Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-24T04:58:18.573Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural interactions mediating the detection of motion in the retina of the tiger salamander

Published online by Cambridge University Press:  02 June 2009

Frank Werblin ,
Greg Maguire ,
Peter Lukasiewicz ,
Scott Eliasof  and
Samuel M. Wu
Frank Werblin
Affiliation:
Neurobiology Group, University of California at Berkeley, Berkeley, California
Greg Maguire
Affiliation:
Neurobiology Group, University of California at Berkeley, Berkeley, California
Peter Lukasiewicz
Affiliation:
Neurobiology Group, University of California at Berkeley, Berkeley, California
Scott Eliasof
Affiliation:
Neurobiology Group, University of California at Berkeley, Berkeley, California
Samuel M. Wu
Affiliation:
Cullen Eye Institute, Baylor Medical School, Houston, Texas
Get access Rights & Permissions [Opens in a new window]

Abstract

The neural circuitry underlying movement detection was inferred from studies of amacrine cells under whole-cell patch clamp in retinal slices. Cells were identified by Lucifer yellow staining. Synaptic inputs were driven by “puffing“ transmitter substances at the dendrites of presynaptic cells. Spatial sensitivity profiles for amacrine cells were measured by puffing transmitter substances along the lateral spread of their processes. Synaptic pathways were separated and identified with appropriate pre- and postsynaptic pharmacological blocking agents.

Two distinct amacrine cell types were found: one with narrow spread of processes that sustained excitatory synaptic current, the other with very wide spread of processes that transient excitatory synaptic currents. The transient currents found only in the wide-field amacrine cell were formed presynaptically at GABAB receptors. They could be blocked with baclofen, a GABAB agonist, and their time course was extended by AVA, a GABAB antagonist. Baclofen and AVA had no direct affect upon the wide-field amacrine cell, but picrotoxin blocked a separate, direct GABA input to this cell.

The narrow-field amacrine cell was shown to be GABAergic by counterstaining with anti-GABA antiserum after it was filled with Lucifer yellow. Its narrow, spatial profile and sustained synaptic input are properties that closely match those of the GABAergic antagonistic signal that forms transient activity (described above), suggesting that the narrow-field amacrine cell itself is the source of the GABAergic interaction mediating transient activity in the inner plexiform layer (IPL). Other work has shown a GABAB sensitivity at some bipolar terminals, suggesting a population of bipolars as the probable site of interaction mediating transient action.

The results suggest that two local populations of amacrine cell types (sustained and transient) interact with the two populations of bipolar cell types (transient forming and nontransient forming). These interactions underlie the formation of the change-detecting subunits. We suggest that local populations of these subunits converge to form the receptive fields of movement-detecting ganglion cells.

Keywords

Neural circuitryAmacrine cellsInner plexiform layerMovement detectionGABABLateral inhibition
Type
Research Article
Information
Visual Neuroscience , Volume 1 , Issue 3 , May 1988 , pp. 317 - 329
Copyright
Copyright © Cambridge University Press 1988

