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The modulatory cholinergic system in goldfish tectum may be necessary for retinotopic sharpening

Published online by Cambridge University Press:  02 June 2009

John T. Schmidt
John T. Schmidt
Affiliation:
Department of Biological Science and Neurobiology Research Center, State University of New York at Albany, Albany
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Abstract

The cholinergic circuit within the tectum and the cholinergic input from the nucleus isthmi mediate a presynaptic augmentation of retinotectal transmitter release via nicotinic receptors. In this study, the cholinergic systems were either eliminated using the cholinergic neurotoxin AF64A or blocked using nicotinic antagonists to test for effects on the activity-driven sharpening of the regenerating retinotectal projection. The effectiveness of the AF64A was verified by recording field potentials elicited by optic tract stimulation and by immunohistochemical staining for choline acetyltransferase (ChAT). At 1 week after intracranial (IC) injection of AF64A (12 to 144 nmoles) into the fluid above the tectum, field potentials showed a selective dose-dependent decrement of the cholinergic polysynaptic component with no effect on the amplitude of the glutamatergic monosynaptic component. The decrement was only partially recovered in recordings at 2 and 6 weeks. In normal fish, the ChAT antibody stains a population of periventricular neurons, their apical dendrites, and a dense plexus within the optic terminal lamina that consists of their local axons and fine dendrites and of input fibers from the nucleus isthmi. One week after IC AF64A injection (48–72 nmoles), most immunostaining in superficial tectum was lost but most neuronal somas in the deep tectum could still be seen, and staining in the tegmentum below the tectum was completely intact. At 2 weeks and later, the staining of neuronal somata largely recovered, but staining of the superficial plexus did not. AF64A treatment at 18 days after nerve crush, when regenerating retinal fibers are beginning to form synapses, prevented retinotopic sharpening of the projection. Recordings showed a rough retinotopic map on the tectum but the multiunit receptive fields (MURFs) at each tectal point averaged 34 deg vs. 11 deg in vehicle-injected control regenerates. AF64A treatment before nerve crush also blocked sharpening, ruling out a direct effect on retinal growth cones or retinal fibers, as AF64A rapidly decomposes, whereas its effect on the cholinergic fibers is long-lasting. IC injection or minipump infusion of the nicotinic antagonists α-bungarotoxin (αBTX), neuronal bungarotoxin (nBTX), and pancuronium during regeneration also prevented sharpening (MURFs averaging 29.4 deg, 33.0 deg, and 31.4 deg, respectively). Control Ringer≈s solution infusions or injections over the same period (19–37 days postcrush) had no effect on regenerated MURF size (11.7 deg). The results show that the cholinergic innervation, which modulates transmitter release, is required for activity-driven retinotopic sharpening, thought to be triggered by NMDA receptor activation.

Keywords

Nicotinic cholinergicRetinotectal projectionAF64A cholinotoxinBungarotoxinPancuroniumCholine acetyltransferaseSynaptic modulationField potentials
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 6 , November 1995 , pp. 1093 - 1103
Copyright
Copyright © Cambridge University Press 1995

