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Direction selectivity in a model of the starburst amacrine cell

Published online by Cambridge University Press:  01 July 2004

JOHN J. TUKKER ,
W. ROWLAND TAYLOR  and
ROBERT G. SMITH
JOHN J. TUKKER
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
W. ROWLAND TAYLOR
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
ROBERT G. SMITH
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
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Abstract

The starburst amacrine cell (SBAC), found in all mammalian retinas, is thought to provide the directional inhibitory input recorded in On–Off direction-selective ganglion cells (DSGCs). While voltage recordings from the somas of SBACs have not shown robust direction selectivity (DS), the dendritic tips of these cells display direction-selective calcium signals, even when γ-aminobutyric acid (GABAa,c) channels are blocked, implying that inhibition is not necessary to generate DS. This suggested that the distinctive morphology of the SBAC could generate a DS signal at the dendritic tips, where most of its synaptic output is located. To explore this possibility, we constructed a compartmental model incorporating realistic morphological structure, passive membrane properties, and excitatory inputs. We found robust DS at the dendritic tips but not at the soma. Two-spot apparent motion and annulus radial motion produced weak DS, but thin bars produced robust DS. For these stimuli, DS was caused by the interaction of a local synaptic input signal with a temporally delayed “global” signal, that is, an excitatory postsynaptic potential (EPSP) that spread from the activated inputs into the soma and throughout the dendritic tree. In the preferred direction the signals in the dendritic tips coincided, allowing summation, whereas in the null direction the local signal preceded the global signal, preventing summation. Sine-wave grating stimuli produced the greatest amount of DS, especially at high velocities and low spatial frequencies. The sine-wave DS responses could be accounted for by a simple mathematical model, which summed phase-shifted signals from soma and dendritic tip. By testing different artificial morphologies, we discovered DS was relatively independent of the morphological details, but depended on having a sufficient number of inputs at the distal tips and a limited electrotonic isolation. Adding voltage-gated calcium channels to the model showed that their threshold effect can amplify DS in the intracellular calcium signal.

Keywords

Direction selectivityStarburst amacrineMorphologyCalcium channelsModeling
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 4 , July 2004 , pp. 611 - 625
Copyright
2004 Cambridge University Press