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

Agardh, E., Bruun, A., Ehinger, B., Ekstrom, P., Van Veen, T. & Wu, J.-Y. (1987). Gama-aminobutyric acid and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. Journal of Comparative Neurology 258, 622–630.Google Scholar
Ariel, M. & Daw, N.W. (1982 a). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.Google Scholar
Ariel, M. & DAW, N.W. (1982 b). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135–160.CrossRefGoogle ScholarPubMed
Attwell, D., Mobbs, P., Tessier-Lavigne, M. & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolotl Ambystoma mexicanum. Journal of Physiology 387, 125–161.CrossRefGoogle ScholarPubMed
Ball, A.K. (1987). Immunocytochemical and autoradiographic localization of GABAergic neurons of the goldfish retina. Journal of Comparative Neurology 255, 317–325.CrossRefGoogle ScholarPubMed
Barlow, H.B. (1953). Summation and inhibition in the frogs retina. Journal of Physiology 119, 69–88.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanisms of directionally selective units in rabbit's retina. Journal of Physiology 178, 477–504.Google Scholar
Barnes, S. & Werblin, F.S. (1986). Gated currents generate single spike activity in amacrine cells of the tiger salamander retina. Proceedings of the National Academy of Sciences of the United States of America 83, 1509–1512.CrossRefGoogle ScholarPubMed
Barnes, S. & Werblin, F.S. (1987). Direct excitatory and lateral inhibitory synaptic inputs to amacrine cells in the tiger salamander retina. Brain Research 406, 233–237.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1984). Strychnine blocks transient but not sustained inhibition in mudpuppy retinal ganglion cells. Journal of Physiology 354, 273–286.CrossRefGoogle Scholar
Bowery, N.G., Doble, A., Hill, D.R., Hudson, A.L., Shaw, J.S., Turnbull, M.G. & Warrington, R. (1981). Bicuculline insensitive GABA receptors on peripheral autonomic nerve terminals. European Journal of Pharmacology 71, 53–70.CrossRefGoogle ScholarPubMed
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral inteeractions for cells with more complex receptive fields. Journal of Physiology 276, 277–298.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology 240, 457–492.CrossRefGoogle Scholar
Cronly-Dillon, J.R. (1964). Units sensitive to direction of movement in goldfish optic tectum. Nature 203, 214–215.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Werblin, F.S. (1969). Functional organization of vertebrate retina: I. Synaptic structure. Journal of Neurophysiology 32, 315–338.CrossRefGoogle Scholar
Eliasof, S.R., Barnes, S. & Werblin, F.S. (1987). The interaction of ionic currents mediating single spike activity in retinal amacrine cells of the tiger salamander. Journal of Neuroscience (New York) 7, 3512–3524.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr. (1983). “Starburst” amacrine cells and cholinergic neurons: mirror symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.Google Scholar
Famiglietti, E.V. Jr., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Famiglietti, E.V. Jr. & Kolb, H. (1976). Structural basis of “ON”- and “OFF”-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle Scholar
Frishman, L.J. & Linsenmeier, R.A. (1982). Effects of picrotoxin and strychnine on non-linear responses of Y-type retinal ganglion cells. Journal of Physiology 324, 347–363.CrossRefGoogle Scholar
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pfluegers Archiv. European Journal of Physiology 391, 85–100.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.Google Scholar
Lipetz, L.E. & Hill, R.M. (1970). Discrimination characteristics of the turtle's retinal ganglion cells. Experientia 26, 373–374.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D. & Werblin, F.S. (1988). A slowly-inactivating potassium current truncates spike activity in ganglion cells of the tiger salamander retina. Journal of Neuroscience, in press.Google Scholar
Maguire, G.W., Lukasiewicz, P.D. & Werblin, F.S. (1988). Neural interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience, in press.Google Scholar
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–245.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. & Torre, V. (1978). The responses of amacrine cells to light and intracellularly applied currents. Journal of Physiology 276, 83–102.CrossRefGoogle ScholarPubMed
