Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T19:36:31.916Z Has data issue: false hasContentIssue false
  • English
  • Français

Inhibitory components of retinal bipolar cell receptive fields are differentially modulated by dopamine D1 receptors

Published online by Cambridge University Press:  12 February 2020

Reece E. Mazade  and
Erika D. Eggers Open the ORCID record for Erika D. Eggers [Opens in a new window]
Reece E. Mazade
Affiliation:
Departments of Physiology and Biomedical Engineering, University of Arizona, Tucson, Arizona
Erika D. Eggers*
Affiliation:
Departments of Physiology and Biomedical Engineering, University of Arizona, Tucson, Arizona
*
*Address correspondence to: Erika D. Eggers, Email: eeggers@u.arizona.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

During adaptation to an increase in environmental luminance, retinal signaling adjustments are mediated by the neuromodulator dopamine. Retinal dopamine is released with light and can affect center-surround receptive fields, the coupling state between neurons, and inhibitory pathways through inhibitory receptors and neurotransmitter release. While the inhibitory receptive field surround of bipolar cells becomes narrower and weaker during light adaptation, it is unknown how dopamine affects bipolar cell surrounds. If dopamine and light have similar effects, it would suggest that dopamine could be a mechanism for light-adapted changes. We tested the hypothesis that dopamine D1 receptor activation is sufficient to elicit the magnitude of light-adapted reductions in inhibitory bipolar cell surrounds. Surrounds were measured from OFF bipolar cells in dark-adapted mouse retinas while stimulating D1 receptors, which are located on bipolar, horizontal, and inhibitory amacrine cells. The D1 agonist SKF-38393 narrowed and weakened OFF bipolar cell inhibitory receptive fields but not to the same extent as with light adaptation. However, the receptive field surround reductions differed between the glycinergic and GABAergic components of the receptive field. GABAergic inhibitory strength was reduced only at the edges of the surround, while glycinergic inhibitory strength was reduced across the whole receptive field. These results expand the role of retinal dopamine to include modulation of bipolar cell receptive field surrounds. Additionally, our results suggest that D1 receptor pathways may be a mechanism for the light-adapted weakening of glycinergic surround inputs and the furthest wide-field GABAergic inputs to bipolar cells. However, remaining differences between light-adapted and D1 receptor–activated inhibition demonstrate that non-D1 receptor mechanisms are necessary to elicit the full effect of light adaptation on inhibitory surrounds.

Keywords

Bipolar cellGABAGlycineAmacrine cellLuminance
Type
Research Article
Information
Visual Neuroscience , Volume 37 , 2020 , E01
Copyright
Copyright © Cambridge University Press 2020 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Current address: Department of Biological and Vision Sciences, Alonso Laboratory, State University of New York College of Optometry, 33 W 42nd St., New York, New York.

References

Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A. & Robbins, J.T. (2000). The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513–523.CrossRefGoogle Scholar
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat’s retina during dark adaptation. Journal of Physiology 137, 338–354.CrossRefGoogle ScholarPubMed
Bauer, B., Ehinger, B. & Aberg, L. (1980). [3H]-dopamine release from the rabbit retina. Albrecht Von Graefes Archiv fuer Klinische und Experimentelle Ophthalmologie 215, 71–78.CrossRefGoogle ScholarPubMed
Bloomfield, S.A., Xin, D. & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565–576.CrossRefGoogle ScholarPubMed
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization. Brain Research 482, 164–168.CrossRefGoogle ScholarPubMed
