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. 1980 Feb 1;75(2):141–162. doi: 10.1085/jgp.75.2.141

Neurons, potassium, and glia in proximal retina of Necturus

PMCID: PMC2215744  PMID: 6246191

Abstract

Light-evoked K+ flux and intracellular Muller (glial) cell and on/off- neuron responses were recorded from the proximal retina of Necturus in eyecups from which the vitreous was not drained. On/off-responses, probably arising from amacrine cells, showed an initial transient and a sustained component that always exhibited surround antagonism. Muller cell responses were small but otherwise similar to those recorded in eyecups drained of vitreous. The proximal K+ increase and Muller cell responses had identical decay times, and on some occasions the latency and rise time of the K+ increase nearly matched Muller cell responses, indicating that the recorded K+ responses were not always appreciably degraded by electrode "dead space." The spatiotemporal distribution of the K+ increase showed that both diffusion and active reuptake play important roles in K+ clearance. The relationship between on/off-neuron responses and the K+ increase was modelled by assuming that (a) K+ release is positively related to the instantaneous amplitude of the neural response, and (b) K+ accumulating in extracellular space is cleared via mechanisms with approximately exponential time-courses. These two processes were approximated by low-pass filtering the on/off- neuron responses, resulting in modelled responses that match the wave form and time-course of the K+ increase and behave quantitatively like the K+ increase to changes in stimulus intensity and diameter. Thus, on/off-neurons are probably a primary source of the proximal light- evoked K+ increase that depolarizes glial cells to generate the M-wave.

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Selected References

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  1. Burkhardt D. A. Proximal negative response of frog retina. J Neurophysiol. 1970 May;33(3):405–420. doi: 10.1152/jn.1970.33.3.405. [DOI] [PubMed] [Google Scholar]
  2. Cordingley G. E., Somjen G. G. The clearing of excess potassium from extracellular space in spinal cord and cerebral cortex. Brain Res. 1978 Aug 4;151(2):291–306. doi: 10.1016/0006-8993(78)90886-7. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Futamachi K. J., Pedley T. A. Glial cells and extracellular potassium: their relationship in mammalian cortex. Brain Res. 1976 Jun 11;109(2):311–322. doi: 10.1016/0006-8993(76)90532-1. [DOI] [PubMed] [Google Scholar]
  6. Gardner-Medwin A. R., Gibson J. L., Willshaw D. J. The mechanism of potassium dispersal in brain tissue [proceedings]. J Physiol. 1979 Aug;293:37P–38P. [PubMed] [Google Scholar]
  7. Herz A., Zieglgänsberger W., Färber G. Microelectrophoretic studies concerning the spread of glutamic acid and GABA in brain tissue. Exp Brain Res. 1969;9(3):221–235. doi: 10.1007/BF00234456. [DOI] [PubMed] [Google Scholar]
  8. Karwoski C. J., Brukhardt D. A. Ganglion cell responses of the mudpuppy retina to flashing and moving stimuli. Vision Res. 1976;16(12):1483–1495. doi: 10.1016/0042-6989(76)90169-3. [DOI] [PubMed] [Google Scholar]
  9. Karwoski C. J., Proenza L. M. A comparison of the proximal negative response and ganglion cell responses to sinusoidal flicker. Brain Res. 1978 Feb 17;142(1):41–52. doi: 10.1016/0006-8993(78)90175-0. [DOI] [PubMed] [Google Scholar]
  10. Karwoski C. J., Proenza L. M. Hyperpolarizing on/off-responses in mudpuppy retina. Vision Res. 1977;17(1):152–153. doi: 10.1016/0042-6989(77)90214-0. [DOI] [PubMed] [Google Scholar]
  11. Karwoski C. J., Proenza L. M. Light-evoked changes in extracellular potassium concentration in munpuppy retina. Brain Res. 1978 Mar 10;142(3):515–530. doi: 10.1016/0006-8993(78)90913-7. [DOI] [PubMed] [Google Scholar]
  12. Karwoski J., Criswell M. H., Proenza L. M. Laminar separation of light-evoked K+ flux and field potentials in frog retina. Invest Ophthalmol Vis Sci. 1978 Jul;17(7):678–682. [PubMed] [Google Scholar]
  13. Kline R. P., Ripps H., Dowling J. E. Generation of b-wave currents in the skate retina. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5727–5731. doi: 10.1073/pnas.75.11.5727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kuffler S. W., Nicholls J. G., Orkand R. K. Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):768–787. doi: 10.1152/jn.1966.29.4.768. [DOI] [PubMed] [Google Scholar]
  15. Lothman E. W., Somjen G. G. Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord. J Physiol. 1975 Oct;252(1):115–136. doi: 10.1113/jphysiol.1975.sp011137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Matsumoto N. Responses of the amacrine cell to optic nerve stimulation in the frog retina. Vision Res. 1975 Apr;15(4):509–514. doi: 10.1016/0042-6989(75)90028-0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. 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]
  22. Mori S., Miller W. H., Tomita T. Microelectrode study of spreading depression (SD) in frog retina-Müller cell activity and [K+] during SD--. Jpn J Physiol. 1976;26(2):219–233. doi: 10.2170/jjphysiol.26.219. [DOI] [PubMed] [Google Scholar]
  23. Murakami M., Shimoda Y. Identification of amacrine and ganglion cells in the carp retina. J Physiol. 1977 Jan;264(3):801–818. doi: 10.1113/jphysiol.1977.sp011695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Naka K., Otsuka T. Morphological and functional identifications of catfish retinal neurons. II. Morphological identification. J Neurophysiol. 1975 Jan;38(1):72–91. doi: 10.1152/jn.1975.38.1.72. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. 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]
  28. Oakley B., 2nd, Green D. G. Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol. 1976 Sep;39(5):1117–1133. doi: 10.1152/jn.1976.39.5.1117. [DOI] [PubMed] [Google Scholar]
  29. Proenza L. M., Burkhardt D. A. Proximal negative response and retinal sensitivity in the mudpuppy, Necturus maculosus. J Neurophysiol. 1973 May;36(3):502–518. doi: 10.1152/jn.1973.36.3.502. [DOI] [PubMed] [Google Scholar]
  30. Somjen G. G. Extracellular potassium in the mammalian central nervous system. Annu Rev Physiol. 1979;41:159–177. doi: 10.1146/annurev.ph.41.030179.001111. [DOI] [PubMed] [Google Scholar]
  31. Vern B. A., Schuette W. H., Thibault L. E. [K+]o clearance in cortex: a new analytical model. J Neurophysiol. 1977 Sep;40(5):1015–1023. doi: 10.1152/jn.1977.40.5.1015. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Werblin F. S., Dowling J. E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969 May;32(3):339–355. doi: 10.1152/jn.1969.32.3.339. [DOI] [PubMed] [Google Scholar]
  34. Werblin F. S. Regenerative amacrine cell depolarization and formation of on-off ganglion cell response. J Physiol. 1977 Jan;264(3):767–785. doi: 10.1113/jphysiol.1977.sp011693. [DOI] [PMC free article] [PubMed] [Google Scholar]

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