Maturana, H.R. & Frank, S. (1963). Directional movement and horizontal edge detectors in the pigeon retina. Science 142, 977–979.CrossRefGoogle ScholarPubMed
Maturana, H.R., Lettvin, J.Y., Pitts, W.H. & McCulloch, W.S. (1960). Journal of General Physiology (New York) 43 (Suppl.), 129–175.CrossRefGoogle Scholar
Michael, C.R. (1968). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. II. Directionally selective units. Journal of Neurophysiology 31, 257–267.CrossRefGoogle Scholar
Miles, F.A. (1972). Centrifugal control of the avian retina. I. Receptive field properties of retinal ganglion cells. Brain Research 48, 65–92.Google Scholar
Muhyaddin, M., Roberts, P.J. & Woodruff, G.N. (1982). Presynaptic g-aminobutyric acid receptors in the rat anococcygeus muscle and their antagonism by 5 aminovaleric acid. British Journal of Pharmacology 77, 163–168.CrossRefGoogle Scholar
Nakahiro, M., Kihachi, S., Yamoda, I. & Yoshida, H. (1985). Antagonistic effect of gamino valeric acid on bicuculline-insensitive g-aminobutyric acid (GABAB) sites in rat's brain. Neuroscience Letters (Limerick) 57, 263–266.CrossRefGoogle Scholar
Nelson, R., Famiglietti, E.V. Jr., & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for ON and OFF center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–483.CrossRefGoogle ScholarPubMed
Robertson, B. & Taylor, W.R. (1986). Effects of g-aminobutyric acid and (−) Baclofen on calcium and potassium currents in cat dorsal root ganglion neurones in vitro. British Journal of Pharmacology 89, 661–672.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1983 a). Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537–538.Google Scholar
Slaughter, M.M. & Miller, R.F. (1983 b). The role of excitatory amino acid transmitters in the mudpuppy retina: an analysis with kainic acid and n-methyl aspartate. Journal of Neuroscience 3, 1701–1711.CrossRefGoogle ScholarPubMed
Stell, W.K., Ishida, A.T. & Lightfoot, D.O. (1977). Structural basis for on and off-center responses in the retina of the goldfish. Science 198, 1269–1271.CrossRefGoogle Scholar
Stewart, W.W. (1978). Functional connections between cells as revealed by a highly fluorescent naphthalimide tracer. Cell 14, 741–759.CrossRefGoogle ScholarPubMed
Stone, J. & Fabian, M. (1966). Specialized receptive fields of the cat's retina. Science 152, 1277–1279.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1987). Bipolar cells receive negative feedback input from GABAergic amacrine cells. Investigative Opthalmology and Visual Science, Suppl. 28, 51.Google Scholar
Vallerga, S. (1981). Physiological and morphological identification of amacrine cells in the retina of the larval tiger salamander. Vision Research 21, 1307–1317.CrossRefGoogle ScholarPubMed
Vaughn, J.E., Famiglietti, E.V. Jr., Barber, R.P., Saito, K., Roberts, E. & Ribak, C.E. (1981). GABAergic amacrine cells in rat retina, immunocytochemical identification and synaptic connectivity. Journal of Comparative Neurology 197, 113–127.CrossRefGoogle ScholarPubMed
Wartzok, D. & Marks, W.B. (1973). Directionally selective units recorded in optic tectum of the goldfish. Journal of Neurophysiology 36, 588–604.CrossRefGoogle ScholarPubMed
Werblin, F.S. (1979). Integrative pathways in local circuits between slow-potential cells in the retina. In The Neurosciences: Fourth Study Program, ed. Schmitt, F.S. & Worden, F.G. Cambridge, Mass.: MIT Press, pp. 193–211.Google Scholar
Werblin, F.S. (1978). Transmission along and between rods in the retina of the tiger salamander. Journal of Physiology 294, 613–626.CrossRefGoogle Scholar
Werblin, F.S. (1970). Responses of retinal cells to moving spots: Intracellular recording in Necturus maculosus. Journal of Neurophysiology 33, 342–350.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1974). Synaptic organization of the inner plexiform layer in the retina of the tiger salamander. Journal of Neurocytology 3, 1–33.CrossRefGoogle Scholar
Wu, J.Y., Brandon, C., SU, Y.T. & LAM, D.M.K. (1981). Immunocytochemical and autoradiographic localization of GABA system in the vertebrate retina. Molecular and Cell Biochemistry 39, 229–237.CrossRefGoogle ScholarPubMed
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204–205.Google Scholar
Zenkin, G.M. & Pigarev, I.N. (1969). Detector properties of the ganglion cells of the pike retina. Biophysics 14, 763–772.Google ScholarPubMed