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. 1989 Jan 1;93(1):101–122. doi: 10.1085/jgp.93.1.101

B-wave of the electroretinogram. A reflection of ON bipolar cell activity

PMCID: PMC2216200  PMID: 2915211

Abstract

Light-evoked intraretinal field potentials (electroretinogram, ERG) have been measured simultaneously with extracellular potassium fluxes in the amphibian retina. The application of highly selective pharmacologic agents permitted us to functionally isolate various classes of retinal neurons. It was found that: (a) application of APB (2-amino-4-phosphonobutyrate), which has previously been shown to selectively abolish the light responsiveness of ON bipolar cells, causes a concomitant loss of the ERG b-wave and ON potassium flux. (b) Conversely, PDA (cis 2,3-piperidine-dicarboxylic acid) or KYN (kynurenic acid), which have been reported to suppress the light responses of OFF bipolar, horizontal, and third-order retinal neurons, causes a loss of the ERG d-wave as well as OFF potassium fluxes. The b- wave and ON potassium fluxes, however, remain undiminished. (c) NMA (N- methyl-DL-aspartate) or GLY (glycine), which have been reported to suppress the responses of third-order neurons, do not diminish the b- or d-waves, nor the potassium fluxes at ON or OFF. This leads to the conclusion that the b-wave of the ERG is a result of the light-evoked depolarization of the ON bipolar neurons. This experimental approach has resulted in two further conclusions: (a) that the d-wave is an expression of OFF bipolar and/or horizontal cell depolarization at the termination of illumination and (b) that light-induced increases in extracellular potassium concentration in both the inner (proximal) and outer (distal) retina are the result of ON bipolar cell depolarization.