Borghuis, B.G., Ratliff, C.P. & Smith, R.G. (2018). Impact of light-adaptive mechanisms on mammalian retinal visual encoding at high light levels. Journal of Neurophysiology 119, 1437–1449.CrossRefGoogle ScholarPubMed
Brainard, D.H. (1997). The psychophysics toolbox. Spatial Vision 10, 433–436.CrossRefGoogle ScholarPubMed
Bu, J.Y., Li, H., Gong, H.Q., Liang, P.J. & Zhang, P.M. (2014). Gap junction permeability modulated by dopamine exerts effects on spatial and temporal correlation of retinal ganglion cells’ firing activities. Journal of Computational Neuroscience 36, 67–79.CrossRefGoogle ScholarPubMed
Buldyrev, I. & Taylor, W.R. (2013). Inhibitory mechanisms that generate centre and surround properties in ON and OFF brisk-sustained ganglion cells in the rabbit retina. Journal of Physiology 591, 303–325.CrossRefGoogle ScholarPubMed
Calaza, K.C., de Mello, F.G. & Gardino, P.F. (2001). GABA release induced by aspartate-mediated activation of NMDA receptors is modulated by dopamine in a selective subpopulation of amacrine cells. Journal of Neurocytology 30, 181–193.CrossRefGoogle Scholar
Chaffiol, A., Ishii, M., Cao, Y. & Mangel, S.C. (2017). Dopamine regulation of GABAA receptors contributes to light/dark modulation of the ON-cone bipolar cell receptive field surround in the retina. Current Biology 27, 2600–2609.e4.CrossRefGoogle ScholarPubMed
Chichilnisky, E.J. & Kalmar, R.S. (2002). Functional asymmetries in ON and OFF ganglion cells of primate retina. Journal of Neuroscience 22, 2737–2747.CrossRefGoogle ScholarPubMed
Cohen, A.I., Todd, R.D., Harmon, S. & O’Malley, K.L. (1992). Photoreceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proceedings of the National Academy of Sciences of the United States of America 89, 12093–12097.CrossRefGoogle ScholarPubMed
Dedek, K., Pandarinath, C., Alam, N.M., Wellershaus, K., Schubert, T., Willecke, K., Prusky, G.T., Weiler, R. & Nirenberg, S. (2008). Ganglion cell adaptability: Does the coupling of horizontal cells play a role? PLoS One 3, e1714.CrossRefGoogle ScholarPubMed
Dong, C.J. & McReynolds, J.S. (1991). The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina. Journal of Physiology 440, 291–309.CrossRefGoogle ScholarPubMed
Doyle, S.E., Grace, M.S., McIvor, W. & Menaker, M. (2002). Circadian rhythms of dopamine in mouse retina: The role of melatonin. Visual Neuroscience 19, 593–601.CrossRefGoogle ScholarPubMed
Dunn, F.A., Doan, T., Sampath, A.P. & Rieke, F. (2006). Controlling the gain of rod-mediated signals in the mammalian retina. Journal of Neuroscience 26, 3959–3970.CrossRefGoogle ScholarPubMed
Dunn, F.A., Lankheet, M.J. & Rieke, F. (2007). Light adaptation in cone vision involves switching between receptor and post-receptor sites. Nature 449, 603–606.CrossRefGoogle ScholarPubMed
Eggers, E.D. & Lukasiewicz, P.D. (2006). GABA(A), GABA(C) and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. Journal of Physiology 572, 215–225.CrossRefGoogle ScholarPubMed
Eggers, E.D., Mazade, R.E. & Klein, J.S. (2013). Inhibition to retinal rod bipolar cells is regulated by light levels. Journal of Neurophysiology 110, 153–161.CrossRefGoogle ScholarPubMed
Eggers, E.D., McCall, M.A. & Lukasiewicz, P.D. (2007). Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. Journal of Physiology 582, 569–582.CrossRefGoogle ScholarPubMed
Falch, E., Hedegaard, A., Nielsen, L., Jensen, B.R., Hjeds, H. & Krogsgaard-Larsen, P. (1986). Comparative stereostructure-activity studies on GABAA and GABAB receptor sites and GABA uptake using rat brain membrane preparations. Journal of Neurochemistry 47, 898–903.CrossRefGoogle ScholarPubMed
Farrow, K., Teixeira, M., Szikra, T., Viney, T.J., Balint, K., Yonehara, K. & Roska, B. (2013). Ambient illumination toggles a neuronal circuit switch in the retina and visual perception at cone threshold. Neuron 78, 325–338.CrossRefGoogle ScholarPubMed
