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Directionally selective calcium signals in dendrites of starburst amacrine cells

Nature volume 418, pages 845–852 (2002)Cite this article

Abstract

The detection of image motion is fundamental to vision. In many species, unique classes of retinal ganglion cells selectively respond to visual stimuli that move in specific directions. It is not known which retinal cell first performs the neural computations that give rise to directional selectivity in the ganglion cell. A prominent candidate has been an interneuron called the ‘starburst amacrine cell’. Using two-photon optical recordings of intracellular calcium concentration, here we find that individual dendritic branches of starburst cells act as independent computation modules. Dendritic calcium signals, but not somatic membrane voltage, are directionally selective for stimuli that move centrifugally from the cell soma. This demonstrates that direction selectivity is computed locally in dendritic branches at a stage before ganglion cells.

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Figure 1: Calcium responses in starburst amacrine cell dendrites.
Figure 2: Surround stimulation evokes a decrease in [Ca2+] and occasionally transient increases after the end of the stimulus.
Figure 3: Local stimulation evokes local calcium signals.
Figure 4: Moving stimuli evoke direction-selective calcium responses in dendrites.
Figure 5: Preferred direction and cellular morphology.
Figure 6: The GABAA blocker SR-95531 caused increased spontaneous activity but no reduction of [Ca2+]-signal direction selectivity.
Figure 7: Responses to expanding and contracting waves.

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References

  1. Barlow, H. B., Hill, R. M. & Levick, W. R. Rabbit retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol. 173, 377–407 (1964)

    Article  CAS  Google Scholar 

  2. Vaney, D. I., He, S., Taylor, W. R. & Levick, W. R. in Motion Vision—Computational, Neural, and Ecological Constraints (eds Zanker, J. M. & Zeil, J.) (Springer, Berlin, 2001)

    Google Scholar 

  3. Masland, R. H., Mills, J. W. & Cassidy, C. The functions of acetylcholine in the rabbit retina. Proc. R. Soc. Lond. B 223, 121–139 (1984)

    Article  ADS  CAS  Google Scholar 

  4. Borg-Graham, L. J. & Grzywacz, N. M. in Single Neuron Computation (eds McKenna, T., Zornetzer, S. F. & Davis, J. L.) 347–375 (Academic, London, 1992)

    Book  Google Scholar 

  5. Famiglietti, E. V. Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J. Comp. Neurol. 309, 40–70 (1991)

    Article  CAS  Google Scholar 

  6. Tauchi, M. & Masland, R. H. The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc. R. Soc. Lond. B 223, 101–191 (1984)

    Article  ADS  CAS  Google Scholar 

  7. He, S. & Masland, R. H. Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382 (1997)

    Article  ADS  CAS  Google Scholar 

  8. Borg-Graham, L. J. The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nature Neurosci. 4, 176–183 (2001)

    Article  CAS  Google Scholar 

  9. Taylor, W. R., He, S., Levick, W. R. & Vaney, D. I. Dendritic computation of direction selectivity by retinal ganglion cells. Science 289, 2347–2350 (2000)

    Article  ADS  CAS  Google Scholar 

  10. Yoshida, K. et al. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780 (2001)

    Article  CAS  Google Scholar 

  11. Euler, T. & Denk, W. Dendritic processing. Curr. Opin. Neurobiol. 11, 415–422 (2001)

    Article  CAS  Google Scholar 

  12. Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990)

    Article  ADS  CAS  Google Scholar 

  13. Ehinger, B., Zucker, C. L., Bruun, A. & Adolph, A. In vivo staining of oligodendroglia in the rabbit retina. Glia 10, 40–48 (1994)

    Article  CAS  Google Scholar 

  14. Miller, R. F. et al. Structure and functional connections of presynaptic terminals in the vertebrate retina revealed by activity-dependent dyes and confocal microscopy. J. Comp. Neurol. 437, 129–155 (2001)

    Article  CAS  Google Scholar 

  15. Brandon, C. Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity. Brain Res. 426, 119–130 (1987)

    Article  CAS  Google Scholar 

  16. Denk, W. & Detwiler, P. B. Optical recording of light-evoked calcium signals in the functionally intact retina. Proc. Natl Acad. Sci. USA 96, 7035–7040 (1999)

    Article  ADS  CAS  Google Scholar 

  17. Bloomfield, S. A. Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. J. Neurophys. 68, 711–725 (1992)

    Article  CAS  Google Scholar 

  18. Taylor, W. R. & Wassle, H. Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. Eur. J. Neurosci. 7, 2300–2321 (1995)

    Article  Google Scholar 

  19. Peters, B. N. & Masland, R. H. Responses to light of starburst amacrine cells. J. Neurophysiol. 75, 469–480 (1996)

    Article  CAS  Google Scholar 

  20. Miller, R. F. & Bloomfield, S. A. Electroanatomy of a unique amacrine cell in the rabbit retina. Proc. Natl Acad. Sci. USA 80, 3069–3073 (1983)

    Article  ADS  CAS  Google Scholar 

  21. Poznanski, R. R. Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: a functional interpretation of dendritic morphology. Bull. Math. Biol. 54, 905–928 (1992)

    Article  CAS  Google Scholar 

  22. Taylor, W. R. & Wässle, H. Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. Eur. J. Neurosci. 7, 2308–2321 (1995)

