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A circuit suppressing retinal drive to the optokinetic system during fast image motion

Author

Listed:
  • Adam Mani

    (Brown University)

  • Xinzhu Yang

    (Brown University)

  • Tiffany A. Zhao

    (Brown University)

  • Megan L. Leyrer

    (Brown University)

  • Daniel Schreck

    (Brown University)

  • David M. Berson

    (Brown University)

Abstract

Optokinetic nystagmus (OKN) assists stabilization of the retinal image during head rotation. OKN is driven by ON direction selective retinal ganglion cells (ON DSGCs), which encode both the direction and speed of global retinal slip. The synaptic circuits responsible for the direction selectivity of ON DSGCs are well understood, but those sculpting their slow-speed preference remain enigmatic. Here, we probe this mechanism in mouse retina through patch clamp recordings, functional imaging, genetic manipulation, and electron microscopic reconstructions. We confirm earlier evidence that feedforward glycinergic inhibition is the main suppressor of ON DSGC responses to fast motion, and reveal the source for this inhibition—the VGluT3 amacrine cell, a dual neurotransmitter, excitatory/inhibitory interneuron. Together, our results identify a role for VGluT3 cells in limiting the speed range of OKN. More broadly, they suggest VGluT3 cells shape the response of many retinal cell types to fast motion, suppressing it in some while enhancing it in others.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40527-z
    DOI: 10.1038/s41467-023-40527-z
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    References listed on IDEAS

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    1. Shai Sabbah & John A. Gemmer & Ananya Bhatia-Lin & Gabrielle Manoff & Gabriel Castro & Jesse K. Siegel & Nathan Jeffery & David M. Berson, 2017. "A retinal code for motion along the gravitational and body axes," Nature, Nature, vol. 546(7659), pages 492-497, June.
    2. Bao-hua Liu & Andrew D. Huberman & Massimo Scanziani, 2016. "Cortico-fugal output from visual cortex promotes plasticity of innate motor behaviour," Nature, Nature, vol. 538(7625), pages 383-387, October.
    3. Keisuke Yonehara & Kamill Balint & Masaharu Noda & Georg Nagel & Ernst Bamberg & Botond Roska, 2011. "Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit," Nature, Nature, vol. 469(7330), pages 407-410, January.
    4. 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.
    5. Moritz Helmstaedter & Kevin L. Briggman & Srinivas C. Turaga & Viren Jain & H. Sebastian Seung & Winfried Denk, 2013. "Connectomic reconstruction of the inner plexiform layer in the mouse retina," Nature, Nature, vol. 500(7461), pages 168-174, August.
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