Farshi, P., Fyk-Kolodziej, B., Krolewski, D.M., Walker, P.D. & Ichinose, T. (2016). Dopamine D1 receptor expression is bipolar cell type-specific in the mouse retina. Journal of Comparative Neurology 524, 2059–2079.CrossRefGoogle ScholarPubMed
Feigenspan, A. & Bormann, J. (1994a). Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proceedings of the National Academy of Sciences of the United States of America 91, 10893–10897.CrossRefGoogle Scholar
Feigenspan, A. & Bormann, J. (1994b). Modulation of GABAC receptors in rat retinal bipolar cells by protein kinase C. Journal of Physiology 481(Pt. 2), 325–330.CrossRefGoogle Scholar
Flores-Herr, N., Protti, D.A. & Wassle, H. (2001). Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. Journal of Neuroscience 21, 4852–4863.CrossRefGoogle ScholarPubMed
Ghosh, K.K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wassle, H. (2004). Types of bipolar cells in the mouse retina. Journal of Comparative Neurology 469, 70–82.CrossRefGoogle ScholarPubMed
Godley, B.F. & Wurtman, R.J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: Effect of light stimulation. Brain Research 452, 393–395.CrossRefGoogle ScholarPubMed
Graydon, C.W., Lieberman, E.E., Rho, N., Briggman, K.L., Singer, J.H. & Diamond, J.S. (2018). Synaptic transfer between rod and cone pathways mediated by AII amacrine cells in the mouse retina. Current Biology 28, 2739–2751 e2733.CrossRefGoogle ScholarPubMed
Green, D.G., Dowling, J.E., Siegel, I.M. & Ripps, H. (1975). Retinal mechanisms of visual adaptation in the skate. The Journal of General Physiology 65, 483–502.CrossRefGoogle ScholarPubMed
Green, D.G. & Powers, M.K. (1982). Mechanisms of light adaptation in rat retina. Vision Research 22, 209–216.CrossRefGoogle ScholarPubMed
Hampson, E.C., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.CrossRefGoogle ScholarPubMed
Haverkamp, S., Wassle, H., Duebel, J., Kuner, T., Augustine, G.J., Feng, G. & Euler, T. (2005). The primordial, blue-cone color system of the mouse retina. Journal of Neuroscience 25, 5438–5445.CrossRefGoogle ScholarPubMed
Hu, E.H., Pan, F., Volgyi, B. & Bloomfield, S.A. (2010). Light increases the gap junctional coupling of retinal ganglion cells. Journal of Physiology 588, 4145–4163.CrossRefGoogle ScholarPubMed
Ichinose, T. & Lukasiewicz, P.D. (2007). Ambient light regulates sodium channel activity to dynamically control retinal signaling. Journal of Neuroscience 27, 4756–4764.CrossRefGoogle ScholarPubMed
Jackson, C.R., Ruan, G.X., Aseem, F., Abey, J., Gamble, K., Stanwood, G., Palmiter, R.D., Iuvone, P.M. & McMahon, D.G. (2012). Retinal dopamine mediates multiple dimensions of light-adapted vision. Journal of Neuroscience 32, 9359–9368.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1989). Mechanism and site of action of a dopamine D1 antagonist in the rabbit retina. Visual Neuroscience 3, 573–585.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1991). Involvement of glycinergic neurons in the diminished surround activity of ganglion cells in the dark-adapted rabbit retina. Visual Neuroscience 6, 43–53.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1992). Effects of the dopamine antagonist (+)-SCH 23390 on intracellularly recorded responses of ganglion cells in the rabbit retina. Visual Neuroscience 8, 463–467.CrossRefGoogle ScholarPubMed
Jensen, R.J. & Daw, N.W. (1984). Effects of dopamine antagonists on receptive fields of brisk cells and directionally selective cells in the rabbit retina. Journal of Neuroscience 4, 2972–2985.CrossRefGoogle ScholarPubMed
Jensen, R.J. & Daw, N.W. (1986). Effects of dopamine and its agonists and antagonists on the receptive field properties of ganglion cells in the rabbit retina. Neuroscience 17, 837–855.CrossRefGoogle ScholarPubMed