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Selected References

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  1. Attwell D., Mobbs P., Tessier-Lavigne M., Wilson M. Neurotransmitter-induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. J Physiol. 1987 Jun;387:125–161. doi: 10.1113/jphysiol.1987.sp016567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bonaventure N., Roussel G., Wioland N. Effects of DL-alpha-amino adipic acid on Müller cells in frog and chicken retinae in vivo: relation to ERG b wave, ganglion cell discharge and tectal evoked potentials. Neurosci Lett. 1981 Nov 18;27(1):81–87. doi: 10.1016/0304-3940(81)90209-3. [DOI] [PubMed] [Google Scholar]
  3. Brew H., Attwell D. Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. 1987 Jun 25-Jul 1Nature. 327(6124):707–709. doi: 10.1038/327707a0. [DOI] [PubMed] [Google Scholar]
  4. Brown K. T. The eclectroretinogram: its components and their origins. Vision Res. 1968 Jun;8(6):633–677. doi: 10.1016/0042-6989(68)90041-2. [DOI] [PubMed] [Google Scholar]
  5. Coleman P. A., Massey S. C., Miller R. F. Kynurenic acid distinguishes kainate and quisqualate receptors in the vertebrate retina. Brain Res. 1986 Aug 27;381(1):172–175. doi: 10.1016/0006-8993(86)90708-0. [DOI] [PubMed] [Google Scholar]
  6. Coles J. A., Tsacopoulos M. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol. 1979 May;290(2):525–549. doi: 10.1113/jphysiol.1979.sp012788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dick E., Miller R. F., Bloomfield S. Extracellular K+ activity changes related to electroretinogram components. II. Rabbit (E-type) retinas. J Gen Physiol. 1985 Jun;85(6):911–931. doi: 10.1085/jgp.85.6.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dick E., Miller R. F. Light-evoked potassium activity in mudpuppy retina: its relationship to the b-wave of the electroretinogram. Brain Res. 1978 Oct 13;154(2):388–394. doi: 10.1016/0006-8993(78)90711-4. [DOI] [PubMed] [Google Scholar]
  9. Fisher R. S., Pedley T. A., Prince D. A. Kinetics of potassium movement in norman cortex. Brain Res. 1976 Jan 16;101(2):223–237. doi: 10.1016/0006-8993(76)90265-1. [DOI] [PubMed] [Google Scholar]
  10. Fujimoto M., Tomita T. Field potential induced by injection of potassium ion into the frog retina: a test of current interpretations of the electroretinographic (ERG) b-wave. Brain Res. 1981 Jan 5;204(1):51–64. doi: 10.1016/0006-8993(81)90651-x. [DOI] [PubMed] [Google Scholar]
  11. Granit R. The components of the retinal action potential in mammals and their relation to the discharge in the optic nerve. J Physiol. 1933 Feb 8;77(3):207–239. doi: 10.1113/jphysiol.1933.sp002964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Immel J., Steinberg R. H. Spatial buffering of K+ by the retinal pigment epithelium in frog. J Neurosci. 1986 Nov;6(11):3197–3204. doi: 10.1523/JNEUROSCI.06-11-03197.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kaneko A., Tachibana M. A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. J Physiol. 1985 Jan;358:131–152. doi: 10.1113/jphysiol.1985.sp015544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Karwoski C. J., Newman E. A., Shimazaki H., Proenza L. M. Light-evoked increases in extracellular K+ in the plexiform layers of amphibian retinas. J Gen Physiol. 1985 Aug;86(2):189–213. doi: 10.1085/jgp.86.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Karwoski C. J., Proenza L. M. Neurons, potassium, and glia in proximal retina of Necturus. J Gen Physiol. 1980 Feb;75(2):141–162. doi: 10.1085/jgp.75.2.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kline R. P., Ripps H., Dowling J. E. Light-induced potassium fluxes in the skate retina. Neuroscience. 1985 Jan;14(1):225–235. doi: 10.1016/0306-4522(85)90175-7. [DOI] [PubMed] [Google Scholar]
  17. Knapp A. G., Schiller P. H. The contribution of on-bipolar cells to the electroretinogram of rabbits and monkeys. A study using 2-amino-4-phosphonobutyrate (APB). Vision Res. 1984;24(12):1841–1846. doi: 10.1016/0042-6989(84)90016-6. [DOI] [PubMed] [Google Scholar]
  18. Kondo H., Toyoda J. GABA and glycine effects on the bipolar cells of the carp retina. Vision Res. 1983;23(11):1259–1264. doi: 10.1016/0042-6989(83)90101-3. [DOI] [PubMed] [Google Scholar]
  19. Lux H. D., Neher E. The equilibration time course of (K + ) 0 in cat cortex. Exp Brain Res. 1973 Apr 30;17(2):190–205. doi: 10.1007/BF00235028. [DOI] [PubMed] [Google Scholar]
  20. Massey S. C., Redburn D. A., Crawford M. L. The effects of 2-amino-4-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Res. 1983;23(12):1607–1613. doi: 10.1016/0042-6989(83)90174-8. [DOI] [PubMed] [Google Scholar]
  21. Matsuura T., Miller W. H., Tomita T. Cone-specific c-wave in the turtle retina. Vision Res. 1978;18(7):767–775. doi: 10.1016/0042-6989(78)90115-3. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Miller R. F., Dacheux R., Proenza L. Müller cell depolarization evoked by antidromic optic nerve stimulation. Brain Res. 1977 Jan 31;121(1):162–166. doi: 10.1016/0006-8993(77)90446-2. [DOI] [PubMed] [Google Scholar]
  24. Miller R. F., Dowling J. E. Intracellular responses of the Müller (glial) cells of mudpuppy retina: their relation to b-wave of the electroretinogram. J Neurophysiol. 1970 May;33(3):323–341. doi: 10.1152/jn.1970.33.3.323. [DOI] [PubMed] [Google Scholar]
  25. Miller R. F., Frumkes T. E., Slaughter M., Dacheux R. F. Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. I. Receptors, horizontal cells, bipolars, and G-cells. J Neurophysiol. 1981 Apr;45(4):743–763. doi: 10.1152/jn.1981.45.4.743. [DOI] [PubMed] [Google Scholar]
