Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-04T21:08:51.840Z Has data issue: false hasContentIssue false
  • English
  • Français

Opioid receptors in the accessory optic system of the rat: Effects of monocular enucleation

Published online by Cambridge University Press:  02 June 2009

R.A. Giolli ,
R.H.I. Blanks ,
Y. Torigoe ,
R.J. Clarke ,
J.H. Fallon  and
F.M. Leslie
R.A. Giolli
Affiliation:
Department of Anatomy and Neurobiology, California College of Medicine, University of California, Irvine
R.H.I. Blanks
Affiliation:
Department of Anatomy and Neurobiology, California College of Medicine, University of California, Irvine Department of Surgery, Division of Otolaryngology – Head and Neck Surgery, California College of Medicine, University of California, Irvine
Y. Torigoe
Affiliation:
Department of Anatomy and Neurobiology, California College of Medicine, University of California, Irvine
R.J. Clarke
Affiliation:
Department of Anatomy and Neurobiology, California College of Medicine, University of California, Irvine Departamento de Fisiologia e Farmacologia, Universidade de Pernambuco, Cidade Universitaria, Recife 50.000 PE, Brazil
J.H. Fallon
Affiliation:
Department of Anatomy and Neurobiology, California College of Medicine, University of California, Irvine
F.M. Leslie
Affiliation:
Department of Pharmacology, California College of Medicine, University of California, Irvine
Get access Rights & Permissions [Opens in a new window]

Abstract

The presence and concentrations of each of the three subtypes of opioid receptors (mu, kappa, and delta) has been studied in the accessory optic nuclei (dorsal, lateral, and medial terminal nuclei and the interstitial nucleus of the superior fasciculus, posterior fibers: DTN, LTN, MTN, and inSFp) in normal young rats with radioligands directed towards each opioid receptor subtype. The changes in mu opioid receptors have also been investigated in monocularly enucleated rats in which one eye was removed and the rats sacrificed at postoperative day (PO) 2, 3, 5, 7, 14, and 30. As the MTN is the only accessory optic nucleus of the rat large enough for semiquantitative evaluation, the mu receptor population of the MTN has been subjected to optical microdensitometric analysis.

All four of the accessory optic nuclei (AOS nuclei) are found to contain exceedingly high levels of mu opioid receptor binding with the selective radioligand [3H]-[D-Ala, MePhe4, Gly-ol5] (DAGO), low levels of kappa opioid receptor binding using the radioligand [3H]-[ethylketocyclazocine] (EKC) together with the competing agents [D-Pro4]-morphiceptin and [D-Ser2, Thr6]-Leu-enkephalin, and an absence of delta opioid receptor binding with the radioligand [3H]-[D-A1a2, D-Leu5]-enkephalin (DADLE) combined with the competing agent [D-Pro4]-morphiceptin. Monocular enucleation, as studied on the mu opioid receptor population with this experimental approach, results in virtually a complete loss of mu opioid receptors throughout all four of the contralaterally located AOS nuclei, including both dorsal and ventral subdivisions of the medial terminal nucleus (MTNd, v). Kappa and delta receptors are very few (kappa receptors) or are lacking (delta receptors) in the AOS nuclei, and for this reason, the effects of monocular enucleation on these two opioid receptor subtypes have not been investigated. Monocular enucleation also produces a significant lowering in mu receptor binding in other primary optic nuclei (the lateral geniculate nuclei, nucleus of the optic tract, and superficial layers of the superior colliculus) and in the pars principalis of the medial geniculate nucleus (description of changes in mu receptors in non-accessory optic primary optic nuclei will be considered elsewhere).

Microdensitometric study of the MTNd, v shows that the decreased binding of mu receptors in this nucleus is barely detectable (about 6%) at PO2 and rises to 6–15% at PO3. At PO5 receptor loss reaches approximately 62%, whereas at PO7 it is about 81% complete. At PO14 and PO30, the mu receptor loss is nearly complete at around 93%. Mu receptor loss involves all of the AOS nuclei contralateral, but none ipsilateral, to ocular enucleation, an observation entirely consistent with the overwhelmingly crossed (about 97%) nature of the retinofugal projection to the rat accessory optic nuclei. These opioid receptors represent a prominent feature in the AOS and other primary optic nuclei of the rat. Their role in visuomotor control remains uncertain but probably involves the fine-tuning of information concerned with compensatory eye movements.

