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. 1976 Jun 1;67(6):679–690. doi: 10.1085/jgp.67.6.679

Synaptic organization and ionic basis of on and off channels in mudpuppy retina. III. A model of ganglion cell receptive field organization based on chloride-free experiments

PMCID: PMC2214974  PMID: 932670

Abstract

A chloride-free environment produces selective changes in the retinal network which include a separation of on and off channels. The identification of chloride-sensitive and insensitivie neuronal activity permits identification of some of the connections and intervening polarities of synaptic interactions which are expressed in ganglion cell receptive field organization. These experiments support previous suggestions that surround antagonism is dependent on horizontal cell activity. In addition they suggest a model of the neuronal connections which subserve on-center, off-center, and on-off ganglion cells. Experimental tests of the on-off ganglion cell model favor the idea that this type of ganglion cell receives inhibitory input from amacrine cells and excitatory activation from depolarizing and hyperpolarizing bipolar cells.

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Selected References

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  1. BARLOW H. B., HILL R. M., LEVICK W. R. RETINAL GANGLION CELLS RESPONDING SELECTIVELY TO DIRECTION AND SPEED OF IMAGE MOTION IN THE RABBIT. J Physiol. 1964 Oct;173:377–407. doi: 10.1113/jphysiol.1964.sp007463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARLOW H. B. Summation and inhibition in the frog's retina. J Physiol. 1953 Jan;119(1):69–88. doi: 10.1113/jphysiol.1953.sp004829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barlow H. B., Levick W. R. Changes in the maintained discharge with adaptation level in the cat retina. J Physiol. 1969 Jun;202(3):699–718. doi: 10.1113/jphysiol.1969.sp008836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor D. A., Fuortes M. G., O'Bryan P. M. Receptive fields of cones in the retina of the turtle. J Physiol. 1971 Apr;214(2):265–294. doi: 10.1113/jphysiol.1971.sp009432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bortoff A. Localization of slow potential responses in the Necturus retina. Vision Res. 1964 Dec;4(11):627–635. doi: 10.1016/0042-6989(64)90048-3. [DOI] [PubMed] [Google Scholar]
  6. Brown J. E., Pinto L. H. Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus. J Physiol. 1974 Feb;236(3):575–591. doi: 10.1113/jphysiol.1974.sp010453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cervetto L., Piccolino M. Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science. 1974 Feb 1;183(4123):417–419. doi: 10.1126/science.183.4123.417. [DOI] [PubMed] [Google Scholar]
  8. Dacheux R. F., Miller R. F. Photoreceptor-bipolar cell transmission in the perfused retina eyecup of the mudpuppy. Science. 1976 Mar 5;191(4230):963–964. doi: 10.1126/science.175443. [DOI] [PubMed] [Google Scholar]
  9. Dowling J. E., Ripps H. Effect of magnesium on horizontal cell activity in the skate retina. Nature. 1973 Mar 9;242(5393):101–103. doi: 10.1038/242101a0. [DOI] [PubMed] [Google Scholar]
  10. Dowling J. E. Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates. Proc R Soc Lond B Biol Sci. 1968 Jun 11;170(1019):205–228. doi: 10.1098/rspb.1968.0034. [DOI] [PubMed] [Google Scholar]
  11. Dowling J. E., Werblin F. S. Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. J Neurophysiol. 1969 May;32(3):315–338. doi: 10.1152/jn.1969.32.3.315. [DOI] [PubMed] [Google Scholar]
  12. HAGIWARA S., TASAKI I. A study on the mechanism of impulse transmission across the giant synapse of the squid. J Physiol. 1958 Aug 29;143(1):114–137. doi: 10.1113/jphysiol.1958.sp006048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jung R. Neuronale Grundlagen des Hell-Dunkelsehens und der Farbwahrnehmung. Ber Zusammenkunft Dtsch Ophthalmol Ges. 1965;66:69–111. [PubMed] [Google Scholar]
