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. 1995 Nov 7;92(23):10658–10662. doi: 10.1073/pnas.92.23.10658

An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina.

S H DeVries 1, D A Baylor 1
PMCID: PMC40671  PMID: 7479860

Abstract

Rod signals in the mammalian retina are thought to reach ganglion cells over the circuit rod-->rod depolarizing bipolar cell-->AII amacrine cell-->cone bipolar cells-->ganglion cells. A possible alternative pathway involves gap junctions linking the rods and cones, the circuit being rod-->cone-->cone bipolar cells-->ganglion cells. It is not clear whether this second pathway indeed relays rod signals to ganglion cells. We studied signal flow in the isolated rabbit retina with a multielectrode array, which allows the activity of many identified ganglion cells to be observed simultaneously while the preparation is stimulated with light and/or exposed to drugs. When transmission between rods and rod depolarizing bipolar cells was blocked by the glutamate agonist 2-amino-4-phosphonobutyric acid (APB), rod input to all On-center and briskly responding Off-center ganglion cells was dramatically reduced as expected. Off responses persisted, however, in Off-center sluggish and On-Off direction-selective ganglion cells. Presumably these responses were generated by the alternative pathway involving rod-cone junctions. This APB-resistant pathway may carry the major rod input to Off-center sluggish and On-Off direction-selective ganglion cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  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. Baylor D. A., Hodgkin A. L. Detection and resolution of visual stimuli by turtle photoreceptors. J Physiol. 1973 Oct;234(1):163–198. doi: 10.1113/jphysiol.1973.sp010340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baylor D. A., Nunn B. J., Schnapf J. L. Spectral sensitivity of cones of the monkey Macaca fascicularis. J Physiol. 1987 Sep;390:145–160. doi: 10.1113/jphysiol.1987.sp016691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Caldwell J. H., Daw N. W. New properties of rabbit retinal ganglion cells. J Physiol. 1978 Mar;276:257–276. doi: 10.1113/jphysiol.1978.sp012232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cohen E., Sterling P. Demonstration of cell types among cone bipolar neurons of cat retina. Philos Trans R Soc Lond B Biol Sci. 1990 Dec 29;330(1258):305–321. doi: 10.1098/rstb.1990.0201. [DOI] [PubMed] [Google Scholar]
  6. Conner J. D., MacLeod D. I. Rod photoreceptors detect rapid flicker. Science. 1977 Feb 18;195(4279):698–699. doi: 10.1126/science.841308. [DOI] [PubMed] [Google Scholar]
  7. Conner J. D. The temporal properties of rod vision. J Physiol. 1982 Nov;332:139–155. doi: 10.1113/jphysiol.1982.sp014406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DARTNALL H. J. A. The interpretation of spectral sensitivity curves. Br Med Bull. 1953;9(1):24–30. doi: 10.1093/oxfordjournals.bmb.a074302. [DOI] [PubMed] [Google Scholar]
  9. Dacheux R. F., Raviola E. Horizontal cells in the retina of the rabbit. J Neurosci. 1982 Oct;2(10):1486–1493. doi: 10.1523/JNEUROSCI.02-10-01486.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dacheux R. F., Raviola E. The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. J Neurosci. 1986 Feb;6(2):331–345. doi: 10.1523/JNEUROSCI.06-02-00331.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Daw N. W., Jensen R. J., Brunken W. J. Rod pathways in mammalian retinae. Trends Neurosci. 1990 Mar;13(3):110–115. doi: 10.1016/0166-2236(90)90187-f. [DOI] [PubMed] [Google Scholar]
  12. Dolan R. P., Schiller P. H. Evidence for only depolarizing rod bipolar cells in the primate retina. Vis Neurosci. 1989;2(5):421–424. doi: 10.1017/s0952523800012311. [DOI] [PubMed] [Google Scholar]