Kato, S., Negishi, K. & Teranishi, T. (1985). Dopamine inhibits calcium-independent gamma-[3H]aminobutyric acid release induced by kainate and high K+ in the fish retina. Journal of Neurochemistry 44, 893–899.CrossRefGoogle Scholar
Kothmann, W.W., Massey, S.C. & O’Brien, J. (2009). Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. Journal of Neuroscience 29, 14903–14911.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the United States of America 82, 3025–3029.CrossRefGoogle ScholarPubMed
Lee, S.C., Meyer, A., Schubert, T., Huser, L., Dedek, K. & Haverkamp, S. (2015). Morphology and connectivity of the small bistratified A8 amacrine cell in the mouse retina. Journal of Comparative Neurology 523, 1529–1547.CrossRefGoogle ScholarPubMed
Li, H., Zhang, Z., Blackburn, M.R., Wang, S.W., Ribelayga, C.P. & O’Brien, J. (2013). Adenosine and dopamine receptors coregulate photoreceptor coupling via gap junction phosphorylation in mouse retina. Journal of Neuroscience 33, 3135–3150.CrossRefGoogle ScholarPubMed
Liu, X., Grove, J.C., Hirano, A.A., Brecha, N.C. & Barnes, S. (2016). Dopamine D1 receptor modulation of calcium channel currents in horizontal cells of mouse retina. Journal of Neurophysiology 116, 686–697.CrossRefGoogle ScholarPubMed
Maguire, G. & Hamasaki, D.I. (1994). The retinal dopamine network alters the adaptational properties of retinal ganglion cells in the cat. Journal of Neurophysiology 72, 730–741.CrossRefGoogle ScholarPubMed
Maguire, G.W. & Smith, E.L. 3rd (1985). Cat retinal ganglion cell receptive-field alterations after 6-hydroxydopamine induced dopaminergic amacrine cell lesions. Journal of Neurophysiology 53, 1431–1443.CrossRefGoogle ScholarPubMed
Mazade, R., Jin, J., Pons, C. & Alonso, J.M. (2019a). Functional specialization of ON and OFF cortical pathways for global-slow and local-fast vision. Cell Reports 27, 2881–2894.e5.CrossRefGoogle Scholar
Mazade, R.E. & Eggers, E.D. (2013). Light adaptation alters the source of inhibition to the mouse retinal OFF pathway. Journal of Neurophysiology 110, 2113–2128.CrossRefGoogle ScholarPubMed
Mazade, R.E. & Eggers, E.D. (2016). Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling. Journal of Neurophysiology 115, 2761–2778.CrossRefGoogle ScholarPubMed
Mazade, R.E., Flood, M.D. & Eggers, E.D. (2019b). Dopamine D1 receptor activation reduces local inner retinal inhibition to light-adapted levels. Journal of Neurophysiology 121, 1232–1243.CrossRefGoogle Scholar
Merwine, D.K., Amthor, F.R. & Grzywacz, N.M. (1995). Interaction between center and surround in rabbit retinal ganglion cells. Journal of Neurophysiology 73, 1547–1567.CrossRefGoogle ScholarPubMed
Naka, K.I., Chan, R.Y. & Yasui, S. (1979). Adaptation in catfish retina. Journal of Neurophysiology 42, 441–454.CrossRefGoogle ScholarPubMed
Neal, M., Cunningham, J. & Matthews, K. (1998). Selective release of nitric oxide from retinal amacrine and bipolar cells. Investigative Ophthalmology & Visual Science 39, 850–853.Google ScholarPubMed
Nguyen-Legros, J., Simon, A., Caille, I. & Bloch, B. (1997). Immunocytochemical localization of dopamine D1 receptors in the retina of mammals. Visual Neuroscience 14, 545–551.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J., Versaux-Botteri, C. & Vernier, P. (1999). Dopamine receptor localization in the mammalian retina. Molecular Neurobiology 19, 181–204.CrossRefGoogle ScholarPubMed
O’Brien, D.R. & Dowling, J.E. (1985). Dopaminergic regulation of GABA release from the intact goldfish retina. Brain Research 360, 41–50.CrossRefGoogle ScholarPubMed
Page-McCaw, P.S., Chung, S.C., Muto, A., Roeser, T., Staub, W., Finger-Baier, K.C., Korenbrot, J.I. & Baier, H. (2004). Retinal network adaptation to bright light requires tyrosinase. Nature Neuroscience 7, 1329–1336.CrossRefGoogle ScholarPubMed
Protti, D.A., Di Marco, S., Huang, J.Y., Vonhoff, C.R., Nguyen, V. & Solomon, S.G. (2014). Inner retinal inhibition shapes the receptive field of retinal ganglion cells in primate. Journal of Physiology 592, 49–65.CrossRefGoogle ScholarPubMed