Keywords

Mu opioid receptorsKappa opioid receptorsDelta opioid receptorsAccessory optic systemAccessory optic nucleiRetinofugal fibersMonocular enucleationRat
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 5 , November 1990 , pp. 497 - 506
Copyright
Copyright © Cambridge University Press 1990

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

Atweh, S.F. & Kuhar, M.J. (1977). Autoradiographic localization of opiate receptors in rat brain, II: The brain stem. Brain Research 129, 1–12.Google Scholar
Atweh, S.F. & Kuhar, M.J. (1983). Distribution and physiological significance of opioid receptors in the brain. British Medical Bulletin 39, 47–52.Google Scholar
Atweh, S.F., Murrin, L.C. & Kuhar, M.J. (1978). Presynaptic localization of opiate receptors in the vagal and accessory optic systems:an autoradiographic study. Neuropharmacology 17, 65–71.CrossRefGoogle ScholarPubMed
Bennassi, C., Biral, G.P., Porro, C.A., & Corazza, R. (1989). The interstitial nucleus of the superior fasciculus, posterior bundle (inSFp) in the guinea pig: another nucleus of the accessory optic system processing the vertical retinal slip signal. Visual Neuroscience 2, 377–382.Google Scholar
Biral, G.P., Porro, C.A., Cavazzuti, M., Benassi, C. & Corazza, R. (1987). Vertical and horizontal visual whole-field motion differently affect the metabolic activity of the rat medial terminal nucleus. Brain Research 412, 43–53.CrossRefGoogle ScholarPubMed
Brecha, N., Johnson, D., Bolz, J., Sharma, S., Parnavelas, J.G. & Liberman, A.R. (1987). Substance P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit. Nature (London) 327, 155–158.CrossRefGoogle ScholarPubMed
Brown, R.M., Clouet, D.H. & Friedman, D.P. (1986). Preface. In Opiate Receptor Subtypes and Brain Function. ed. Brown, R.M., Clouet, D.H. & Friedman, D.P., pp. vii–xiii. NIDA Research Monograph 71, U.S. Department of Health & Human Services. Washington, D.C.Google Scholar
Bunt, S.M., Lund, R.D. & Land, P.W. (1983). Prenatal development of the optic projection in albino and hooded rats. Developmental Brain Research 6, 149–168.Google Scholar
Chevalier, G., Thierry, A.M., Shibazaki, T. & Feger, J. (1981). Evidence for a GABAergic inhibitory nigrotectal pathway in the rat. Neuroscience Letters 21, 67–70.CrossRefGoogle ScholarPubMed
Fallon, J.H. & Leslie, F.M. (1986). Distribution of dynorphin and enkephalin peptides in the rat brain. Journal of Comparative Neurology 249, 293–336.CrossRefGoogle ScholarPubMed
Fink, R.P. & Heimer, L. (1967). Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Research 4, 369–374.CrossRefGoogle ScholarPubMed
Fite, K.V., (1985). Pretectal and accessory-optic visual nuclei of fish, amphibia, and reptiles. Brain, Behavior and Evolution 26, 71–90.CrossRefGoogle ScholarPubMed
Fite, K.V., Reiner, A. & Hunt, S.P. (1979). Optokinetic nystagmus and the accessory optic system of pigeon and turtle. Brain, Behavior and Evolution 16, 192–202.CrossRefGoogle ScholarPubMed
Giardino, L., Biral, G.P., Calza, L. & Corazza, R. (1990). Different distribution of opiate and GABA systems in pretectal and accessory optic nuclei of the albino and pigmented rat and guinea pig. European Journal Neuroscience (Suppl.) (Abstract, in press).Google Scholar
Giolli, R.A. (1961). An experimental study of the accessory optic tracts (transpeduncular tracts and anterior accessory optic tracts) in the rabbit. Journal of Comparative Neurology 117, 77–96.Google Scholar
Giolli, R.A., Peterson, G.M., Ribak, C.E., McDonald, H.M., Blanks, R.H.I. & Fallon, J.H. (1985). GABAergic neurons comprise a major cell type in rodent visual relay nuclei: an immunocytochemical study of pretectal and accessory optic nuclei. Experimental Brain Research 61, 194–203.Google Scholar
Giolli, R.A. & Guthrie, M.D. (1969). The primary optic projections in the rabbit. An experimental degeneration study. Journal of Comparative Neurology 136, 99–126.CrossRefGoogle ScholarPubMed
Giolli, R.A. & Karamanlidis, A.N. (1978). The study of degenerating nerve fibers using silver-impregnation methods. In Neuroanatomical Research Techniques: Methods in Physiological Psychology, Vol. 2, ed. Robertson, R.T., pp. 211–240. New York: Academic Press.CrossRefGoogle Scholar
Giolli, R.A., Torigoe, Y. & Blanks, R.H.I. (1988). Nonretinal projections to the medial terminal accessory optic system in rabbit and rat: a retrograde and anterograde transport study. Journal of Comparative Neurology 269, 73–86.CrossRefGoogle Scholar