  13. Dowling J. E., Boycott B. B. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci. 1966 Nov 15;166(1002):80–111. doi: 10.1098/rspb.1966.0086. [DOI] [PubMed] [Google Scholar]
  14. Famiglietti E. V., Jr Functional architecture of cone bipolar cells in mammalian retina. Vision Res. 1981;21(11):1559–1563. doi: 10.1016/0042-6989(81)90032-8. [DOI] [PubMed] [Google Scholar]
  15. Juliusson B., Bergström A., Röhlich P., Ehinger B., van Veen T., Szél A. Complementary cone fields of the rabbit retina. Invest Ophthalmol Vis Sci. 1994 Mar;35(3):811–818. [PubMed] [Google Scholar]
  16. Karschin A., Wässle H. Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. J Neurophysiol. 1990 Apr;63(4):860–876. doi: 10.1152/jn.1990.63.4.860. [DOI] [PubMed] [Google Scholar]
  17. Meister M., Pine J., Baylor D. A. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods. 1994 Jan;51(1):95–106. doi: 10.1016/0165-0270(94)90030-2. [DOI] [PubMed] [Google Scholar]
  18. Meister M., Wong R. O., Baylor D. A., Shatz C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science. 1991 May 17;252(5008):939–943. doi: 10.1126/science.2035024. [DOI] [PubMed] [Google Scholar]
  19. Müller F., Wässle H., Voigt T. Pharmacological modulation of the rod pathway in the cat retina. J Neurophysiol. 1988 Jun;59(6):1657–1672. doi: 10.1152/jn.1988.59.6.1657. [DOI] [PubMed] [Google Scholar]
  20. Nawy S., Jahr C. E. cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron. 1991 Oct;7(4):677–683. doi: 10.1016/0896-6273(91)90380-i. [DOI] [PubMed] [Google Scholar]
  21. Nelson R. Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J Comp Neurol. 1977 Mar 1;172(1):109–135. doi: 10.1002/cne.901720106. [DOI] [PubMed] [Google Scholar]
  22. Nelson R., Kolb H. Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Res. 1983;23(10):1183–1195. doi: 10.1016/0042-6989(83)90032-9. [DOI] [PubMed] [Google Scholar]
  23. Raviola E., Gilula N. B. Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1677–1681. doi: 10.1073/pnas.70.6.1677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Reid R. C., Shapley R. M. Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature. 1992 Apr 23;356(6371):716–718. doi: 10.1038/356716a0. [DOI] [PubMed] [Google Scholar]
  25. Schneeweis D. M., Schnapf J. L. Photovoltage of rods and cones in the macaque retina. Science. 1995 May 19;268(5213):1053–1056. doi: 10.1126/science.7754386. [DOI] [PubMed] [Google Scholar]
  26. Shiells R. A., Falk G., Naghshineh S. Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature. 1981 Dec 10;294(5841):592–594. doi: 10.1038/294592a0. [DOI] [PubMed] [Google Scholar]
  27. Slaughter M. M., Miller R. F. 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science. 1981 Jan 9;211(4478):182–185. doi: 10.1126/science.6255566. [DOI] [PubMed] [Google Scholar]
  28. Smith R. G., Freed M. A., Sterling P. Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. J Neurosci. 1986 Dec;6(12):3505–3517. doi: 10.1523/JNEUROSCI.06-12-03505.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Steinberg R. H. Rod and cone contributions to S-potentials from the cat retina. Vision Res. 1969 Nov;9(11):1319–1329. doi: 10.1016/0042-6989(69)90069-8. [DOI] [PubMed] [Google Scholar]
  30. Strettoi E., Dacheux R. F., Raviola E. Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. J Comp Neurol. 1990 May 15;295(3):449–466. doi: 10.1002/cne.902950309. [DOI] [PubMed] [Google Scholar]
  31. Suzuki S., Tachibana M., Kaneko A. Effects of glycine and GABA on isolated bipolar cells of the mouse retina. J Physiol. 1990 Feb;421:645–662. doi: 10.1113/jphysiol.1990.sp017967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vaney D. I., Young H. M., Gynther I. C. The rod circuit in the rabbit retina. Vis Neurosci. 1991 Jul-Aug;7(1-2):141–154. doi: 10.1017/s0952523800011019. [DOI] [PubMed] [Google Scholar]

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