  14. Kaneko A. Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J Physiol. 1970 May;207(3):623–633. doi: 10.1113/jphysiol.1970.sp009084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Miles F. A. Centrifugal control of the avian retina. I. Receptive field properties of retinal ganglion cells. Brain Res. 1972 Dec 24;48:65–92. doi: 10.1016/0006-8993(72)90171-0. [DOI] [PubMed] [Google Scholar]
  16. Miller R. F., Aacheux R. F. Information processing in the retina: importance of chloride ions. Science. 1973 Jul 20;181(4096):266–268. doi: 10.1126/science.181.4096.266. [DOI] [PubMed] [Google Scholar]
  17. Miller R. F., Dacheux R. F. Synaptic organization and ionic basis of on and off channels in mudpuppy retina. I. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolar cells, and amacrine cells. J Gen Physiol. 1976 Jun;67(6):639–659. doi: 10.1085/jgp.67.6.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miller R. F., Dacheux R. F. Synaptic organization and ionic basis of on and off channels in mudpuppy retina. II. Chloride-dependent ganglion cell mechanisms. J Gen Physiol. 1976 Jun;67(6):661–678. doi: 10.1085/jgp.67.6.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Miller R. F., Dacheux R. Chloride-sensitive receptive field mechanisms in the isolated retina-eye cup of the rabbit. Brain Res. 1975 Jun 13;90(2):329–334. doi: 10.1016/0006-8993(75)90315-7. [DOI] [PubMed] [Google Scholar]
  20. Murakami M., Otsuka T., Shimazaki H. Effects of aspartate and glutamate on the bipolar cells in the carp retina. Vision Res. 1975 Mar;15(3):456–458. doi: 10.1016/0042-6989(75)90101-7. [DOI] [PubMed] [Google Scholar]
  21. Naka K. I., Nye P. W. Role of horizontal cells in organization of the catfish retinal receptive field. J Neurophysiol. 1971 Sep;34(5):785–801. doi: 10.1152/jn.1971.34.5.785. [DOI] [PubMed] [Google Scholar]
  22. Naka K. I., Witkovsky P. Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells. J Physiol. 1972 Jun;223(2):449–460. doi: 10.1113/jphysiol.1972.sp009857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nelson R. A comparison of electrical properties of neurons in Necturus retina. J Neurophysiol. 1973 May;36(3):519–535. doi: 10.1152/jn.1973.36.3.519. [DOI] [PubMed] [Google Scholar]
  24. Oyster C. W. The analysis of image motion by the rabbit retina. J Physiol. 1968 Dec;199(3):613–635. doi: 10.1113/jphysiol.1968.sp008671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. TAKEUCHI A., TAKEUCHI N. Electrical changes in pre- and postsynaptic axons of the giant synapse of Loligo. J Gen Physiol. 1962 Jul;45:1181–1193. doi: 10.1085/jgp.45.6.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tomita T. Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harb Symp Quant Biol. 1965;30:559–566. doi: 10.1101/sqb.1965.030.01.054. [DOI] [PubMed] [Google Scholar]
  27. Toyoda J., Hashimoto H., Otsu K. Bipolar-amacrine transmission in the carp retina. Vision Res. 1973 Feb;13(2):295–307. doi: 10.1016/0042-6989(73)90108-9. [DOI] [PubMed] [Google Scholar]
  28. Trifonov I. U. Izuchenie sinapticheskoi peredachi mezhdu fotoretseptorom i gorizontal'noi kletkoi pri pomoshchi élektricheskikh razdrazhenii setchatki. Biofizika. 1968 Sep-Oct;13(5):809–817. [PubMed] [Google Scholar]
  29. Trifonov Iu A., Byzov A. L. Reaktsiia kletok-istochnikov s-potentsialov setchatki cherepakhi-na tok propuskaemyi cherez glaznoi bokal. Biofizika. 1965;10(4):673–680. [PubMed] [Google Scholar]
  30. Werblin F. S. Control of retinal sensitivity. II. Lateral interactions at the outer plexi form layer. J Gen Physiol. 1974 Jan;63(1):62–87. doi: 10.1085/jgp.63.1.62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Werblin F. S., Copenhagen D. R. Control of retinal sensitivity. 3. Lateral interactions at the inner plexiform layer. J Gen Physiol. 1974 Jan;63(1):88–110. doi: 10.1085/jgp.63.1.88. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Werblin F. S. Functional organization of a vertebrate retina: sharpening up in space and intensity. Ann N Y Acad Sci. 1972 Aug 25;193:75–85. doi: 10.1111/j.1749-6632.1972.tb27825.x. [DOI] [PubMed] [Google Scholar]

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