Grasse, K.L. & Cynader, M.S. (1982). Electrophysiology of medial terminal nucleus of the accessory optic system in the cat. Journal of Neurophysiology 48, 490–504.Google Scholar
Grasse, K.L. & Cynader, M.S. (1984). Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. Journal of Neurophysiology 51, 276–293.CrossRefGoogle ScholarPubMed
Hayhow, W.R., Sefton, A. & Webb, C. (1962). Primary optic centers in the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers. Journal of Comparative Neurology 118, 295–322.CrossRefGoogle Scholar
Hayhow, W.R., Webb, C. & Jervie, A. (1960). The accessory optic fiber system in the rat. Journal of Comparative Neurology 115, 185–215.Google Scholar
Herkenham, M. & Pert, C.B. (1982). Light-microscopic localization of brain opiate receptors: a general autoradiographic method which preserves tissue quality. Journal of Neuroscience 2, 1129–1149.Google Scholar
Holstege, G. & Collewijn, H. (1982). The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. Journal of Comparative Neurology 209, 139–175.Google Scholar
Hommer, D.W. & Pert, A. (1983). The actions of opiates in the rat substantia nigra: an electrophysiological analysis. Peptides 4, 603–608.CrossRefGoogle ScholarPubMed
Iwatsubo, K. & Kondo, Y. (1978). Inhibitory effects of morphine on the release of preloaded [3H]-GABA from rat substantia nigra in response to the stimulation of caudate nucleus and globus pallidus. In Characteristics and Functions of Opioids: Developments in Neuroscience, Vol. 4. ed. van Ree, J.M. & Terenws, L., pp. 357–358. Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
Jessell, T.M. & Iversen, L.L. (1977). Opiate analgesics inhibit substance P release from rat trigeminal nucleus. Nature 268, 549–551.CrossRefGoogle ScholarPubMed
Johnson, D., Yoser, S. & Brecha, N. (1986). Substance P-like in immunoreactivity in central visual pathways of the rabbit. Anatomical Record 214, 61A.Google Scholar
Kornblum, H.I., Hurlbut, D.E. & Leslie, F.M. (1987). Postnatal development of multiple opioid receptors in rat brain. Developmental Brain Research 37, 21–41.CrossRefGoogle Scholar
Kuhar, M.J. (1985). The mismatch problem in receptor mapping studies. Trends in Neurosciences 8, 190–191.Google Scholar
Kuhar, M.J., Pert, C.B. & Snyder, S. (1973). Regional distribution of opiate-receptor binding in monkey and human brain. Nature (London) 245, 447–450.Google Scholar
Lavin, A. & Garcia-Munoz, M. (1985). Electrophysiological changes in substantia nigra after dynorphin administration. Brain Research 369, 298–302.CrossRefGoogle Scholar
Lazar, G. (1983). Transection of the basal optic root in the frog abolishes vertical optokinetic head nystagmus. Neuroscience Letters 43, 7–11.CrossRefGoogle ScholarPubMed
Leslie, F.M. (1987). Methods used for the study of opioid receptors. Pharmacological Reviews 39, 197–249.Google Scholar
Llorens-Cortes, C., Pollard, H. & Schwartz, J.C. (1979). Localization of Opiate receptors in substantia nigra evidenced by lesion studies. Neuroscience Letters 12, 165–170.Google Scholar
Lui, F., Biral, G.P., Benassi, C., Ferrari, R. & Corazza, R. (1990). Correlation between retinal afferent distribution, neuronal size, and functional activity in the guinea pig medial terminal accessory optic nucleus. Experimental Brain Research 81, 77–84.CrossRefGoogle ScholarPubMed
Mansour, A., Khachaturian, H., Lewis, M.E., Akil, H. & Watson, S.J. (1987). Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. Journal of Neuroscience 7, 2445–2464.Google Scholar
McKenna, O.C. & Wallman, J. (1985). Accessory optic system and pretectum of birds: comparison with those of other vertebrates. Brain, Behavior, and Evolution 26, 91–116.CrossRefGoogle ScholarPubMed
McLean, S., Skirboll, L.R. & Pert, C.B. (1985). Comparison of substance P and enkephalin distribution in the rat brain: an overview using radioimmunocytochemistry. Neuroscience 14, 837–852.CrossRefGoogle Scholar
Mugnaini, E. & Oertel, W.H. (1985). An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In Handbook of Chemical Neuroanatomy. GABA and Neuropeptides in the CNS, Part 1, Vol. 4, ed. Bjorklund, A. & Hokfelt, T., pp 436–608. Amsterdam: Elsevier.Google Scholar
Mustari, M.J. & Fuchs, A.F. (1989). Response properties of single units in the lateral terminal nucleus of the accessory optic system in a behaving primate. Journal of Neurophysiology 61, 1207–1220.Google Scholar
