Article | Published:

Retinal origin of direction selectivity in the superior colliculus

Nature Neuroscience volume 20, pages 550558 (2017) | Download Citation

Abstract

Detecting visual features in the environment, such as motion direction, is crucial for survival. The circuit mechanisms that give rise to direction selectivity in a major visual center, the superior colliculus (SC), are entirely unknown. We optogenetically isolate the retinal inputs that individual direction-selective SC neurons receive and find that they are already selective as a result of precisely converging inputs from similarly tuned retinal ganglion cells. The direction-selective retinal input is linearly amplified by intracollicular circuits without changing its preferred direction or level of selectivity. Finally, using two-photon calcium imaging, we show that SC direction selectivity is dramatically reduced in transgenic mice that have decreased retinal selectivity. Together, our studies demonstrate a retinal origin of direction selectivity in the SC and reveal a central visual deficit as a consequence of altered feature selectivity in the retina.

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Acknowledgements

We thank X. Zhao and H. Chen for their help with data analysis. For the use of GCaMP6s, we gratefully acknowledge V. Jayaraman, R.A. Kerr, D.S. Kim, L.L. Looger and K. Svoboda from the GENIE Project, Janelia Farm Research Campus, Howard Hughes Medical Institute. This research was supported by US National Institutes of Health (NIH) grants (EY026286 to J.C. and X.L., and EY024016 to W.W.), National Natural Science Foundation of China (NSFC) grant (81371049 to X.S.), China Scholarship Council (CSC) scholarship (201309120003 to X.S.) and Tianjin 131 Innovative Talent Project first-level talent scholarship (to X.S.).

Author information

Author notes

    • Xuefeng Shi
    •  & Jad Barchini

    These authors contributed equally to this work.

Affiliations

  1. Department of Neurobiology, Northwestern University, Evanston, Illinois, USA.

    • Xuefeng Shi
    • , Jad Barchini
    • , Yanjiao Jin
    • , Xiaorong Liu
    •  & Jianhua Cang
  2. Tianjin Eye Hospital, Tianjin Key Laboratory of Ophthalmology and Visual Science, Tianjin Eye Institute, Clinical College of Ophthalmology, Tianjin Medical University, Tianjin, China.

    • Xuefeng Shi
  3. Interdepartmental Neuroscience Program, Northwestern University, Evanston, Illinois, USA.

    • Jad Barchini
  4. Department of Neurobiology, The University of Chicago, Chicago, Illinois, USA.

    • Hector Acaron Ledesma
    • , David Koren
    •  & Wei Wei
  5. General Hospital, Tianjin Medical University, Tianjin, China.

    • Yanjiao Jin
  6. Department of Ophthalmology, Northwestern University, Chicago, Illinois, USA.

    • Xiaorong Liu

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Contributions

X.S., J.B., X.L., W.W. and J.C. designed the experiments. X.S. performed in vivo whole-cell recording experiments and analyzed the data. J.B. performed in vivo two-photon imaging experiments and analyzed the data. H.A.L. and D.K. performed retinal imaging experiments and analyzed the data. J.C. performed intrinsic imaging. Y.J. performed histology. W.W. and J.C. guided data analysis and oversaw the project. All authors discussed the results and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jianhua Cang.

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DOI

https://doi.org/10.1038/nn.4498

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