Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-19T04:20:25.492Z Has data issue: false hasContentIssue false
  • English
  • Français

Prolonged depolarization in rods in situ

Published online by Cambridge University Press:  02 June 2009

Dwight A. Burkhardt ,
Shaoqi Zhang  and
Jon Gottesman
Dwight A. Burkhardt
Affiliation:
Departments of Psychology and Physiology, University of Minnesonta, Minneapolis Graduate Program in Neuroscience, University of Minnesota, Minneapolis
Shaoqi Zhang
Affiliation:
Departments of Psychology and Physiology, University of Minnesonta, Minneapolis
Jon Gottesman
Affiliation:
Departments of Psychology and Physiology, University of Minnesonta, Minneapolis
Get access Rights & Permissions [Opens in a new window]

Abstract

Intracellular recordings were made from rods in the superfused retina of the marine toad (Bufo marinus). It was found that injection of a brief depolarizing current pulse (0.04–1 nA) evoked a distinctive, long-lasting response, here called “the prolonged depolarization.” The response appears to be regenerative, has a stereotypical waveform, is typically about 6 mV in &litude and 3 s in duration, and has a relatively long recovery period (10–60 s). As a rule, the response cannot be directly evoked by light but the current-evoked response is significantly enhanced in the presence of steady illumination. The light-evoked hyperpolarization and the depolarizing spikes of the rod are both attenuated in the presence of the prolonged depolarization. The prolonged depolarization is not an altered manifestation of the depolarizing spikes of toad rods since both can be recorded simultaneously and steady illumination suppresses the spikes while enhancing the prolonged depolarization. The response is enhanced in chloride-free superfusate and also appears to be enhanced by the use of electrodes containing chloride. The response is markedly shortened in superfusates that lack calcium or contain 1–5 mM cobalt. On this and other evidence, it is suggested that the response may be generated by the sequential action of calcium channels and calcium-activated chloride channels. Although rarely evoked by light, the prolonged depolarization of toad rods is otherwise remarkably similar to the prolonged depolarization of turtle cones. It is proposed that the prolonged depolarization, in contrast to the feedback depolarization of cones, arises from mechanisms common to both rods and cones.

Keywords

RodsProlonged depolarizationCones
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 6 , June 1991 , pp. 607 - 614
Copyright
Copyright © Cambridge University Press 1991