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References

Aizenman, E., Loring, R.H. & Lipton, S.A. (1990). Blockade of nicotinic responses in rat retinal ganglion cells by neuronal bungarotoxin. Brain Research 517, 209–214.CrossRefGoogle ScholarPubMed
Britto, L.R.G., Hamassaki-Britto, D.E., Ferro, E.S., Keyser, K.T., Karten, H.J. & Lindstrom, J.M. (1992). Neurons of the chick brain and retina expressing both alpha-bungarotoxin-sensitive and alpha-bungarotoxin-insensitive nicotinic acetylcholine receptors: An immunohistochemical analysis. Brain Research 590, 193–200.CrossRefGoogle ScholarPubMed
Castro, N.G. & Albuquerque, E.X. (1995). Alpha-bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. Biophysical Journal 68, 516–524.CrossRefGoogle Scholar
Cline, H.T. & Constantine-Paton, M. (1989). NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3, 413–426.CrossRefGoogle ScholarPubMed
Constantine-Paton, M., Cline, H.T. & Debski, E.A. (1990). Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Review of Neuroscience 13, 129–154.CrossRefGoogle ScholarPubMed
Contestabile, A., Bissoli, R., Saverino, O. & Villani, L. (1987). Neurochemical and anatomical effects of the presumptive cholinergic toxin, AF64A, in various areas of the goldfish brain. Comparison with the effects in mammalian brain. In Cellular and Molecular Basis of Cholinergic Function, ed. Dowdall, M.J. & Hawthorne, J.N., pp. 651–657. Chichester: Ellis Horwood.Google Scholar
Couturier, S., Bertrand, D., Matter, J.-M., Hernandez, M.C., Bertrand, S., Millar, N., Valera, S., Barkas, T. & Ballivet, M. (1990). A neuronal nicotinic acetylcholine receptor subunit (α7). is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5, 847–856.CrossRefGoogle Scholar
Cserr, H.F. & Bundgaard, M. (1984). Blood-brain interfaces in vertebrates: A comparative approach. American Journal of Physiology 246, R277–R288.Google ScholarPubMed
Eisele, L.E. & Schmidt, J.T. (1988). Activity sharpens the regenerating retinotectal projection in goldfish: Sensitive period for strobe illumination and lack of effect on synaptogenesis and on ganglion cell receptive fields. Journal of Neurobiology 19, 395–411.CrossRefGoogle Scholar
Ekstrom, P. (1987). Distribution of choline acetyltransferase-immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.). Journal of Comparative Neurology 256, 494–515.CrossRefGoogle ScholarPubMed
Fisher, A., Mantione, C.R., Abraham, D.J. & Hanin, I. (1982). Longterm central cholinergic hypofunction induced in mice by ethylcholine aziridinium ion (AF64A) in vivo. Journal of Pharmacology and Experimental Therapeutics 222, 140–145.Google ScholarPubMed
Freeman, J.A. (1977). Possible regulatory function of acetylcholine receptor in maintenance of retinotectal synapses. Nature 269, 218–222.CrossRefGoogle ScholarPubMed
Goodman, C.S. & Shatz, C.J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Neuron 10 (Suppl.), 77–98.Google Scholar
Henley, J.M., Linstrom, J.M. & Oswald, R.E. (1986). Acetylcholine receptor synthesis in retina and transport to optic tectum in goldfish. Science 232, 1627–1629.CrossRefGoogle ScholarPubMed
Hortnagl, H., Potter, P.E. & Hannin, I. (1987). Effect of cholinergic deficit induced by ethylcholine aziridinium on serotinergic parameters in rat brain. Neuroscience 22, 203–213.CrossRefGoogle Scholar
Kageyama, G.H. & Meyer, R.L. (1989). Glutamate-immunoreactivity in the retina and optic tectum of goldfish. Brain Research 503, 118–127.CrossRefGoogle ScholarPubMed
Keyser, K.T., Britto, L.R.G., Schoepfer, R., Whiting, P., Cooper, J., Conroy, W., Brozozowska-Prechtl, A., Karten, H.J. & Lind-strom, J. (1993). Three subtypes of α-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina. Journal of Neuroscience 13, 442–454.CrossRefGoogle ScholarPubMed
Kiernan, J.A. & Contestabile, A. (1980). Vascular permeability associated with axonal regeneration in the optic system of the goldfish. Acta Neuropathologica (Berlin) 51, 39–45.CrossRefGoogle ScholarPubMed