    Article  CAS  Google Scholar 

  23. Pan, Z. H. & Lipton, S. A. Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. J. Neurosci. 15, 2668–2679 (1995)

    Article  CAS  Google Scholar 

  24. Linn, D. M. & Massey, S. C. GABA inhibits ACh release from the rabbit retina: a direct effect or feedback to bipolar cells? Vis. Neurosci. 8, 97–106 (1992)

    Article  CAS  Google Scholar 

  25. Massey, S. C., Linn, D. M., Kittila, C. A. & Mirza, W. Contributions of GABAA receptors and GABAC receptors to acetylcholine release and directional selectivity in the rabbit retina. Vis. Neurosci. 14, 939–948 (1997)

    Article  CAS  Google Scholar 

  26. Wyatt, H. J. & Daw, N. W. Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204–205 (1976)

    Article  ADS  CAS  Google Scholar 

  27. Reichardt, W. in Sensory Communication (ed. Rosenblith, W. A.) 377–390 (MIT Press/Wiley, New York, 1961)

    Google Scholar 

  28. Velte, T. J. & Miller, R. F. Spiking and nonspiking models of starburst amacrine cells in the rabbit retina. Vis. Neurosci. 14, 1073–1088 (1997)

    Article  CAS  Google Scholar 

  29. Keyser, K. T. et al. Amacrine, ganglion, and displaced amacrine cells in the rabbit retina express nicotinic acetylcholine receptors. Vis. Neurosci. 17, 743–752 (2000)

    Article  CAS  Google Scholar 

  30. Zhou, Z. J. & Fain, G. L. Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices. J. Neurosci. 15, 5334–5345 (1995)

    Article  CAS  Google Scholar 

  31. Wässle, H., Koulen, P., Brandstätter, J. H., Fletcher, E. L. & Becker, C. M. Glycine and GABA receptors in the mammalian retina. Vision Res. 38, 1411–1430 (1998)

    Article  Google Scholar 

  32. Masland, R. H., Mills, J. W. & Hayden, S. A. Acetylcholine-synthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proc. R. Soc. Lond. B 223, 79–100 (1984)

    Article  ADS  CAS  Google Scholar 

  33. Brecha, N., Johnson, D., Peichl, L. & Wassle, H. Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proc. Natl Acad. Sci. USA 85, 6187–6191 (1988)

    Article  ADS  CAS  Google Scholar 

  34. Vaney, D. I. & Young, H. M. GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res. 438, 369–373 (1988)

    Article  CAS  Google Scholar 

  35. O'Malley, D. M., Sandell, J. H. & Masland, R. H. Co-release of acetylcholine and GABA by the starburst amacrine cells. J. Neurosci. 12, 1394–1408 (1992)

    Article  CAS  Google Scholar 

  36. Schwartz, E. A. Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science 238, 350–355 (1987)

    Article  ADS  CAS  Google Scholar 

  37. Dodge, F. A. Jr & Rahamimoff, R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193, 419–432 (1967)

    Article  CAS  Google Scholar 

  38. Ariel, M. & Daw, N. W. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J. Physiol. 324, 161–185 (1982)

    Article  CAS  Google Scholar 

  39. Grzywacz, N. M., Tootle, J. S. & Amthor, F. R. Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit retinal directional selectivity? Vis. Neurosci. 14, 39–54 (1997)

    Article  CAS  Google Scholar 

  40. Kittila, C. A. & Massey, S. C. Pharmacology of directionally selective ganglion cells in the rabbit retina. J. Neurophysiol. 77, 675–689 (1997)

    Article  CAS  Google Scholar 

  41. Grzywacz, N. M., Merwine, D. K. & Amthor, F. R. Complementary roles of two excitatory pathways in retinal directional selectivity. Vis. Neurosci. 15, 1119–1127 (1998)

    Article  CAS  Google Scholar 

  42. Masland, R. H. & Mills, J. W. Autoradiographic identification of acetylcholine in the rabbit retina. J. Cell Biol. 83, 159–178 (1979)

    Article  CAS  Google Scholar 

  43. Borst, A. & Egelhaaf, M. Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process. Proc. Natl Acad. Sci. USA 87, 9363–9367 (1990)

    Article  ADS  CAS  Google Scholar 

  44. Vaney, D. I., Collins, S. P. & Young, H. M. in Neurobiology of the Inner Retina (eds Weiler, R. & Osborn, N. N.) 157–168 (Springer, Berlin, 1989)

    Book  Google Scholar 

  45. Barlow, H. B. & Levick, W. R. The mechanism of directionally selective units in rabbit's retina. J. Physiol. 178, 477–504 (1965)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank A. Borst and D. Margolis for useful discussions, R. Friedrich for comments on the manuscript, and M. Müller, J. Tritthart and J. Sawinski for technical help.

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Authors and Affiliations

  1. Max Planck Institute for Medical Research, Jahnstrasse 29, D-69120, Heidelberg, Germany

    Thomas Euler & Winfried Denk

  2. Department of Physiology & Biophysics, University of Washington, Box 357290, Seattle, Washington, 98195, USA

    Peter B. Detwiler

  3. Biophysics, Box 357290

    Peter B. Detwiler

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Correspondence to Thomas Euler.

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W.D. is a co-holder of a patent for two-photon microscopy.

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Euler, T., Detwiler, P. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852 (2002). https://doi.org/10.1038/nature00931

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