  26. Miller R. F., Frumkes T. E., Slaughter M., Dacheux R. F. Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. II. Amacrine and ganglion cells. J Neurophysiol. 1981 Apr;45(4):764–782. doi: 10.1152/jn.1981.45.4.764. [DOI] [PubMed] [Google Scholar]
  27. Miller R. F. Role of K + in generation of b-wave of electroretinogram. J Neurophysiol. 1973 Jan;36(1):28–38. doi: 10.1152/jn.1973.36.1.28. [DOI] [PubMed] [Google Scholar]
  28. NOELL W. K. The origin of the electroretinogram. Am J Ophthalmol. 1954 Jul;38(12):78–90. doi: 10.1016/0002-9394(54)90012-4. [DOI] [PubMed] [Google Scholar]
  29. Newman E. A. Current source-density analysis of the b-wave of frog retina. J Neurophysiol. 1980 May;43(5):1355–1366. doi: 10.1152/jn.1980.43.5.1355. [DOI] [PubMed] [Google Scholar]
  30. Newman E. A. High potassium conductance in astrocyte endfeet. Science. 1986 Jul 25;233(4762):453–454. doi: 10.1126/science.3726539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Newman E. A. Membrane physiology of retinal glial (Müller) cells. J Neurosci. 1985 Aug;5(8):2225–2239. doi: 10.1523/JNEUROSCI.05-08-02225.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Newman E. A., Odette L. L. Model of electroretinogram b-wave generation: a test of the K+ hypothesis. J Neurophysiol. 1984 Jan;51(1):164–182. doi: 10.1152/jn.1984.51.1.164. [DOI] [PubMed] [Google Scholar]
  33. Newman E. A. Regional specialization of retinal glial cell membrane. Nature. 1984 May 10;309(5964):155–157. doi: 10.1038/309155a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nicholson C., Phillips J. M., Gardner-Medwin A. R. Diffusion from an iontophoretic point source in the brain: role of tortuosity and volume fraction. Brain Res. 1979 Jun 29;169(3):580–584. doi: 10.1016/0006-8993(79)90408-6. [DOI] [PubMed] [Google Scholar]
  35. Nygaard R. W., Frumkes T. E. LEDs: convenient, inexpensive sources for visual experimentation. Vision Res. 1982;22(4):435–440. doi: 10.1016/0042-6989(82)90190-0. [DOI] [PubMed] [Google Scholar]
  36. Oakley B., 2nd, Flaming D. G., Brown K. T. Effects of the rod receptor potential upon retinal extracellular potassium concentration. J Gen Physiol. 1979 Dec;74(6):713–737. doi: 10.1085/jgp.74.6.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rodieck R. W. Components of the electroretinogram--a reappraisal. Vision Res. 1972 May;12(5):773–780. doi: 10.1016/0042-6989(72)90003-x. [DOI] [PubMed] [Google Scholar]
  38. Shimazaki H., Karwoski C. J., Proenza L. M. Aspartate-induced dissociation of proximal from distal retinal activity in the mudpuppy. Vision Res. 1984;24(6):587–595. doi: 10.1016/0042-6989(84)90113-5. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Slaughter M. M., Miller R. F. An excitatory amino acid antagonist blocks cone input to sign-conserving second-order retinal neurons. Science. 1983 Mar 11;219(4589):1230–1232. doi: 10.1126/science.6131536. [DOI] [PubMed] [Google Scholar]
  41. Slaughter M. M., Miller R. F. Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature. 1983 Jun 9;303(5917):537–538. doi: 10.1038/303537a0. [DOI] [PubMed] [Google Scholar]
  42. Slaughter M. M., Miller R. F. Characterization of an extended glutamate receptor of the on bipolar neuron in the vertebrate retina. J Neurosci. 1985 Jan;5(1):224–233. doi: 10.1523/JNEUROSCI.05-01-00224.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Slaughter M. M., Miller R. F. Identification of a distinct synaptic glutamate receptor on horizontal cells in mudpuppy retina. Nature. 1985 Mar 7;314(6006):96–97. doi: 10.1038/314096a0. [DOI] [PubMed] [Google Scholar]
  44. Slaughter M. M., Miller R. F. The role of excitatory amino acid transmitters in the mudpuppy retina: an analysis with kainic acid and N-methyl aspartate. J Neurosci. 1983 Aug;3(8):1701–1711. doi: 10.1523/JNEUROSCI.03-08-01701.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Steinberg R. H., Oakley B., 2nd, Niemeyer G. Light-evoked changes in [K+]0 in retina of intact cat eye. J Neurophysiol. 1980 Nov;44(5):897–921. doi: 10.1152/jn.1980.44.5.897. [DOI] [PubMed] [Google Scholar]
  46. Szamier R. B., Ripps H., Chappell R. L. Changes in ERG b-wave and Müller cell structure induced by alpha-aminoadipic acid. Neurosci Lett. 1981 Feb 6;21(3):307–312. doi: 10.1016/0304-3940(81)90222-6. [DOI] [PubMed] [Google Scholar]
  47. Tachibana M., Kaneko A. gamma-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proc Natl Acad Sci U S A. 1987 May;84(10):3501–3505. doi: 10.1073/pnas.84.10.3501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tessier-Lavigne M., Attwell D., Mobbs P., Wilson M. Membrane currents in retinal bipolar cells of the axolotl. J Gen Physiol. 1988 Jan;91(1):49–72. doi: 10.1085/jgp.91.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tomita T., Yanagida T. Origins of the ERG waves. Vision Res. 1981;21(11):1703–1707. doi: 10.1016/0042-6989(81)90062-6. [DOI] [PubMed] [Google Scholar]
  50. Witkovsky P., Dudek F. E., Ripps H. Slow PIII component of the carp electroretinogram. J Gen Physiol. 1975 Feb;65(2):119–134. doi: 10.1085/jgp.65.2.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yanagida T., Tomita T. Local potassium concentration changes in the retina and the electroretinographic (ERG) b-wave. Brain Res. 1982 Apr 15;237(2):479–483. doi: 10.1016/0006-8993(82)90459-0. [DOI] [PubMed] [Google Scholar]
  52. Zimmerman R. P., Corfman T. P. A comparison of the effects of isomers of alpha-aminoadipic acid and 2-amino-4-phosphonobutyric acid on the light response of the müller glial cell and the electroretinogram. Neuroscience. 1984 May;12(1):77–84. doi: 10.1016/0306-4522(84)90139-8. [DOI] [PubMed] [Google Scholar]

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