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Amacrine-to-amacrine cell inhibition: Spatiotemporal properties of GABA and glycine pathways

Published online by Cambridge University Press:  07 June 2011

XIN CHEN ,
HAIN ANN HSUEH  and
FRANK S. WERBLIN
XIN CHEN
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California
HAIN ANN HSUEH
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California
FRANK S. WERBLIN*
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California
*
*Address correspondence and reprint requests to: Frank S. Werblin, Werblin Lab, University of California, Berkeley, Department of Molecular & Cell Biology, 142 Life Sciences Addition # 3200, Berkeley, CA 94720-3200.
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Abstract

We measured the spatial and temporal properties of GABAergic and glycinergic inhibition to amacrine cells in the whole-mount rabbit retina. The amacrine cells were parsed into two morphological classes: narrow-field cells with processes spreading less than 200 μm and wide-field cells with processes extending more than 300 μm. The inhibition was also parsed into two types: sustained glycine and transient GABA. Narrow-field amacrine cells receive 1) very transient GABAergic inhibition with a fast onset latency of 140 ± 16 ms decaying to 30% of the peak level within 208 ± 27 ms elicited broadly over a lateral distance of up to 1500 μm and 2) sustained glycinergic inhibition with a medium onset latency of 286 ± 23 ms that was elicited over a spatial area often broader than the processes of the narrow-field amacrine cells. Wide-field amacrine cells received sustained glycinergic inhibition but no broad transient GABAergic inhibition. Surprisingly, neither of these amacrine cell classes received sustained local GABAergic inhibition, commonly found in an earlier study of ganglion cells.

Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 3 , May 2011 , pp. 193 - 204
Copyright
Copyright © Cambridge University Press 2011

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References

Baccus, S.A., Olveczky, B.P., Manu, M. & Meister, M. (2008). A retinal circuit that computes object motion. The Journal of Neuroscience 28, 6807–6817.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Volgyi, B. (2004). Function and plasticity of homologous coupling between AII amacrine cells. Vision Research 44, 3297–3306.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Xin, D. (2000). Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. The Journal of Physiology 523(Pt 3), 771–783.CrossRefGoogle ScholarPubMed
Chen, X., Hsueh, H.A., Greenberg, K. & Werblin, F.S. (2010). Three forms of spatial temporal feedforward inhibition are common to different ganglion cell types in rabbit retina. Journal of Neurophysiology 103, 2618–2632.CrossRefGoogle ScholarPubMed
Cook, P.B. & McReynolds, J.S. (1998). Modulation of sustained and transient lateral inhibitory mechanisms in the mudpuppy retina during light adaptation. Journal of Neurophysiology 79, 197–204.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1986) Dopamine: A retinal neuromodulator? Trends in Neurosciences 9, 236–240.CrossRefGoogle Scholar
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. The Journal of Physiology 572, 215–225.CrossRefGoogle Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2010). Interneuron circuits tune inhibition in retinal bipolar cells. Journal of Neurophysiology 103, 25–37.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992 a). Polyaxonal amacrine cells of rabbit retina: Morphology and stratification of PA1 cells. The Journal of Comparative Neurology 316, 391–405.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992 b). Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. The Journal of Comparative Neurology 316, 422–446.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992 c). Polyaxonal amacrine cells of rabbit retina: Size and distribution of PA1 cells. The Journal of Comparative Neurology 316, 406–421.CrossRefGoogle ScholarPubMed
Fried, S.I., Munch, T.A. & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.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
Hsueh, H.A., Molnar, A. & Werblin, F.S. (2008). Amacrine-to-amacrine cell inhibition in the rabbit retina. Journal of Neurophysiology 100, 2077–2088.CrossRefGoogle ScholarPubMed
Ichinose, T. & Lukasiewicz, P.D. (2005). Inner and outer retinal pathways both contribute to surround inhibition of salamander ganglion cells. The Journal of Physiology 565, 517–535.CrossRefGoogle ScholarPubMed
Keeley, P.W. & Reese, B.E. (2010). Morphology of dopaminergic amacrine cells in the mouse retina: Independence from homotypic interactions. The Journal of Comparative Neurology 518, 1220–1231.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D., Eggers, E.D., Sagdullaev, B.T. & McCall, M.A. (2004). GABAC receptor-mediated inhibition in the retina. Vision Research 44, 3289–3296.CrossRefGoogle ScholarPubMed
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photo filled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. The Journal of Comparative Neurology 413, 305–326.3.0.CO;2-E>CrossRefGoogle Scholar
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971–982.CrossRefGoogle ScholarPubMed
Masland, R.H. (2001). The fundamental plan of the retina. Nature Neuroscience 4, 877–886.CrossRefGoogle ScholarPubMed
Molnar, A., Hsueh, H.A., Roska, B. & Werblin, F.S. (2009). Crossover inhibition in the retina: Circuitry that compensates for nonlinear rectifying synaptic transmission. The Journal of computational Neuroscience 27, 569–590.CrossRefGoogle ScholarPubMed
Molnar, A. & Werblin, F. (2007). Inhibitory feedback shapes bipolar cell responses in the rabbit retina. Journal of Neurophysiology 98, 3423–3435.CrossRefGoogle ScholarPubMed
Olveczky, B.P., Baccus, S.A. & Meister, M. (2003). Segregation of object and background motion in the retina. Nature 423, 401–408.CrossRefGoogle ScholarPubMed
Roska, B., Molnar, A. & Werblin, F.S. (2006). Parallel processing in retinal ganglion cells: How integration of space-time patterns of excitation and inhibition form the spiking output. Journal of Neurophysiology 95, 3810–3822.CrossRefGoogle ScholarPubMed
Roska, B. & Werblin, F. (2003). Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nature Neuroscience 6, 600–608.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
Taylor, W.R. (1999). TTX attenuates surround inhibition in rabbit retinal ganglion cells. Visual Neuroscience 16, 285–290.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444–446.CrossRefGoogle ScholarPubMed
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 13250–13263.CrossRefGoogle ScholarPubMed
Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. The Journal of Comparative Neurology 440, 109–125.CrossRefGoogle ScholarPubMed
Volgyi, 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
Werblin, F.S. (2010) Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission. Visual Neuroscience 27, 1–8.CrossRefGoogle ScholarPubMed
Wright, L.L. & Vaney, D.I. (2004). The type 1 polyaxonal amacrine cells of the rabbit retina: A tracer-coupling study. Visual Neuroscience 21, 145–155.CrossRefGoogle ScholarPubMed
Zhang, A.J. & Wu, S.M. (2009). Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic circuitry. The Journal of Neuroscience 29, 789–797.CrossRefGoogle ScholarPubMed
Zhang, A.J. & Wu, S.M. (2010). Responses and receptive fields of amacrine cells and ganglion cells in the salamander retina. Vision Research 50, 614–622.CrossRefGoogle ScholarPubMed
Zhou, Z.J. & Lee, S. (2008). Synaptic physiology of direction selectivity in the retina. The Journal of Physiology 586, 4371–4376.CrossRefGoogle ScholarPubMed