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References

REFERENCES

Amthor, F.R., Keyser, K.T., & Dmitrieva, N.A. (2002). Effects of the destruction of starburst-cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity. Visual Neuroscience 19, 495–509.CrossRefGoogle Scholar
Barlow, H.B. & Hill, R.M. (1963). Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139, 412–414.CrossRefGoogle Scholar
Bloomfield, S.A. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit. Journal of Neurophysiology 75, 1878–1893.Google Scholar
Borg-Graham, L.J. & Grzywacz, N.M. (1992). A model of the directional selectivity circuit in retina: Transformations by neurons singly and in concert. In Single Neuron Computation, ed. McKenna, T., Davis, J. & Zornetzer, S.F., pp. 347–376. New York: Academic Press, Inc.
Brandstätter, J.H., Greferath, U., Euler, T., & Wässle, H. (1995). Co-stratification of GABAA receptors with the directionally selective circuitry of the rat retina. Visual Neuroscience 12, 345–358.CrossRefGoogle Scholar
Brecha, N., Johnson, D., Peichl, L., & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.CrossRefGoogle Scholar
Cohen, E. (2001). Voltage-gated calcium and sodium currents of starburst amacrine cells in the rabbit retina. Visual Neuroscience 18, 799–809.CrossRefGoogle Scholar
Cohen, E. & Sterling, P. (1990). Demonstration of cell types among cone bipolar neurons of cat retina. Philosophical Transactions of the Royal Society B (London) 330, 305–321.CrossRefGoogle Scholar
Dacheux, R.F., Chimento, M.F., & Amthor, F.R. (2003). Synaptic input to the On–Off directionally selective ganglion cell in the rabbit retina. Journal of Comparative Neurology 456, 267–278.CrossRefGoogle Scholar
Euler, T., Detwiler, P.B., & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.CrossRefGoogle Scholar
Famiglietti, E.V. (1983). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells. Vision Research 23, 1265–1279.CrossRefGoogle Scholar
Famiglietti, E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. Journal of Comparative Neurology 309, 40–70.CrossRefGoogle Scholar
Famiglietti, E.V. (2002). A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Visual Neuroscience 19, 145–162.CrossRefGoogle Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.Google Scholar
Fried, S.I., Münch, T.A., & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle Scholar
Gavrikov, K.E., Dmitriev, A.V., Keyser, K.T., & Mangel, S.C. (2003) Cation-chloride cotransporters mediate neural computation in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 100, 16047–16052.CrossRefGoogle Scholar
Hassenstein, B. & Reichardt, W.E. (1956). Functional structure of a mechanism of perception of optical movement. Proceedings 1st International Congress Cybernetics Namar, 797–801.
He, S. & Masland, R.H. (1997). Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382.Google Scholar
Jensen, R.J. (1995). Effects of Ca2+ channel blockers on directional selectivity of rabbit retinal ganglion cells. Journal of Neurophysiology 74, 12–23.Google Scholar
Joyner, R.W., Westerfield, M., Moore, J.W., & Stockbridge, N. (1978). A numerical method to model excitable cells. Biophysical Journal 22, 155–170.CrossRefGoogle Scholar
Kier, C.K., Buchsbaum, G., & Sterling, P. (1995). How retinal microcircuits scale for ganglion cells of different size. Journal of Neuroscience 15, 7673–7683.Google Scholar
Mao, B.Q., MacLeish, P.R., & Victor, J.D. (2002). Relation between potassium-channel kinetics and the intrinsic dynamics in isolated retinal bipolar cells. Journal of Computational Neuroscience 12, 147–163.CrossRefGoogle Scholar
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269–280.CrossRefGoogle Scholar
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S., & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog (rana pipiens). Journal of General Physiology 43 (Suppl. 2), 129–171.CrossRefGoogle Scholar
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.CrossRefGoogle Scholar
Miller, R.F. & Bloomfield, S.A (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 80, 3069–3073.CrossRefGoogle Scholar
O'Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and γ-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.Google Scholar
O'Malley, D.M., Sandell, J.H., & Masland, R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 1394–1408.Google Scholar
Perkel, D.H. & Mulloney, B. (1978). Elecrotonic properties of neurons: steady-state compartmental model. Journal of Neurophysiology 41, 621–639.Google Scholar
Peters, B.N. & Masland, R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469–480.Google Scholar
Poznanski, R.R. (1992). Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology. Bulletin of Mathematical Biology 54, 905–928.CrossRefGoogle Scholar
Rall, W. (1959). Branching dendritic trees and motoneuron membrane resistivity. Experimental Neurology 1, 491–527.CrossRefGoogle Scholar
Rall, W. (1964). Theoretical significance of dendritic trees for neuronal input–output relations. In Neural Theory and Modeling, ed. Reis, R.F., pp. 72–97. Stanford, California: Stanford University Press.
Rall, W. (1967). Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. Journal of Neurophysiology 30, 1138–1168.Google Scholar
Sather, W.A., Tanabe, T., Zhang, J.-F., Mori, Y., Adams, M.E., & Tsien, R.W. (1993). Distinctive biophysical and pharmacological properties of Class A (BI) calcium channel α1 subunits. Neuron 11, 291–303.CrossRefGoogle Scholar
Schneeweis, D.M. & Schnapf, J.L. (1999). The photovoltage of macaque cone photoreceptors: Adaptation, noise, and kinetics. Journal of Neuroscience 19, 1203–1216.Google Scholar
Schwartz, E.A. (1987). Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science 238, 350–355.CrossRefGoogle Scholar
Serrano, J.R., Perez-Reyes, E., & Jones, S.W. (1999). State-dependent inactivation of the alpha1G T-type calcium channel. Journal of General Physiology 114, 185–201.CrossRefGoogle Scholar
Shields, C.R. & Lukasiewicz, P.D. (2003). Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. Journal of Neurophysiology 89, 2449–2458.CrossRefGoogle Scholar
Smith, R.G. (1992). NeuronC: A computational language for investigating functional architecture of neural circuits. Journal of Neuroscience Methods 43, 83–108.CrossRefGoogle Scholar
Smith, R.G. (2004). The NeuronC neural circuit simulation language. Available for academic use at: ftp://retina.anatomy.upenn.edu/pub/nc.tgz.
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–305.CrossRefGoogle Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–191.CrossRefGoogle Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. Journal of Neuroscience 22, 7712–7720.Google Scholar
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 2308–2321.CrossRefGoogle Scholar
Torre, V. & Poggio, T. (1978). A synaptic mechanism possibly underlying directional selectivity to motion. Proceedings of the Royal Society (London) 202, 409–416.CrossRefGoogle Scholar
Vaney, D.I. (1984). “Coronate” amacrine cells in the rabbit retina have the “starburst” dendritic morphology. Proceedings of the Royal Society of London Series B. Biological Sciences 220, 501–508.CrossRefGoogle Scholar
Vaney, D.I., Collin, S.P., & Young, H.M. (1989). Dendritic relationships between cholinergic amacrine cells and direction-selective ganglion cells. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 157–168. Berlin: Springer.CrossRef
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle Scholar
van Rossum, M.C., O'Brien, B.J., & Smith, R.G. (2003). Effects of noise on the spike timing precision of retinal ganglion cells. Journal of Neurophysiology 89, 2406–2419.CrossRefGoogle Scholar
Velte, T.J. & Miller, R.F. (1997). Spiking and nonspiking models of starburst amacrine cells in the rabbit retina. Visual Neuroscience 14, 1073–1088.CrossRefGoogle Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.CrossRefGoogle Scholar
Yamada, E.S., Dmitrieva, N., Keyser, K.T., Lindstrom, J.M., Hersh, L.B., & Marshak, D.W. (2003). Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. Journal of Comparative Neurology 461, 76–90.CrossRefGoogle Scholar
Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I., & Nakanishi, S. (2001). A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780.CrossRefGoogle Scholar
Zhou, Z.J. & Fain, G.L. (1996). Starburst amacrine cells change from spiking to non-spiking neurons during retinal development. Proceedings of the National Academy of Sciences of the U.S.A. 93, 8057–8062.CrossRefGoogle Scholar