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Species-specific wiring for direction selectivity in the mammalian retina

Author

Listed:
  • Huayu Ding

    (Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke)

  • Robert G. Smith

    (University of Pennsylvania)

  • Alon Poleg-Polsky

    (Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke)

  • Jeffrey S. Diamond

    (Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke)

  • Kevin L. Briggman

    (Max Planck Institute for Medical Research
    Circuit Dynamics and Connectivity Unit, National Institute of Neurological Disorders and Stroke)

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.

Suggested Citation

  • Huayu Ding & Robert G. Smith & Alon Poleg-Polsky & Jeffrey S. Diamond & Kevin L. Briggman, 2016. "Species-specific wiring for direction selectivity in the mammalian retina," Nature, Nature, vol. 535(7610), pages 105-110, July.
    • Handle: RePEc:nat:nature:v:535:y:2016:i:7610:d:10.1038_nature18609
    DOI: 10.1038/nature18609
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    Cited by:

    1. John A. Gaynes & Samuel A. Budoff & Michael J. Grybko & Joshua B. Hunt & Alon Poleg-Polsky, 2022. "Classical center-surround receptive fields facilitate novel object detection in retinal bipolar cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Carles Bosch & Tobias Ackels & Alexandra Pacureanu & Yuxin Zhang & Christopher J. Peddie & Manuel Berning & Norman Rzepka & Marie-Christine Zdora & Isabell Whiteley & Malte Storm & Anne Bonnin & Chris, 2022. "Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron microtomography and volume electron microscopy," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Ling Li & Shasha Li & Wenhai Wang & Jielian Zhang & Yiming Sun & Qunrui Deng & Tao Zheng & Jianting Lu & Wei Gao & Mengmeng Yang & Hanyu Wang & Yuan Pan & Xueting Liu & Yani Yang & Jingbo Li & Nengjie, 2024. "Adaptative machine vision with microsecond-level accurate perception beyond human retina," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Tyler R. Sizemore & Julius Jonaitis & Andrew M. Dacks, 2023. "Heterogeneous receptor expression underlies non-uniform peptidergic modulation of olfaction in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    5. Zhuiri Peng & Lei Tong & Wenhao Shi & Langlang Xu & Xinyu Huang & Zheng Li & Xiangxiang Yu & Xiaohan Meng & Xiao He & Shengjie Lv & Gaochen Yang & Hao Hao & Tian Jiang & Xiangshui Miao & Lei Ye, 2024. "Multifunctional human visual pathway-replicated hardware based on 2D materials," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    6. Adam Mani & Xinzhu Yang & Tiffany A. Zhao & Megan L. Leyrer & Daniel Schreck & David M. Berson, 2023. "A circuit suppressing retinal drive to the optokinetic system during fast image motion," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. David Swygart & Wan-Qing Yu & Shunsuke Takeuchi & Rachel O. L. Wong & Gregory W. Schwartz, 2024. "A presynaptic source drives differing levels of surround suppression in two mouse retinal ganglion cell types," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    8. Héctor Acarón Ledesma & Jennifer Ding & Swen Oosterboer & Xiaolin Huang & Qiang Chen & Sui Wang & Michael Z. Lin & Wei Wei, 2024. "Dendritic mGluR2 and perisomatic Kv3 signaling regulate dendritic computation of mouse starburst amacrine cells," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Yeon Jin Kim & Beth B. Peterson & Joanna D. Crook & Hannah R. Joo & Jiajia Wu & Christian Puller & Farrel R. Robinson & Paul D. Gamlin & King-Wai Yau & Felix Viana & John B. Troy & Robert G. Smith & O, 2022. "Origins of direction selectivity in the primate retina," Nature Communications, Nature, vol. 13(1), pages 1-20, December.

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