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K+-dependent Müller cell-generated components of the electroretinogram

Published online by Cambridge University Press:  23 July 2021

Andrey V. Dmitriev Open the ORCID record for Andrey V. Dmitriev [Opens in a new window] ,
Alexander A. Dmitriev  and
Robert A. Linsenmeier
Andrey V. Dmitriev*
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston, Illinois
Alexander A. Dmitriev
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston, Illinois
Robert A. Linsenmeier
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston, Illinois Department of Neurobiology, Northwestern University, Evanston, Illinois Department of Ophthalmology, Northwestern University, Chicago, Illinois
*
Address correspondence to: *Andrey V. Dmitriev, Department of Biomedical Engineering, Northwestern University, 2145 Sheridan Rd, #310, Evanston, IL 60208. E-mail: andrey.dmitriev@northwestern.edu
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Abstract

The electroretinogram (ERG) has been employed for years to collect information about retinal function and pathology. The usefulness of this noninvasive test depends on our understanding of the cell sources that generate the ERG. Important contributors to the ERG are glial Müller cells (MCs), which are capable of generating substantial transretinal potentials in response to light-induced changes in extracellular K+ concentration ([K+]o). For instance, the MCs generate the slow PIII (sPIII) component of the ERG as a reaction to a photoreceptor-induced [K+]o decrease in the subretinal space. Similarly, an increase of [K+]o related to activity of postreceptor retinal neurons also produces transretinal glial currents, which can potentially influence the amplitude and shape of the b-wave, one of the most frequently analyzed ERG components. Although it is well documented that the majority of the b-wave originates from On-bipolar cells, some contribution from MCs was suggested many years ago and has never been experimentally rejected. In this work, detailed information about light-evoked [K+]o changes in the isolated mouse retina was collected and then analyzed with a relatively simple linear electrical model of MCs. The results demonstrate that the cornea-positive potential generated by MCs is too small to contribute noticeably to the b-wave. The analysis also explains why MCs produce the large cornea-negative sPIII subcomponent of the ERG, but no substantial cornea-positive potential.

Keywords

Müller cellselectroretinogramretinaK+-selective microelectrodescomputer simulation

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Type
Research Article
Information
Visual Neuroscience , Volume 38 , 2021 , E010
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© The Author(s), 2021. Published by Cambridge University Press