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

Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. Journal of Physiology 331, 253–284.CrossRefGoogle ScholarPubMed
Bader, C.R., Bertrand, D. & Schlichter, R. (1987). Calcium-activated chloride current in cultured sensory and parasympathetic quail neurons. Journal of Physiology 394, 125–148.CrossRefGoogle Scholar
Barish, M.E. (1983). A transient calcium-dependent chloride current in the immature Xenopus oocyte. Journal of Physiology 342, 309–325.CrossRefGoogle ScholarPubMed
Barnes, S. & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. Journal of General Physiology 94, 719–743.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fourtes, M.G.F. & O'Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.CrossRefGoogle ScholarPubMed
Brown, K.T. & Flaming, D.G. (1978). Opposing effects of calcium and barium in vertebrate rod photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 75, 1587–1590.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1977). Responses and receptive-field organization of cones in perch retinas. Journal of Neurophysiology 40, 53–62.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Hassin, G., Levine, J.S. & MacNichol, E.F. Jr (1980). Electrical responses and photopigments of twin cones in the retina of the walleye. Journal of Physiology 309, 215–228.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Gottesman, J. (1987). Light adaptation and responses to contrast flashes in cones of the walleye retina. Vision Research 27, 1409–1420.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1988). Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive-field surround. Journal of Physiology 407, 329–348.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1989). An eye-cup slice preparation for intracellular recording in vertebrate retinas. Journal of Neuroscience Methods 28, 179–187.CrossRefGoogle Scholar
Capovilla, L., Cervetto, L. & Torre, V. (1980). Effects of changing external potassium and chloride concentrations on the photoresponse of Bufo Bufo rods. Journal of Physiology 307, 529–551.CrossRefGoogle ScholarPubMed
Evans, M.G. & Marty, A. (1986). Calcium-dependent chloride currents in isolated cells from rat lacrimal glands. Journal of Physiology 378, 437–460.CrossRefGoogle ScholarPubMed
Fain, G.L., Gerschenfeld, H.M. & Quandt, F.N. (1980). Calcium spikes in toad rods. Journal of Physiology 303, 495–513.CrossRefGoogle ScholarPubMed
Fain, G.L. & Quandt, F.N. (1980). The effects of tetraethylammonium and cobalt ions on responses to extrinsic current in toad rods. Journal of Physiology 303, 515–533.CrossRefGoogle ScholarPubMed
Fuortes, M.G.F., Schwartz, E.A. & Simon, E.J. (1973). Colour-dependence of cone responses in the turtle retina. Journal of Physiology 234, 199–216.CrossRefGoogle ScholarPubMed
Lasansky, A. (1981). Synaptic action mediating cone response to annular illumination in the retina of the larval tiger salamander. Journal of Physiology 310, 205–214.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1982). A white-noise analysis of responses and receptive fields of catfish cones. Journal of Neurophysiology 47, 1057–1068.CrossRefGoogle ScholarPubMed
Maricq, A.V. & Korenbrot, J.I. (1988). Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1, 503–515.CrossRefGoogle ScholarPubMed
Mayer, M.L. (1985). A calcium-activated chloride current generates the afterdepolarization of rat sensory neurones in culture, Journal of Physiology 364, 217–239.CrossRefGoogle ScholarPubMed
Miyachi, E.-I., Takahashi, K.-I. & Murakami, M. (1984). Electrically evoked calcium responses in rods of frog retina. Japanese Journal of Physiology 34, 307–318.Google ScholarPubMed
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E. & Watanabe, S. (1982). GABA-mediated feedback from horizontal cells to cones in carp retina. Japanese Journal of Physiology 32, 911–926.Google ScholarPubMed
Oakley, B., Flaming, D. & Brown, K.T. (1979). Effects of rod receptor potential upon retinal potassium concentration. Journal of General Physiology 74, 713–737.CrossRefGoogle ScholarPubMed
O'Bryan, P.M. (1973). Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. Journal of Physiology 235, 207–223.CrossRefGoogle ScholarPubMed
Owen, D.G., Segal, M. & Barker, J.L. (1984). A Ca-dependent Cl– conductance in cultured mouse spinal neurons. Nature 311, 567–570.CrossRefGoogle Scholar
Owen, W.G. (1987). Ionic conductances in rod photoreceptors. Annual Review of Physiology 49, 743–764.CrossRefGoogle ScholarPubMed
Perlman, I., Normann, R.A., Itzhaki, A. & Daly, S.J. (1985). Chromatic and spatial information processing by red cones and L-type horizontal cells in the turtle retina. Vision Research 25, 543–549.CrossRefGoogle ScholarPubMed
Piccolino, M. & Gerschenfeld, H.M. (1980). Characteristics and ionic processes involved in feedback spikes of turtle cones. Proceedings of the Royal Society B (London) 206, 439–463.Google ScholarPubMed
Rogawski, M.A., Inoue, K., Suzuki, S. & Baker, J.L. (1988). A slow calcium-dependent chloride conductance in clonal anterior pituitary cells. Journal of Neurophysiology 59, 1854–1870.CrossRefGoogle ScholarPubMed
Skryzpek, J. & Werblin, F. (1983). Lateral interactions in absence of feedback to cones. Journal of Neurophysiology 49, 1007–1016.CrossRefGoogle Scholar
Somlyo, A.P. & Walz, B. (1985). Elemental distribution in Rana pipiens retinal rods: quantitative electron probe analysis. Journal of Physiology 397, 183–195.CrossRefGoogle Scholar
Thoreson, W.B. & Burkhardt, D.A. (1990). Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Visual Neuroscience 5, 571–583.CrossRefGoogle ScholarPubMed
Thoreson, W.B. & Burkhardt, D.A. (1991). Ionic influences on the prolonged depolarization of turtle cones in situ. Journal of Neurophysiology 65, 96–110.CrossRefGoogle ScholarPubMed
Yagi, T. & MacLeisch, P.R. (1989). Large calcium-activated current in solitary primate cones. Investigative Ophthalmology and Visual Science (Suppl.) 30, 62.Google Scholar