Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Mechanisms and circuitry underlying directional selectivity in the retina

Abstract

In the retina, directionally selective ganglion cells respond with robust spiking to movement in their preferred direction, but show minimal response to movement in the opposite, or null, direction1,2. The mechanisms and circuitry underlying this computation have remained controversial3. Here we show, by isolating the excitatory and inhibitory inputs to directionally selective cells and measuring direct connections between these cells and presynaptic neurons, that a presynaptic interneuron, the starburst amacrine cell, delivers direct inhibition to directionally selective cells. The processes of starburst cells are connected asymmetrically to directionally selective cells: those pointing in the null direction deliver inhibition; those pointing in the preferred direction do not. Starburst cells project inhibition laterally ahead of a stimulus moving in the null direction. In addition, starburst inhibition is itself directionally selective: it is stronger for movement in the null direction. Excitation in response to null direction movement is reduced by an inhibitory signal acting at a site that is presynaptic to the directionally selective cell. The interplay of these components generates reduced excitation and enhanced inhibition in the null direction, thereby ensuring robust directional selectivity.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Excitatory and inhibitory inputs to DS ganglion cells: asymmetries in magnitude and space.
Figure 2: Starburst cells on the null side supply directionally selective inhibition to DS cells.
Figure 3: Null movement vetoes excitatory input to the DS cell.
Figure 4: Proposed circuitry underlying the DS response.

Similar content being viewed by others

References

  1. Barlow, H. B. & Hill, R. M. Selective sensitivity to direction of movement in ganglion cells of rabbit retina. Science 139, 412–414 (1963)

    Article  ADS  CAS  Google Scholar 

  2. Barlow, H. B. & Levick, W. R. Mechanism of directionally selective units in rabbits retina. J. Physiol. (Lond.) 178, 477–504 (1965)

    Article  CAS  Google Scholar 

  3. Vaney, D. I., He, S., Taylor, W. R. & Levick, W. R. Motion Vision—Computational, Neural, and Ecological Constraints (ed. Zeil, J.) 13–56 (Springer, Berlin, 2001)

    Google Scholar 

  4. 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 

  5. Caldwell, J. H., Daw, N. W. & Wyatt, H. J. Effects of picrotoxin and strychnine on rabbit retinal ganglion-cells—lateral interactions for cells with more complex receptive fields. J. Physiol. (Lond.) 276, 277–298 (1978)

    Article  CAS  Google Scholar 

  6. Famiglietti, E. V. Dendritic Costratification of on and on-off directionally selective ganglion-cells with starburst amacrine cells in rabbit retina. J. Comp. Neurol. 324, 322–335 (1992)

    Article  CAS  Google Scholar 

  7. Vaney, D. I. & Pow, D. V. The dendritic architecture of the cholinergic plexus in the rabbit retina: selective labeling by glycine accumulation in the presence of sarcosine. J. Comp. Neurol. 421, 1–13 (2000)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  10. 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 

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

    Article  ADS  CAS  Google Scholar 

  12. 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 

  13. Taylor, W. R., He, S. Y., 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 

  14. 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 

  15. Famiglietti, E. V. Starburst amacrine cells and cholinergic neurons—mirror-symmetric on and off amacrine cells of rabbit retina. Brain Res. 261, 138–144 (1983)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  17. 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 

  18. Linn, D. M., Blazynski, C., Redburn, D. A. & Massey, S. C. Acetylcholine-release from the rabbit retina mediated by kainate receptors. J. Neurosci. 11, 111–122 (1991)

    Article  CAS  Google Scholar 

  19. Masland, R. H. & Ames, A. Responses to acetylcholine of ganglion-cells in an isolated mammalian retina. J. Neurophysiol. 39, 1220–1235 (1976)

    Article  CAS  Google Scholar 

  20. Famiglietti, E. V. Starburst amacrine cells—morphological constancy and systematic variation in the anisotropic field of rabbit retinal neurons. J. Neurosci. 5, 562–577 (1985)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Borg-Graham, L. J. & Grzywacz, N. M. Single Neuron Computation (ed. Zornetzer, S. F.) 347–375 (Academic, London, 1992)

    Book  Google Scholar 

  23. Poznanski, R. R. Modeling 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 

  24. Vaney, D. I. Progress in Retinal Research (ed. Chader, G. J.) 49–100 (Oxford, Pergamon, 1990)

    Google Scholar 

  25. 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 

  26. Euler, T., Detwiler, P. B. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852 (2002)

    Article  ADS  CAS  Google Scholar 

  27. Mills, S. L. & Massey, S. C. Morphology of bipolar cells labelled by DAPI in the rabbit retina. J. Comp. Neurol. 321, 133–149 (1992)

    Article  CAS  Google Scholar 

  28. Roska, B. & Werblin, F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587 (2001)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. Okazaki for help with confocal preparations and image analysis; J. Hurtado, R. Kramer and C. Kretschmann for discussion; and H. Barlow, R. Froemke, E. Isacoff, X. Ren and R. Zucker for comments on the manuscript. This work was supported by grants from the Office of Naval Research, the National Eye Institute, and an NIH training grant in Vision Science to the University of California Berkeley (S.F.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Frank S. Werblin.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fried, S., Münch, T. & Werblin, F. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414 (2002). https://doi.org/10.1038/nature01179

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01179

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing