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Synaptic inhibition tunes contrast computation in the retina

Published online by Cambridge University Press:  20 May 2019

Nicholas W. Oesch  and
Jeffrey S. Diamond
Nicholas W. Oesch
Affiliation:
Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892-3701
Jeffrey S. Diamond*
Affiliation:
Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892-3701
*
*Address correspondence to: Jeffrey S. Diamond, Email: diamondj@ninds.nih.gov
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Abstract

Inhibition shapes activity and signal processing in neural networks through numerous mechanisms mediated by many different cell types. Here, we examined how one type of GABAergic interneuron in the retina, the A17 amacrine cell, influences visual information processing. Our results suggest that A17s, which make reciprocal feedback inhibitory synapses onto rod bipolar cell (RBC) synaptic terminals, extend the luminance range over which RBC synapses compute temporal contrast and enhance the reliability of contrast signals over this range. Inhibition from other amacrine cells does not influence these computational features. Although A17-mediated feedback is mediated by both GABAA and GABAC receptors, the latter plays the primary role in extending the range of contrast computation. These results identify specific functions for an inhibitory interneuron subtype, as well as specific synaptic receptors, in a behaviorally relevant neural computation.

Keywords

Amacrine cellWeber contrastRibbon synapseFeedback inhibition
Type
Research Article
Information
Visual Neuroscience , Volume 36 , 2019 , E006
Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

†

Present address: University of California, San Diego, Department of Psychology, Department of Ophthalmology, 9500 Gilman Drive MC#0109, La Jolla, California.

References

Aguilar, M. & Stiles, W. (1954). Saturation of the rod mechanism of the retina at high levels of stimulation. Optica Acta: International Journal of Optics 1, 59–65.CrossRefGoogle Scholar
Berntson, A. & Taylor, W.R. (2000). Response characteristics and receptive field widths of on-bipolar cells in the mouse retina. The Journal of Physiology 524(Pt 3), 879–889.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.CrossRefGoogle ScholarPubMed
Carandini, M. & Heeger, D.J. (2012). Normalization as a canonical neural computation. Nature Reviews Neuroscience 13, 51–62.CrossRefGoogle Scholar
Chávez, A.E. & Diamond, J.S. (2008). Diverse mechanisms underlie glycinergic feedback transmission onto rod bipolar cells in rat retina. Journal of Neuroscience 28, 7919–7928.CrossRefGoogle ScholarPubMed
Chávez, A.E., Grimes, W.N. & Diamond, J.S. (2010). Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina. Journal of Neuroscience 30, 2330–2339.CrossRefGoogle ScholarPubMed
Chávez, A.E., Singer, J.H. & Diamond, J.S. (2006). Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443, 705–708.CrossRefGoogle ScholarPubMed
Dong, C.J. & Hare, W.A. (2003). Temporal modulation of scotopic visual signals by A17 amacrine cells in mammalian retina in vivo. Journal of Neurophysiology 89, 2159–2166.CrossRefGoogle ScholarPubMed
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 2171–2180.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London B Biological Sciences 166, 80–111.Google ScholarPubMed
Eggers, E.D. & Lukasiewicz, P.D. (2006a). GABAA, GABAC and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. The Journal of Physiology 572, 215–225.CrossRefGoogle Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2006b). Receptor and transmitter release properties set the time course of retinal inhibition. Journal of Neuroscience 26, 9413–9425.CrossRefGoogle Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2011). Multiple pathways of inhibition shape bipolar cell responses in the retina. Visual Neuroscience, 28, 95–108.CrossRefGoogle ScholarPubMed
Eggers, E.D., McCall, M.A. & Lukasiewicz, P.D. (2007). Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. The Journal of Physiology 582, 569–582.CrossRefGoogle ScholarPubMed
Engelman, H.S. & MacDermott, A.B. (2004). Presynaptic ionotropic receptors and control of transmitter release. Nature Reviews Neuroscience 5, 135–145.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. (1973). Adaptation and dynamics of cat retinal ganglion cells. The Journal of Physiology 233, 271–309.CrossRefGoogle ScholarPubMed
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in a mammalian retina. Journal of Neurophysiology 83, 1817–1829.CrossRefGoogle Scholar
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 35, 733–747.CrossRefGoogle Scholar
Graydon, C.W., Zhang, J., Oesch, N.W., Sousa, A.A., Leapman, R.D. & Diamond, J.S. (2014). Passive diffusion as a mechanism underlying ribbon synapse vesicle release and resupply. Journal of Neuroscience 34, 8948–8962.CrossRefGoogle ScholarPubMed
Grimes, W.N., Li, W., Chavez, A.E. & Diamond, J.S. (2009). BK channels modulate pre- and postsynaptic signaling at reciprocal synapses in retina. Nature Neuroscience 12, 585–592.CrossRefGoogle ScholarPubMed
Grimes, W.N., Schwartz, G.W. & Rieke, F. (2014). The synaptic and circuit mechanisms underlying a change in spatial encoding in the retina. Neuron 82, 460–473.CrossRefGoogle ScholarPubMed
Grimes, W.N., Zhang, J., Graydon, C.W., Kachar, B. & Diamond, J.S. (2010). Retinal parallel processors: More than 100 independent microcircuits operate within a single interneuron. Neuron 65, 873–885.CrossRefGoogle ScholarPubMed
Grimes, W.N., Zhang, J., Tian, H., Graydon, C.W., Hoon, M., Rieke, F. & Diamond, J.S. (2015). Complex inhibitory microcircuitry regulates retinal signaling near visual threshold. Journal of Neurophysiology 114, 341–353.CrossRefGoogle ScholarPubMed
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 2923–2936.CrossRefGoogle ScholarPubMed
Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. (1994). Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513–515.CrossRefGoogle Scholar
Heidelberger, R. & Matthews, G. (1992). Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. The Journal of Physiology 447, 235–256.CrossRefGoogle ScholarPubMed
Holt, M., Cooke, A., Neef, A. & Lagnado, L. (2004). High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Current Biology 14, 173–183.CrossRefGoogle Scholar
Hong, E.J. & Wilson, R.I. (2013). Olfactory neuroscience: Normalization is the norm. Current Biology 23, R1091–R1093.CrossRefGoogle ScholarPubMed
Jarsky, T., Cembrowski, M., Logan, S.M., Kath, W.L., Riecke, H., Demb, J.B. & Singer, J.H. (2011). A synaptic mechanism for retinal adaptation to luminance and contrast. Journal of Neuroscience 31, 11003–11015.CrossRefGoogle Scholar
Ke, J.B., Wang, Y.V., Borghuis, B.G., Cembrowski, M.S., Riecke, H., Kath, W.L., Demb, J.B. & Singer, J.H. (2014). Adaptation to background light enables contrast coding at rod bipolar cell synapses. Neuron 81, 388–401.CrossRefGoogle ScholarPubMed
Kepecs, A. & Fishell, G. (2014). Interneuron cell types are fit to function. Nature 505, 318–326.CrossRefGoogle Scholar
Kullmann, D.M., Ruiz, A., Rusakov, D.M., Scott, R., Semyanov, A. & Walker, M.C. (2005). Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: Where and why? Progress in Biophysics and Molecular Biology 87, 33–46.CrossRefGoogle Scholar
Mitchell, S.J. & Silver, R.A. (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433–445.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.CrossRefGoogle ScholarPubMed
Nikonov, S.S., Kholodenko, R., Lem, J. & Pugh, E.N. Jr. (2006). Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. The Journal of General Physiology 127, 359–374.CrossRefGoogle Scholar
Oesch, N.W. & Diamond, J.S. (2011). Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nature Neuroscience 14, 1555–1561.CrossRefGoogle ScholarPubMed
Pan, Z.H. & Lipton, S.A. (1995). Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. Journal of Neuroscience 15, 2668–2679.CrossRefGoogle ScholarPubMed
Roux, L. & Buzsaki, G. (2015). Tasks for inhibitory interneurons in intact brain circuits. Neuropharmacology 88, 10–23.CrossRefGoogle ScholarPubMed
Sagdullaev, B.T., McCall, M.A. & Lukasiewicz, P.D. (2006). Presynaptic inhibition modulates spillover, creating distinct dynamic response ranges of sensory output. Neuron 50, 923–935.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263–346.CrossRefGoogle Scholar
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. Journal of Neuroscience 23, 10923–10933.CrossRefGoogle Scholar
Singer, J.H., Lassova, L., Vardi, N. & Diamond, J.S. (2004). Coordinated multivesicular release at a mammalian ribbon synapse. Nature Neuroscience 7, 826–833.CrossRefGoogle Scholar
Sterling, P. & Lampson, L.A. (1986). Molecular specificity of defined types of amacrine synapse in cat retina. Journal of Neuroscience 6, 1314–1324.CrossRefGoogle ScholarPubMed
Veruki, M.L., Zhou, Y., Castilho, A., Morgans, C.W. & Hartveit, E. (2018). Extrasynaptic NMDA receptors on rod pathway amacrine cells: Molecular composition, activation, and signaling. Journal of Neuroscience 39, 627–650.CrossRefGoogle ScholarPubMed
Völgyi, B., Xin, D. & Bloomfield, S.A. (2002). Feedback inhibition in the inner plexiform layer underlies the surround-mediated responses of AII amacrine cells in the mammalian retina. The Journal of Physiology 539, 603–614.CrossRefGoogle ScholarPubMed
von Gersdorff, H. & Matthews, G. (1997). Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. Journal of Neuroscience 17, 1919–1927.CrossRefGoogle Scholar
Weber, E. (1834). De Pulsu, resorptione, auditu et tactu. Annotationes anatomicae et physiologicae. Leipzig: C.F. Koehler.Google Scholar
Whittle, P. (1994). The psychophysics of contrast brightness. In Lightness, Brightness, and Transparency, ed. Lawrence, Gilchrist A., 35–110. Hillsdale, NJ: Erlbaum Associates.Google Scholar
Wilson, N.R., Runyan, C.A., Wang, F.L. & Sur, M. (2012). Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 343–348.CrossRefGoogle ScholarPubMed
Zhang, J., Li, W., Trexler, E.B. & Massey, S.C. (2002). Confocal analysis of reciprocal feedback at rod bipolar terminals in the rabbit retina. Journal of Neuroscience 22, 10871–10882.CrossRefGoogle ScholarPubMed