitro autoradiography. Journal of Comparative Neurology 291, 179194.CrossRefGoogle ScholarPubMed
Chai, S.Y., McKinley, M.J., Paxinos, G. & Mendelsohn, F.A.O. (1991). Angiotensin converting enzyme in the monkey (Macaco Fascicularis) brain visualized by in vitro autoradiography. Neuroscience 42, 483495.CrossRefGoogle Scholar
Chai, S.Y., Mendelsohn, F.A.O. & Paxinos, G. (1987). Angiotensin converting enzyme in rat brain visualized by quantitative in vitro autoradiography. Neuroscience 20, 615627.CrossRefGoogle ScholarPubMed
DeSouza, E.B., Insel, T.R., Perrin, M.H., Rivier, J., Vale, W.W. & Kuhar, M.J. (1985). Corticotropin-releasing factor receptors are widely distributed within the rat central nervous system: An autoradiographic study. Journal of Neuroscience 5, 31893202.CrossRefGoogle Scholar
Freund-Mercier, M.J., Stoeckel, M.E., Palacios, J.M., Pazos, A., Reichhart, J.M., Porte, A. & Richard, Ph. (1987). Pharmacological characteristics and anatomical distribution of [3H] oxytocinbinding sites in the wistar rat brain studied by autoradiography. Neuroscience 20, 599614.CrossRefGoogle ScholarPubMed
Gehlert, D.R., Gackenheimer, S.L., Reel, J.K., Lin, H.-S. & Steinberg, M.I. (1990). Non-peptide angiotensin II receptor antagonists discriminate subtypes of 125I-angiotensin II binding sites in the rat brain. European Journal of Pharmacology 187, 123126.CrossRefGoogle ScholarPubMed
Gehlert, D.R., Gackenheimer, S.L. & Schober, D.A. (1991). Autoradiographic localization of subtypes of angiotensin II antagonist binding in the rat brain. Neuroscience 44, 501514.CrossRefGoogle ScholarPubMed
Getz, R., Merchant, C., Rosenstein, J., Merali, Z. & Moody, T.W. (1992). Ontogeny of bombesin/gastrin-releasing peptide binding sites in rat brain. Molecular and Cellular Neuroscience 3, 162170.CrossRefGoogle ScholarPubMed
Goodale, M.A. & Murison, R.C.C. (1975). The effects of lesions of the superior colliculus on locomotor orientation and the orienting reflex in the rat. Brain Research 88, 243261.CrossRefGoogle ScholarPubMed
Harding, J.W., Hanesworth, J.M., Swanson, J.N., Cook, V.I., Wing, A.V., Stobb, J.W., Jensen, L.L., Sardinia, M. & Wright, J.W. (1991). Identification of a new angiotensin receptor subtype in guinea pig brain. Society for Neuroscience Abstracts 17, 809.Google Scholar
Huang, X., Mooney, R.D. & Rhoades, R.W. (1993). Effects of serotonin (5HT) upon the retinotectal, corticotectal and glutamate-induced activity in the superior colliculus of the hamster. Journal of Neurophysiology 70, 723732.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vaneges, H., pp. 687725. New York: Plenum Publishing Corporation.CrossRefGoogle Scholar
Jhamandas, J.H., Lind, R.W. & Renaud, L.P. (1989). Angiotensin II may mediate excitatory neurotransmission from the subfornical organ to the hypothalamic supraoptic nucleus: An anatomical and electrophysiological study in the rat. Brain Research 487, 5261.CrossRefGoogle Scholar
Kang, J., Sumners, C. & Posner, P. (1992). Modulation of net outward current in cultured neurons by angiotensin II: Involvement of AT1, and AT2 receptors. Brain Research 580, 317324.CrossRefGoogle ScholarPubMed
Lind, R.W., Swanson, L.W. & Ganten, D. (1985). Organization of angiotensin II immunoreactive cells and fibers in the rat central nervous system. Neuroendocrinology 40, 224.CrossRefGoogle ScholarPubMed
Loup, F., Tribollet, E., Dubois-Dauphin, M. & Dreifuss, J.J. (1991). Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Research 555, 220232.CrossRefGoogle Scholar
Manaker, S., Winokur, A., Rostene, W.H. & Rainbow, T.C. (1985). Autoradiographic localization of thyrotropin-releasing hormone receptors in the rat central nervous system. Journal of Neuroscience 5, 167174.CrossRefGoogle ScholarPubMed
Mendelsohn, F.A.O., Quirion, R., Saavedra, J.M., Aguilera, G. & Catt, K.J. (1984). Autoradiographic localization of angiotensin II receptors in the rat brain. Procedings of the National Academy of Sciences of the U.S.A. 81, 15751579.CrossRefGoogle ScholarPubMed
Mooney, R.D., Bennett-Clarke, C., Chiaia, N.L., Sahibzada, N. & Rhoades, R.W. (1990). Organization and actions of the noradrenergic input to the hamster's superior colliculus. Journal of Comparative Neurology 292, 214230.CrossRefGoogle Scholar
