Article | Published:

Species-specific wiring for direction selectivity in the mammalian retina

Nature volume 535, pages 105110 (07 July 2016) | Download Citation

Abstract

Directionally tuned signalling in starburst amacrine cell (SAC) dendrites lies at the heart of the circuit that detects the direction of moving stimuli in the mammalian retina. The relative contributions of intrinsic cellular properties and network connectivity to SAC direction selectivity remain unclear. Here we present a detailed connectomic reconstruction of SAC circuitry in mouse retina and describe two previously unknown features of synapse distributions along SAC dendrites: input and output synapses are segregated, with inputs restricted to proximal dendrites; and the distribution of inhibitory inputs is fundamentally different from that observed in rabbit retina. An anatomically constrained SAC network model suggests that SAC–SAC wiring differences between mouse and rabbit retina underlie distinct contributions of synaptic inhibition to velocity and contrast tuning and receptive field structure. In particular, the model indicates that mouse connectivity enables SACs to encode lower linear velocities that account for smaller eye diameter, thereby conserving angular velocity tuning. These predictions are confirmed with calcium imaging of mouse SAC dendrites responding to directional stimuli.

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Acknowledgements

We thank W. Denk for supporting the collection of the serial block-face scanning electron microscopy data in his laboratory. This work was supported by NIH grants EY016607 and EY022070 (RGS), by the NINDS Intramural Research Program (NS003145; J.S.D.) and (NS003133; K.L.B.), the Max-Planck Society (K.L.B.), and the Pew Charitable Trusts (K.L.B.).

Author information

Affiliations

  1. Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892, USA

    • Huayu Ding
    • , Alon Poleg-Polsky
    •  & Jeffrey S. Diamond
  2. Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA

    • Robert G. Smith
  3. Department of Biomedical Optics, Max Planck Institute for Medical Research, Heidelberg 69120, Germany

    • Kevin L. Briggman
  4. Circuit Dynamics and Connectivity Unit, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892, USA

    • Kevin L. Briggman

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Contributions

H.D., R.G.S. and K.L.B. collected and analysed data; H.D., R.G.S., A.P.-P., J.S.D., and K.L.B. designed the study and wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Kevin L. Briggman.

Reviewer Information Nature thanks G. Knott and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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DOI

https://doi.org/10.1038/nature18609

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