King, W.M. (1990). Nicotinic depolarization of optic nerve terminals augments synaptic transmission. Brain Research 527, 150–154.CrossRefGoogle ScholarPubMed
King, W.M. & Schmidt, J.T. (1991). The long latency component of retinotectal transmission: Enhancement by stimulation of nucleus isthmi or tectobulbar tract and block by nicotinic cholinergic antagonists. Neuroscience 40, 701–712.CrossRefGoogle ScholarPubMed
King, W.M. & Schmidt, J.T. (1993). Nucleus isthmi in goldfish: In vitro recordings and fiber connections revealed by HRP injections. Visual Neuroscience 10, 419–437.CrossRefGoogle ScholarPubMed
Langdon, R.B. & Freeman, J.A. (1986). Antagonists of glutaminergic neurotransmission block retinotectal transmission in goldfish. Brain Research 398, 169–174.CrossRefGoogle ScholarPubMed
Leutje, C.W., Wada, K., Rogers, S., Abramson, S.N., Tsuji, K., Heinemann, S. & Patrick, J. (1990). Neurotoxins distinguish between different neuronal nicotinic acetylcholine receptor subunit combinations. Journal of Neurochemistry 55, 632–640.CrossRefGoogle Scholar
Leventer, S.M., Wulfert, E. & Hanin, I. (1987). Time course of ethylcholine aziridinium ion (AF64A)-induced cholinotoxicity in vivo. Neuropharmacology 26, 361–365.CrossRefGoogle ScholarPubMed
Listerud, M., Brussaard, A.B., Devay, P., Colman, D.R. & Role, L.R. (1991). Functional contribution of neuronal AChR subunits revealed by antisense oligonucleotides. Science 254, 1518–1521.CrossRefGoogle ScholarPubMed
Morley, B.J. & Murrin, L.C. (1989). AF64 depletes hypothalamic high-affinity choline uptake and disrupts the circadian rhythm of locomotor activity without altering the density of nicotinic acetylcholine receptors. Brain Research 504, 238–246.CrossRefGoogle ScholarPubMed
Mulle, C., Choquet, D., Korn, H. & Changeux, J.P. (1992). Calcium influx through nicotinic receptor in rat central neurons: Its relevance to cellular regulation. Neuron 8, 135–143.CrossRefGoogle ScholarPubMed
Nooney, J.M., Lambert, J.J. & Chiappinelli, V.A. (1992). The interaction of kappa-Bungarotoxin with the nicotinic receptor of bovine chromaffin cells. Brain Research 573, 77–82.CrossRefGoogle ScholarPubMed
Nowak, L., Bregestovski, P., Ascher, P., Herbert, A. & Prochianz, A. (1984). Magnesium gates glutamate activated channels in mouse central neurons. Nature 307, 462–465.CrossRefGoogle Scholar
Oswald, R.E., Schmidt, J.T., Norden, J.J. & Freeman, J.A. (1980). Localization of alpha bungarotoxin binding sites to the goldfish retinotectal projection. Brain Research 187, 113–127.CrossRefGoogle Scholar
Prusky, G.T. & Cynader, M.S. (1988). (3H)Nicotine binding sites are associated with mammalian optic nerve terminals. Visual Neuroscience 1, 245–248.CrossRefGoogle Scholar
Prusky, G.T., Shaw, C. & Cynader, M.S. (1987). Nicotine receptors are located on lateral geniculate nucleus terminals in cat visual cortex. Brain Research 412, 131–138.CrossRefGoogle ScholarPubMed
Sah, D.W.Y., Loring, R.H. & Zigmond, R.E. (1987). Long-term blockade by toxin F of nicotinic synaptic potentials in cultured sympathetic neurons. Neuroscience 20, 867–874.CrossRefGoogle ScholarPubMed
Sandberg, K., Schnaar, R.L. & Coyle, J.T. (1985). Method for the quantitation and characterization of the cholinergic neurotoxin, monoethylcholine mustard aziridinium ion (AF64A). Journal of Neuroscience Methods 14, 143–148.CrossRefGoogle ScholarPubMed
Schechter, N., Francis, A., Deutsch, D.F. & Gazzaniga, M.S. (1979). Recovery of tectal nicotinic cholinergic receptor sites during optic nerve regeneration in goldfish. Brain Research 166, 57–64.CrossRefGoogle ScholarPubMed
Schmidt, J.T. (1985). Apparent movement of optic terminals out of a local postsynaptically blocked region in goldfish optic tectum. Journal of Neurophysiology 53, 237–251.CrossRefGoogle ScholarPubMed
Schmidt, J.T. (1990). Long-term potentiation and activity-dependent retinotopic sharpening in the regenerating retinotectal projection of goldfish: Common sensitive period and sensitivity to NMDA blockers. Journal of Neuroscience 10, 233–246.CrossRefGoogle ScholarPubMed