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References

Berger, A., Cavallero, S., Dominguez, E., Barbe, P., Simonutti, M., Sahel, J.-A., Sennlaub, F., Raoul, W., Paques, M. & Bemelmans, A.-P. (2014). Spectral-domain optical coherence tomography of the rodent eye: Highlighting layers of the outer retina using signal averaging and comparison with histology. PLoS One 9, e96494.CrossRefGoogle ScholarPubMed
Bolnick, D.A., Walter, A.E. & Sillman, A.J. (1979). Barium suppresses slow PIII in perfused bullfrog retina. Vision Research 19, 1117–1119.CrossRefGoogle ScholarPubMed
Brew, H., Gray, P.T., Mobbs, P. & Attwell, D. (1986). Endfeet of retinal glial cells have higher densities of ion channels that mediate K+ buffering. Nature 324, 466.CrossRefGoogle ScholarPubMed
Bringmann, A., Pannicke, T., Grosche, J., Francke, M., Wiedemann, P., Skatchkov, S.N., Osborne, N.N. & Reichenbach, A. (2006). Müller cells in the healthy and diseased retina. Progress in Retinal and Eye Research 25, 397–424.CrossRefGoogle ScholarPubMed
Brown, K.T. (1968). The electroretinogram: Its components and their origins. Vision Research 8, 633–677.CrossRefGoogle ScholarPubMed
Bykov, K., Dmitriev, A. & Skachkov, S. (1981). Relationship between photoinduced changes in the intercellular concentration of potassium ions and transretinal potential generation by the Muller cells of the retina. Biofizika 26, 104.Google ScholarPubMed
Chao, T., Grosche, J., Biedermann, B., Francke, M., Pannicke, T., Reichelt, W., Wulst, M., Muhle, C., Pritz-Hohmeier, S. & Kuhrt, H. (1997). Comparative studies on mammalian Muller (retinal glial) cells. Journal of Neurocytology 26, 439–454.CrossRefGoogle ScholarPubMed
Coleman, P.A., Carras, P.L. & Miller, R.F. (1987). Barium reverses the transretinal potassium gradient of the amphibian retina. Neuroscience Letters 80, 61–65.CrossRefGoogle ScholarPubMed
Dick, E. & Miller, R.F. (1985). Extracellular K+ activity changes related to electroretinogram components. I. Amphibian (I-type) retinas. The Journal of General Physiology 85, 885–909.CrossRefGoogle ScholarPubMed
Dick, E., Miller, R.F. & Bloomfield, S. (1985). Extracellular K+ activity changes related to electroretinogram components. II. Rabbit (E-type) retinas. The Journal of General Physiology 85, 911–931.CrossRefGoogle ScholarPubMed
Dmitriev, A., Bykov, K. & Gavrikov, K. (1988). Light-induced hyperpolarization of glial Müllerian cells in the frog retina. Sensornye Sistemy 2, 17–26.Google Scholar
Dmitriev, A., Pignatelli, A. & Piccolino, M. (1999). Resistance of retinal extracellular space to Ca2+ level decrease: Implications for the synaptic effects of divalent cations. Journal of Neurophysiology 82, 283–289.CrossRefGoogle ScholarPubMed
Dmitriev, A.V., Gavrikov, K.E. & Mangel, S.C. (2012). GABA‐mediated spatial and temporal asymmetries that contribute to the directionally selective light responses of starburst amacrine cells in retina. The Journal of Physiology 590, 1699–1720.CrossRefGoogle ScholarPubMed
Dmitriev, A.V., Henderson, D. & Linsenmeier, R.A. (2016). Light-induced pH changes in the intact retinae of normal and early diabetic rats. Experimental Eye Research 145, 148–157.CrossRefGoogle ScholarPubMed
Dysli, C., Enzmann, V., Sznitman, R. & Zinkernagel, M.S. (2015). Quantitative analysis of mouse retinal layers using automated segmentation of spectral domain optical coherence tomography images. Translational Vision Science & Technology 4, 9–9.CrossRefGoogle ScholarPubMed
Eberhardt, W. & Reichenbach, A. (1987). Spatial buffering of potassium by retinal Müller (glial) cells of various morphologies calculated by a model. Neuroscience 22, 687–696.CrossRefGoogle ScholarPubMed
Faber, D.S. (1969). Analysis of the Slow Transretinal Potentials in Response to Light (PhD dissertation). Buffalo: State University of New York at Buffalo.Google Scholar
Ferduson, L.R., Dominguez, J.M. II, Balaiya, S., Grover, S. & Chalam, K.V. (2013). Retinal thickness normative data in wild-type mice using customized miniature SD-OCT. PLoS One 8, e67265.CrossRefGoogle Scholar
Ferguson, L.R., Grover, S., IIDominguez, J.M., Balaiya, S. & Chalam, K.V. (2014). Retinal thickness measurement obtained with spectral domain optical coherence tomography assisted optical biopsy accurately correlates with ex vivo histology. PLoS One 9, e111203.CrossRefGoogle ScholarPubMed
Gurevich, L. & Slaughter, M.M. (1993). Comparison of the waveforms of the ON bipolar neuron and the b-wave of the electroretinogram. Vision Research 33, 2431–2435.CrossRefGoogle ScholarPubMed
Hanitzsch, R. (1973). Intraretinal isolation of PIII subcomponents in the isolated rabbit retina after treatment with sodium aspartate. Vision Research 13, 2093–2102.CrossRefGoogle Scholar
Hu, K.G. & Marmor, M.F. (1984). Selective actions of barium on thec-wave and slow negative potential of the rabbit eye. Vision Research 24, 1153–1156.CrossRefGoogle ScholarPubMed
Karowski, C. & Proenza, L.M. (1977). Relationship between Muller cell responses, a local transretinal potential, and potassium flux. Journal of Neurophysiology 40, 244–259.CrossRefGoogle ScholarPubMed
Karwoski, C.J., Frambach, D. & Proenza, L.M. (1985). Laminar profile of resistivity in frog retina. Journal of Neurophysiology 54, 1607–1619.CrossRefGoogle ScholarPubMed
Karwoski, C.J., Lu, H.-K. & Newman, E.A. (1989). Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells. Science (New York, N.Y.) 244, 578.CrossRefGoogle ScholarPubMed
Karwoski, C.J. & Proenza, L.M. (1978). Light-evoked changes in extracellular potassium concentration in mudpuppy retina. Brain Research 142, 515–530.CrossRefGoogle Scholar
Katz, B.J., Wen, R., Zheng, J., Xu, Z. & Oakley, B. (1991). M-wave of the toad electroretinogram. Journal of Neurophysiology 66, 1927–1940.CrossRefGoogle ScholarPubMed
Kline, R.P., Ripps, H. & Dowling, J.E. (1978). Generation of b-wave currents in the skate retina. Proceedings of the National Academy of Sciences 75, 5727–5731.CrossRefGoogle ScholarPubMed
Kofuji, P., Ceelen, P., Zahs, K.R., Surbeck, L.W., Lester, H.A. & Newman, E.A. (2000). Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. The Journal of Neuroscience 20, 5733–5740.CrossRefGoogle ScholarPubMed
Matsuura, T. (1984). Effects of barium on separately recorded fast and slow PIII responses in bullfrog retina. Experientia 40, 817–819.CrossRefGoogle ScholarPubMed
Newman, E. & Reichenbach, A. (1996). The Müller cell: A functional element of the retina. Trends in Neurosciences 19, 307–312.CrossRefGoogle ScholarPubMed
Newman, E.A. (1984). Regional specialization of retinal glial cell membrane. Nature 309, 155.CrossRefGoogle ScholarPubMed
Newman, E.A. (1985). Membrane physiology of retinal glial (Muller) cells. Journal of Neuroscience 5, 2225–2239.CrossRefGoogle ScholarPubMed
Newman, E.A. (1987). Distribution of potassium conductance in mammalian Muller (glial) cells: A comparative study. The Journal of Neuroscience 7, 2423–2432.Google ScholarPubMed
Newman, E.A. (1993). Inward-rectifying potassium channels in retinal glial (Muller) cells. Journal of Neuroscience 13, 3333–3345.CrossRefGoogle ScholarPubMed
Newman, E.A. & Odette, L.L. (1984). Model of electroretinogram b-wave generation: A test of the K+ hypothesis. Journal of Neurophysiology 51, 164–182.CrossRefGoogle ScholarPubMed
Nicholson, C. & Phillips, J. (1981). Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum. The Journal of Physiology 321, 225–257.CrossRefGoogle ScholarPubMed
Nicholson, C. & Rice, M.E. (1991). Diffusion of ions and transmitters in the brain cell microenvironment. In Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission, eds. Fuxe, K. & Agnati, L.F., pp. 279–294. New York: Raven Press.Google Scholar
Oakley, B. & Green, D.G. (1976). Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. Journal of Neurophysiology 39, 1117–1133.CrossRefGoogle ScholarPubMed
Rasmussen, K. (1973). A morphometric study of the Müller cells, their nuclei and mitochondria, in the rat retina. Journal of Ultrastructure Research 44, 96–112.CrossRefGoogle ScholarPubMed
Reichelt, W., Müller, T., Pastor, A., Pannicke, T., Orkand, P., Kettenmann, H. & Schnitzer, J. (1993). Patch-clamp recordings from Müller (glial) cell endfeet in the intact isolated retina and acutely isolated Müller cells of mouse and Guinea-pig. Neuroscience 57, 599–613.CrossRefGoogle ScholarPubMed
Sieving, P.A., Frishman, L.J. & Steinberg, R. (1986). M-wave of proximal retina in cat. Journal of Neurophysiology 56, 1039–1048.CrossRefGoogle ScholarPubMed
Skatchkov, S., Krušek, J., Reichenbach, A. & Orkand, R. (1999). Potassium buffering by Müller cells isolated from the center and periphery of the frog retina. Glia 27, 171–180.3.0.CO;2-F>CrossRefGoogle Scholar
Skatchkov, S.N., Vyklicky, L. & Orkand, R.K. (1995). Potassium currents in endfeet of isolated Müller cells from the frog retina. Glia 15, 54–64.CrossRefGoogle ScholarPubMed
Steinberg, R., Oakley, B.2nd & Niemeyer, G. (1980). Light-evoked changes in [K+] 0 in retina of intact cat eye. Journal of Neurophysiology 44, 897–921.CrossRefGoogle Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B-wave of the electroretinogram. A reflection of ON bipolar cell activity. The Journal of General Physiology 93, 101–122.CrossRefGoogle Scholar
Tomita, T. (1976). Electrophysiological studies of retinal cell function (proctor medal lecture). Investigative Ophthalmology 15, 171–187.Google Scholar
Wen, R. & Oakley, B. (1990). K(+)-evoked Müller cell depolarization generates b-wave of electroretinogram in toad retina. Proceedings of the National Academy of Sciences 87, 2117–2121.CrossRefGoogle ScholarPubMed
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.CrossRefGoogle ScholarPubMed
Witkovsky, P., Dudek, F. & Ripps, H. (1975). Slow PIII component of the carp electroretinogram. The Journal of General Physiology 65, 119–134.CrossRefGoogle ScholarPubMed
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