Pycock, C.J. & Smith, L.F. (1983). Interactions of dopamine and the release of [3H]-taurine and [3H]-glycine from the isolated retina of the rat. British Journal of Pharmacology 78, 395–404.CrossRefGoogle Scholar
Ravi, S., Ahn, D., Greschner, M., Chichilnisky, E.J. & Field, G.D. (2018). Pathway-specific asymmetries between ON and OFF visual signals. Journal of Neuroscience 38, 9728–9740.CrossRefGoogle ScholarPubMed
Ribelayga, C., Cao, Y. & Mangel, S.C. (2008). The circadian clock in the retina controls rod-cone coupling. Neuron 59, 790–801.CrossRefGoogle ScholarPubMed
Russell, T.L. & Werblin, F.S. (2010). Retinal synaptic pathways underlying the response of the rabbit local edge detector. Journal of Neurophysiology 103, 2757–2769.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal and Eye Research 3, 263–346.CrossRefGoogle Scholar
Stroh, S., Puller, C., Swirski, S., Holzel, M.B., van der Linde, L.I.S., Segelken, J., Schultz, K., Block, C., Monyer, H., Willecke, K., Weiler, R., Greschner, M., Janssen-Bienhold, U. & Dedek, K. (2018). Eliminating glutamatergic input onto horizontal cells changes the dynamic range and receptive field organization of mouse retinal ganglion cells. Journal of Neuroscience 38, 2015–2028.CrossRefGoogle ScholarPubMed
Tamura, T., Nakatani, K. & Yau, K.W. (1991). Calcium feedback and sensitivity regulation in primate rods. The Journal of General Physiology 98, 95–130.CrossRefGoogle ScholarPubMed
Troy, J.B., Bohnsack, D.L. & Diller, L.C. (1999). Spatial properties of the cat X-cell receptive field as a function of mean light level. Visual Neuroscience 16, 1089–1104.CrossRefGoogle Scholar
Tsukamoto, Y. & Omi, N. (2017). Classification of mouse retinal bipolar cells: Type-specific connectivity with special reference to rod-driven AII amacrine pathways. Frontiers in Neuroanatomy 11, 92.CrossRefGoogle ScholarPubMed
Veruki, M.L., Oltedal, L. & Hartveit, E. (2010). Electrical coupling and passive membrane properties of AII amacrine cells. Journal of Neurophysiology 103, 1456–1466.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Wassle, H. (1996). Immunohistochemical localization of dopamine D1 receptors in rat retina. European Journal of Neuroscience 8, 2286–2297.CrossRefGoogle ScholarPubMed
Wilcox, W.W. (1932). The basis of the dependence of visual acuity on illumination. Proceedings of the National Academy of Sciences of the United States of America 18, 47–56.CrossRefGoogle ScholarPubMed
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 17–40.CrossRefGoogle ScholarPubMed
Woodruff, M.L., Janisch, K.M., Peshenko, I.V., Dizhoor, A.M., Tsang, S.H. & Fain, G.L. (2008). Modulation of phosphodiesterase6 turnoff during background illumination in mouse rod photoreceptors. Journal of Neuroscience 28, 2064–2074.CrossRefGoogle ScholarPubMed
Xia, X.B. & Mills, S.L. (2004). Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina. Visual Neuroscience 21, 791–805.CrossRefGoogle ScholarPubMed
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. Journal of Comparative Neurology 383, 512–528.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Xin, D. & Bloomfield, S.A. (1999a). Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Visual Neuroscience 16, 653–665.CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (1999b). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 75–87.3.0.CO;2-D>CrossRefGoogle Scholar
Yadav, S.C., Tetenborg, S. & Dedek, K. (2019). Gap junctions in A8 amacrine cells are made of Connexin36 but are differently regulated than gap junctions in AII amacrine cells. Frontiers in Molecular Neuroscience 12, 99.CrossRefGoogle ScholarPubMed
Yang, J., Pahng, J. & Wang, G.Y. (2013). Dopamine modulates the off pathway in light-adapted mouse retina. Journal of Neuroscience Research 91, 138–150.Google ScholarPubMed