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J Gen Physiol. 1980 February 1; 75(2): 141–162.
PMCID: PMC2215744

Neurons, potassium, and glia in proximal retina of Necturus

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

These references are in PubMed. This may not be the complete list of references from this article.
  • Gardner-Medwin AR, Gibson JL, Willshaw DJ. The mechanism of potassium dispersal in brain tissue [proceedings]. J Physiol. 1979 Aug;293:37P–38P. [PubMed]
  • Nicholson C, Phillips JM, Gardner-Medwin AR. Diffusion from an iontophoretic point source in the brain: role of tortuosity and volume fraction. Brain Res. 1979 Jun 29;169(3):580–584. [PubMed]
  • Burkhardt DA. Proximal negative response of frog retina. J Neurophysiol. 1970 May;33(3):405–420. [PubMed]
  • Cordingley GE, Somjen GG. The clearing of excess potassium from extracellular space in spinal cord and cerebral cortex. Brain Res. 1978 Aug 4;151(2):291–306. [PubMed]
  • Dick E, Miller RF. 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. [PubMed]
  • Fisher RS, Pedley TA, Prince DA. Kinetics of potassium movement in norman cortex. Brain Res. 1976 Jan 16;101(2):223–237. [PubMed]
  • Futamachi KJ, Pedley TA. Glial cells and extracellular potassium: their relationship in mammalian cortex. Brain Res. 1976 Jun 11;109(2):311–322. [PubMed]
  • 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. [PubMed]
  • Karwoski CJ, Brukhardt DA. Ganglion cell responses of the mudpuppy retina to flashing and moving stimuli. Vision Res. 1976;16(12):1483–1495. [PubMed]
  • Karwoski J, Criswell MH, Proenza LM. Laminar separation of light-evoked K+ flux and field potentials in frog retina. Invest Ophthalmol Vis Sci. 1978 Jul;17(7):678–682. [PubMed]
  • Karwoski CJ, Proenza LM. Hyperpolarizing on/off-responses in mudpuppy retina. Vision Res. 1977;17(1):152–153. [PubMed]
  • Karwoski CJ, Proenza LM. A comparison of the proximal negative response and ganglion cell responses to sinusoidal flicker. Brain Res. 1978 Feb 17;142(1):41–52. [PubMed]
  • Karwoski CJ, Proenza LM. Light-evoked changes in extracellular potassium concentration in munpuppy retina. Brain Res. 1978 Mar 10;142(3):515–530. [PubMed]
  • Kline RP, Ripps H, Dowling JE. Generation of b-wave currents in the skate retina. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5727–5731. [PubMed]
  • Kuffler SW, Nicholls JG, Orkand RK. Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):768–787. [PubMed]
  • Lothman EW, Somjen GG. Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord. J Physiol. 1975 Oct;252(1):115–136. [PubMed]
  • Lux HD, Neher E. The equilibration time course of (K + ) 0 in cat cortex. Exp Brain Res. 1973 Apr 30;17(2):190–205. [PubMed]
  • Matsumoto N. Responses of the amacrine cell to optic nerve stimulation in the frog retina. Vision Res. 1975 Apr;15(4):509–514. [PubMed]
  • Matsuura T, Miller WH, Tomita T. Cone-specific c-wave in the turtle retina. Vision Res. 1978;18(7):767–775. [PubMed]
  • Miller RF. Role of K + in generation of b-wave of electroretinogram. J Neurophysiol. 1973 Jan;36(1):28–38. [PubMed]
  • Miller RF, Dacheux RF. 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. [PMC free article] [PubMed]
  • Miller RF, Dowling JE. 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. [PubMed]
  • Mori S, Miller WH, 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. [PubMed]
  • Murakami M, Shimoda Y. Identification of amacrine and ganglion cells in the carp retina. J Physiol. 1977 Jan;264(3):801–818. [PubMed]
  • Naka K, Otsuka T. Morphological and functional identifications of catfish retinal neurons. II. Morphological identification. J Neurophysiol. 1975 Jan;38(1):72–91. [PubMed]
  • Nelson R. A comparison of electrical properties of neurons in Necturus retina. J Neurophysiol. 1973 May;36(3):519–535. [PubMed]
  • Oakley B, 2nd, Flaming DG, Brown KT. Effects of the rod receptor potential upon retinal extracellular potassium concentration. J Gen Physiol. 1979 Dec;74(6):713–737. [PMC free article] [PubMed]
  • Oakley B, 2nd, Green DG. Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol. 1976 Sep;39(5):1117–1133. [PubMed]
  • Proenza LM, Burkhardt DA. Proximal negative response and retinal sensitivity in the mudpuppy, Necturus maculosus. J Neurophysiol. 1973 May;36(3):502–518. [PubMed]
  • Somjen GG. Extracellular potassium in the mammalian central nervous system. Annu Rev Physiol. 1979;41:159–177. [PubMed]
  • Vern BA, Schuette WH, Thibault LE. [K+]o clearance in cortex: a new analytical model. J Neurophysiol. 1977 Sep;40(5):1015–1023. [PubMed]
  • Werblin FS. Regenerative amacrine cell depolarization and formation of on-off ganglion cell response. J Physiol. 1977 Jan;264(3):767–785. [PubMed]
  • Werblin FS, Copenhagen DR. Control of retinal sensitivity. 3. Lateral interactions at the inner plexiform layer. J Gen Physiol. 1974 Jan;63(1):88–110. [PMC free article] [PubMed]
  • Werblin FS, Dowling JE. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969 May;32(3):339–355. [PubMed]

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