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Functional polarity of dendrites and axons of primate A1 amacrine cells

Published online by Cambridge University Press:  29 May 2007

CHRISTOPHER M. DAVENPORT ,
PETER B. DETWILER  and
DENNIS M. DACEY
CHRISTOPHER M. DAVENPORT
Affiliation:
Neurobiology and Behavior Graduate Program, University of Washington, Seattle, Washington
PETER B. DETWILER
Affiliation:
Department of Physiology and Biophysics, University of Washington, Seattle, Washington
DENNIS M. DACEY
Affiliation:
Department of Biological Structure, University of Washington, Seattle, Washington
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Abstract

The A1 cell is an axon-bearing amacrine cell of the primate retina with a diffusely stratified, moderately branched dendritic tree (∼400 μm diameter). Axons arise from proximal dendrites forming a second concentric, larger arborization (>4 mm diameter) of thin processes with bouton-like swellings along their length. A1 cells are ON-OFF transient cells that fire a brief high frequency burst of action potentials in response to light (Stafford & Dacey, 1997). It has been hypothesized that A1 cells receive local input to their dendrites, with action potentials propagating output via the axons across the retina, serving a global inhibitory function. To explore this hypothesis we recorded intracellularly from A1 cells in an in vitro macaque monkey retina preparation. A1 cells have an antagonistic center-surround receptive field structure for the ON and OFF components of the light response. Blocking the ON pathway with L-AP4 eliminated ON center responses but not OFF center responses or ON or OFF surround responses. Blocking GABAergic inhibition with picrotoxin increased response amplitudes without affecting receptive field structure. TTX abolished action potentials, with little effect on the sub-threshold light response or basic receptive field structure. We also used multi-photon laser scanning microscopy to record light-induced calcium transients in morphologically identified dendrites and axons of A1 cells. TTX completely abolished such calcium transients in the axons but not in the dendrites. Together these results support the current model of A1 function, whereby the dendritic tree receives synaptic input that determines the center-surround receptive field; and action potentials arise in the axons, which propagate away from the dendritic field across the retina.