Schmidt, J.T. (1991). Long-term potentiation during the activity- dependent sharpening of the retinotopic map in goldfish. Annals of the New York Academy of Sciences 627, 10–25.CrossRefGoogle ScholarPubMed
Schmidt, J.T. (1994). C-kinase manipulations disrupt activity-driven retinotopic sharpening in regenerating goldfish retinotectal projection. Journal of Neurobiology 25, 555–570.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Edwards, D.L. (1983). Activity sharpens the map during the regeneration of the retinotectal projection in goldfish. Brain Research 269, 29–39.CrossRefGoogle ScholarPubMed
Schmidt, J.T., Edwards, D.L. & Stuermer, C.A.O. (1983). The reestablishment of synaptic transmission by regenerating optic axons in goldfish: Time course and effects of blocking activity by intraocular injection of tetrodotoxin. Brain Research 269, 15–27.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Eisele, L.E. (1985). Stroboscopic illumination and dark rearing block the sharpening of the regenerated retinotectal map in goldfish. Neuroscience 14, 535–546.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Shashoua, V.E. (1988). Antibodies to ependymin block the sharpening of the regenerating retinotectal projection in goldfish. Brain Research 446, 269–284.CrossRefGoogle ScholarPubMed
Schwartz, M., Axelrod, D., Feldman, E.L. & Agranoff, B.W. (1980). Histological localization of binding sites of α-ungarotoxin and of antibodies specific to acetylcholine receptor in goldfish optic nerve and tectum. Brain Research 194, 171–180.CrossRefGoogle ScholarPubMed
Seguela, P., Wadiche, J., Dineley-Miller, K., Dani, J.A. & Patrick, J. (1993). Molecular cloning, functional properties, and distribution of rat brain α7: A nicotinic cation channel highly permeable to calcium. Journal of Neuroscience 13, 596–604.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Tennant, M. & Beazley, L.D. (1992). A breakdown of the blood-brain barrier is associated with optic nerve regeneration in the frog. Visual Neuroscience 9, 149–155.CrossRefGoogle ScholarPubMed
Tumosa, N., Stell, W.K., Johnson, C.D. & Epstein, M.L. (1986). Putative cholinergic interneurons in the optic tectum of goldfish. Brain Research 370, 365–369.CrossRefGoogle ScholarPubMed
van Deusen, E.B. & Meyer, R.L. (1990). Pharmacologic evidence for NMDA APB and kainate/quisqualate retinotectal transmission in the isolated whole tectum of goldfish. Brain Research 536, 86–96.CrossRefGoogle ScholarPubMed
Vernino, S., Amador, M., Leutje, C.W., Patrick, J. & Dani, J.A. (1992). Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8, 127–134.CrossRefGoogle ScholarPubMed
Vijayaraghavan, S., Pugh, P.C., Zhang, Z., Rathouz, M.M. & Berg, D.K. (1992). Nicotinic receptors that bind alpha-bungarotoxin on neurons raise intracellular free Ca2+. Neuron 8, 353–362.CrossRefGoogle ScholarPubMed
Villani, L., Bissoli, R., Garolini, S., Guarnieri, T., Battistini, S., Saverino, O. & Contestabile, A. (1988). Effect of AF64A on the cholinergic systems of the retina and optic tectum in goldfish. Experimental Brain Research 70, 455–462.CrossRefGoogle ScholarPubMed
Yazejian, B. & Fain, G.L. (1993). Whole cell currents activated at nicotinic acetylcholine receptors on ganglion cells isolated from goldfish retina. Visual Neuroscience 10, 353–361.CrossRefGoogle ScholarPubMed
Zottoli, S.J., Rhodes, K.J., Corrodi, J.G. & Mufson, E.J. (1988). Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali to the optic tectum in the goldfish (Carassius auratus). Journal of Comparative Neurology 273, 385–398.CrossRefGoogle Scholar
Zottoli, S.J., Rhodes, K.J. & Mufson, E.J. (1987). Comparison of acetylcholinesterase and choline acetyltransferase staining patterns in the optic tectum of the goldfish Carassius auratus. Brain, Behavior, and Evolution 30, 143–159.CrossRefGoogle ScholarPubMed