Mooney, R.D., Klein, B.G. & Rhoades, R.W. (1985). Correlations between the structural and functional characteristics of neurons in the superficial laminae of the hamster's superior colliculus. Journal of Neurosciences, 29893009.CrossRefGoogle ScholarPubMed
Moyse, E., Rosténe, W., Vial, M., Leonard, K., Mazella, J., Kitabgi, P., Vincent, J.-P. & Beaudet, , (1987). A. Distribution of neurotensin binding sites in rat brain: A light microscopic radioautographic study using monoiodo [125I] tyr3-neurotensin. Neuroscience 22, 525536.CrossRefGoogle Scholar
Papas, S., Smith, P. & Ferguson, A.V. (1990). Electrophysiological evidence that systemic angiotensin influences rat area postrema neurons. American Journal of Physiology 258, R70–R76.Google ScholarPubMed
Robinson, J.K. & Crawley, J.N. (1992). Galanin mimics scopolamine in disrupting delayed non-matching to sample (DNMTS) in rats. Society for Neuroscience Abstracts 18, 341.Google Scholar
Rowe, B.P., Grove, K.L., Saylor, D.L. & Speth, R.C. (1990). Angiotensin II receptor subtypes in the rat brain. European Journal of Pharmacology 186, 339342.CrossRefGoogle ScholarPubMed
Saylor, D.L., Perez, R.A., Absher, D.R., Baisden, R.H., Woodruff, M.L., Joyner, W.L. & Rowe, B.P. (1992). Angiotensin II binding sites in the hamster brain: Localization and subtype distribution. Brain Research 595, 98106.CrossRefGoogle ScholarPubMed
Schaffer, M.M. & Moody, T.W. (1986). Autoradiographic visualization of CNS receptors for vasoactive intestinal peptide. Peptides 1, 283288.CrossRefGoogle Scholar
Semple, P.F. & Morton, J.J. (1976). Angiotensin II and angiotensin II in rat blood. Circulatory Research 38 (Suppl. II), 122126.CrossRefGoogle ScholarPubMed
Semple, P.F., Boyd, A.S., Dawes, P.M. & Morton, J.J. (1976). Angiotensin II and its heptapeptide (2–8), hexapeptide (3–8) and pentapeptide (4–8) metabolites in arterial and venous blood of man. Circulatory Research 39, 671678.CrossRefGoogle ScholarPubMed
Skofitsch, G., Sills, M.A. & Jacobowitz, D.M. (1986). Autoradiographic distribution of 125I-galanin binding sites in the rat central nervous system. Peptides 7, 10291042.CrossRefGoogle ScholarPubMed
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In The Neurobiology of Saccadic Eye Movements Vol. 3: Reviews of Oculomotor Research, ed. Wurtz, R.H. & Goldberg, M.E., pp 213255. Amsterdam: Elsevier.Google Scholar
Sprague, J.M. (1991). The role of the superior colliculus in facilitating visual attention and form perception. Proceedings of the National Academy of Sciences of the U.S.A. 88, 12861290.CrossRefGoogle ScholarPubMed
Sprague, J.M. & Meikle, T.H. Jr. (1965). The role of the superior colliculus in visually guided behavior. Experimental Neurology 11, 115146.CrossRefGoogle ScholarPubMed
Sumners, C., Tang, W., Zelezna, B. & Raizada, M.K. (1991). Angiotensin II receptor subtypes are coupled with distinct signal-transduction mechanisms in neurons and astrocytes from rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 88, 75677571.CrossRefGoogle ScholarPubMed
Waterhouse, B.D. & Woodward, D.J. (1980). Interaction of norepinephrine with cerebrocortical activity evoked by stimulation of somatosensory afferent pathways in the rat. Experimental Neurology 67, 1134.CrossRefGoogle ScholarPubMed
Wenk, G.L., Markowska, A.L. & Olton, D.S. (1989). Basal forebrain lesions and memory: Alterations in neurotensin, not acetylcholine, may cause amnesia. Behavioral Neuroscience 103, 765769.CrossRefGoogle Scholar
Wong, P.C., Price, W.A., Chiu, A.T., Duncia, J.V., Carini, D.J., Wexler, R.R., Johnson, A.L. & Timmermans, P.B.M.W.M. (1989). Nonpeptide angiotensin II receptor antagonists. VIII. Characterization of functional antagonism displayed by DuP753, an orally active antihypertensive agent. Journal of Pharmacology and Experimental Therapeutics 252, 719725.Google Scholar
Wurtz, R.H. & Albano, J.E. (1980). Visual-motor function of the primate superior colliculus. Annual Review of Neuroscience 3, 189226.CrossRefGoogle ScholarPubMed
Xiong, H. & Marshall, K.C. (1991). Angiotensin II depresses glutamate-induced depolarization and synaptic transmission of locus coeruleus neurons. Society for Neuroscience Abstracts 17, 808.Google Scholar
Young, W.S. III. & Kuhar, M.J. (1979). Neurotensin receptors: Autoradiographic localization in rat CNS. European Journal of Pharmacology 59, 161163.CrossRefGoogle ScholarPubMed