Keywords

RetinaAmacrineCalciumReceptive FieldAxon
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 449 - 457
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Bloomfield, S.A. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 75, 1878–1893.Google Scholar
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.Google Scholar
Dacey, D., Packer, O.S., Diller, L., Brainard, D., Peterson, B. & Lee, B. (2000a). Center surround receptive field structure of cone bipolar cells in primate retina. Vision Research 40, 1801–1811.Google Scholar
Dacey, D.M. (1988). Dopamine-accumulating retinal neurons revealed by in vitro fluorescence display a unique morphology. Science 240, 1196–1198.Google Scholar
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. Journal of Comparative Neurology 284, 275–293.Google Scholar
Dacey, D.M. (1990). The dopaminergic amacrine cell. Journal of Comparative Neurology 301, 461–489.Google Scholar
Dacey, D.M., Diller, L.C., Verweij, J. & Williams, D.R. (2000b). Physiology of L- and M-cone inputs to H1 horizontal cells in the primate retina. Journal of the Optical Society of America A: Optics Image Science and Vision 17, 589–596.Google Scholar
Dacey, D.M., Peterson, B.B., Robinson, F.R. & Gamlin, P.D. (2003). Fireworks in the primate retina: In Vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15.Google Scholar
Denk, W. & Detwiler, P.B. (1999). Optical recording of light-evoked calcium signals in the functionally intact retina. Proceedings of the National Academy of Sciences 96, 7035–7040.Google Scholar
Denk, W., Strickler, J.H. & Webb, W.W. (1990). Two-photon laser scanning fluorescence microscopy. Science 248, 73.Google Scholar
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.Google Scholar
Famiglietti, E.V. (1992a). Polyaxonal amacrine cells of rabbit retina: morphology and stratification of PA1 cells. Journal of Comparative Neurology 316, 391–405.Google Scholar
Famiglietti, E.V. (1992b). Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. Journal of Comparative Neurology 316, 422–446.Google Scholar
Famiglietti, E.V. (1992c). Polyaxonal amacrine cells of rabbit retina: Size and distribution of PA1 cells. Journal of Comparative Neurology 316, 406–421.Google Scholar
Freed, M.A., Pflug, R., Kolb, H. & Nelson, R. (1996). ON-OFF amacrine cells in cat retina. Journal of Comparative Neurology 364, 556–566.Google Scholar
Goldberg, J.H., Tamas, G. & Yuste, R. (2003). Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation. Journal of Physiology 551, 49–65.Google Scholar
Hirasawa, H. & Kaneko, A. (2003). pH Changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. Journal of General Physiology 122, 657–671.Google Scholar
Kamermans, M., Fahrenfort, I., Schultz, K., Janssen-Bienhold, U., Sjoerdsma, T. & Weiler, R. (2001). Hemichannel-mediated inhibition in the outer retina. Science 292, 1178–1180.Google Scholar
Kruger, J., Fischer, B. & Barth, R. (1975). The shift-effect in retinal ganglion cells of the rhesus monkey. Experimental Brain Research 23, 443–446.Google Scholar
Lev-Ram, V. & Grinvald, A. (1987). Activity-dependent calcium transients in central nervous system myelinated axons revealed by the calcium indicator Fura-2. Biophysical Journal 52, 571–576.Google Scholar
Mariani, A.P., Cosenza-Murphy, D. & Barker. J.L. (1987). GABAergic synapses and benzodiazepine receptors are not identically distributed in the primate retina. Brain Research 415, 153–157.Google Scholar
McMahon, M.J., Packer, O.S. & Dacey, D.M. (2004). The classical receptive field surround of primate parasol ganglion cells is mediated primarily by a non-GABAergic pathway. Journal of Neuroscience 24, 3736–3745.Google Scholar
Oesch, N., Euler, T. & Taylor, W.R. (2005). Direction-selective dendritic action potentials in rabbit retina. Neuron 47, 739.Google Scholar
Olveczky, B.P., Baccus, S.A. & Meister, M. (2003). Segregation of object and background motion in the retina. Nature 423, 401–408.Google Scholar
Packer, O., Diller, L.C., Verweij, J., Lee, B.B., Pokorny, J., Williams, D.R., Dacey, D.M. & Brainard, D.H. (2001). Characterization and use of a digital light projector for vision research. Vision Research 41, 427.Google Scholar
Roska, B. & Werblin, F. (2003). Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nature Neuroscience 6, 600–608.Google Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182–185.Google Scholar
Solomon, S.G., Lee, B.B. & Sun, H. (2006). Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of Macaque. Journal of Neuroscience 26, 8715–8726.Google Scholar
Stafford, D.K. & Dacey, D.M. (1997). Physiology of the A1 amacrine: A spiking, axon-bearing interneuron of the macaque monkey retina. Visual Neuroscience 14, 507–522.Google Scholar
Taylor, W.R. (1996). Response properties of long-range axon-bearing amacrine cells in the dark-adapted rabbit retina. Visual Neuroscience 13, 599–604.Google Scholar
Vessey, J.P., Stratis, A.K., Daniels, B.A., Da Silva, N., Jonz, M.G., Lalonde, M.R., Baldridge, W.H. & Barnes, S. (2005). Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. Journal of Neuroscience 25, 4108–4117.Google Scholar
Vigh, J. & Witkovsky, P. (1999). Sub-millimolar cobalt selectively inhibits the receptive field surround of retinal neurons. Visual Neuroscience 16, 159–168.Google Scholar
Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. Journal of Comparative Neurology 440, 109–125.Google Scholar
Werblin, F.S. (1972). Lateral interactions at inner plexiform layer of vertebrate retina: Antagonistic responses to change. Science 175, 1008–1010.Google Scholar
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 17–40.Google Scholar
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.Google Scholar
Zhang, C-L., Wilson, J.A., Williams, J. & Chiu, S.Y. (2006). Action potentials induce uniform calcium influx in mammalian myelinated optic nerves. Journal of Neurophysiology 96, 695–709.Google Scholar