Natal, C.L. & Britto, L.R.G. (1987). The pretectal nucleus of the optic tract modulates the direction selectivity of accessory optic neurons in rats. Brain Research 419, 320–323.Google Scholar
Nauta, W.J.H. & Gygax, P.A. (1954). Silver impregnation of degenerating axons in the central nervous system. Stain Technology 29, 91–93.Google Scholar
Ottersen, O.P. & Storm-Mathisen, J. (1984). GABA-containing neurons in the thalamus and pretectum of the rodent. Anatomy and Embryology 170, 197–207.Google Scholar
Oyster, C.W., Simpson, J.I., Takahashi, E.S. & Soodak, R.E. (1980). Retinal ganglion cells projecting to the rabbit accessory optic system. Journal of Comparative Neurology 190, 49–61.CrossRefGoogle Scholar
Oyster, C.W., Takahashi, E. & Collewijn, H. (1972). Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Research 12, 183–193.Google Scholar
Pasternak, G.W. (1987). Opioid receptors. In Psychopharmacology: The Third Generation of Progress, ed. Meltzer, H.Y., Chap. 29, pp. 281–288. New York: Raven Press.Google Scholar
Penny, G.R., Conley, M., Schmechel, D.E. & Diamond, I.T. (1984). The distribution of glutamic acid decarboxylase immunoreactivity in the diencephalon of the opossum and rabbit. Journal of Comparative Neurology 228, 38–56.CrossRefGoogle ScholarPubMed
Pert, C.B., Kuhar, M.J. & Snyder, S.H. (1975). Autoradiographic localization of the opiate receptor in rat brain. Life Sciences 16, 1849–1854.Google Scholar
Pert, C.B., Kuhar, M.J. & Snyder, S.H. (1976). The opiate receptor: autoradiographic localization in the rat brain. Proceedings of the National Academy of the Sciences U.S.A. 73, 3729–3733.Google Scholar
Rothenberg, S., Peck, E.A., Schottenfeld, S., Betley, G.E. & Altman, J.L. (1979). Methadone depression of visual signal detection performance. Pharmacology, Biochemistry, and Behavior 11, 521–527.Google Scholar
Rothenberg, S., Schottenfeld, S., Gross, K. & Selkoe, D. (1980 a). Specific oculumotor deficli acute methadone, I: Saccadic eye movements, Psychopharmacology 67, 221–228.Google Scholar
Rothenberg, S., Schottenfeld, S., Selkoe, D. & Gross, K. (1980 b). Specific oculomotor deficit after acute methadone, II: Smooth- pursuit eye movements. Psychopharmacology 67, 229–234.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review Neuroscience 7, 13–41.Google Scholar
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988). The accessory optic system of rabbit, II: Spatial organizaiton of direction selectivity. Journal of Neurophysiology 60, 2055–2072.Google Scholar
Simpson, J.I., Soodak, R. E. & Hess, R. (1979). The accessory optic system and its relation to the vestibulocerebellum. In Reflex Control of Posture and Movement, Vol. 50, ed. Granit, R. & Pompeiano, O. pp. 715–724. Amsterdam: Elsevier.Google Scholar
Starr, M.S. (1985). Multiple opiate receptors may be involved in suppressing gamma animobutyratase in substantia nigra. Life Sciences 37, 2249–2255.Google Scholar
Swanson, L.W., Cowan, W.M. & Jones, E.G. (1974). An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus of the albino rat and the cat. Journal of Comparative Neurology 156, 143–163.Google Scholar
Swanson, L.W., Simmons, D.M., Whiting, P.J. & Lindstrom, J. (1987). Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. Journal of Neuroscience 7, 3334–3342.Google Scholar
Turski, L., Havemann, U., Schwarz, M. & Kuschinsky, K. (1982). Disinhibition of nigral GABA output neurons mediates muscular rigidity elicited by striatal opioid receptor stimulation. Life Sciences 31, 2327–2330.Google Scholar
Voigt, T.J. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed
Walker, J.M., Bowen, W.D., Thompson, L.A., Frascella, J., Lahmkuhle, S. & Hughes, H.C. (1988). Distribution of opiate receptors within visual structures of the cat brain. Experimental Brain Research 73, 523–532.Google Scholar
Wallman, J., McKenna, O.C., Burns, S., Velez, J. & Weinstein, B. (1981). Relations of the accessory optic system and pretectum to optokinetic responses in chicken. In Progress in Oculomotor Research, ed. Fuchs, A.F. & Becker, W., pp. 435–442. Amsterdam: Elsevier/North Holland Press.Google Scholar
Weber, J.T. (1985). Pretectal complex and accessory optic system of primates. Brain, Behavior, and Evolution 26, 117–140.Google Scholar
Wood, P.L. (1982). Multiple opiate receptors: support for unique mu, delta, and kappa sites. Neuropharmacology 21, 487–497.Google Scholar