Spatiotemporally Asymmetric Excitation Supports Mammalian Retinal Motion Sensitivity

Overview

Journal Curr Biol

Publisher Cell Press

Specialty Biology

Date 2019 Oct 1

PMID 31564498

Citations 27

Authors

Akihiro Matsumoto

Kevin L Briggman

Keisuke Yonehara

Affiliations

Soon will be listed here.

Abstract

The detection of visual motion is a fundamental function of the visual system. How motion speed and direction are computed together at the cellular level, however, remains largely unknown. Here, we suggest a circuit mechanism by which excitatory inputs to direction-selective ganglion cells in the mouse retina become sensitive to the motion speed and direction of image motion. Electrophysiological, imaging, and connectomic analyses provide evidence that the dendrites of ON direction-selective cells receive spatially offset and asymmetrically filtered glutamatergic inputs along motion-preference axis from asymmetrically wired bipolar and amacrine cell types with distinct release dynamics. A computational model shows that, with this spatiotemporal structure, the input amplitude becomes sensitive to speed and direction by a preferred direction enhancement mechanism. Our results highlight the role of an excitatory mechanism in retinal motion computation by which feature selectivity emerges from non-selective inputs.

Citing Articles

New insights into retinal circuits through EM connectomics: what we have learnt and what remains to be learned.

Sawant A, Saha A, Khoussine J, Sinha R, Hoon M Front Ophthalmol (Lausanne). 2024; 3:1168548.

PMID: 38983069 PMC: 11182165. DOI: 10.3389/fopht.2023.1168548.

Heterogeneous presynaptic receptive fields contribute to directional tuning in starburst amacrine cells.

Gaynes J, Budoff S, Grybko M, Poleg-Polsky A Elife. 2023; 12.

PMID: 38149980 PMC: 10752589. DOI: 10.7554/eLife.90456.

Neural Circuits Underlying Multifeature Extraction in the Retina.

Chander P, Hanson L, Chundekkad P, Awatramani G J Neurosci. 2023; 44(10).

PMID: 37957014 PMC: 10919202. DOI: 10.1523/JNEUROSCI.0910-23.2023.

Asymmetric connections with starburst amacrine cells underlie the upward motion selectivity of J-type retinal ganglion cells.

Wang B, Zhang Y PLoS Biol. 2023; 21(9):e3002301.

PMID: 37721959 PMC: 10538761. DOI: 10.1371/journal.pbio.3002301.

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

Mani A, Yang X, Zhao T, Leyrer M, Schreck D, Berson D Nat Commun. 2023; 14(1):5142.

PMID: 37612305 PMC: 10447436. DOI: 10.1038/s41467-023-40527-z.

References

Vaney D, Sivyer B, Taylor W . Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci. 2012; 13(3):194-208. DOI: 10.1038/nrn3165. View

Sivyer B, Tomlinson A, Taylor W . Simulated Saccadic Stimuli Suppress ON-Type Direction-Selective Retinal Ganglion Cells via Glycinergic Inhibition. J Neurosci. 2019; 39(22):4312-4322. PMC: 6538852. DOI: 10.1523/JNEUROSCI.3066-18.2019. View

Euler T, Detwiler P, Denk W . Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature. 2002; 418(6900):845-52. DOI: 10.1038/nature00931. View

Poleg-Polsky A, Diamond J . Imperfect space clamp permits electrotonic interactions between inhibitory and excitatory synaptic conductances, distorting voltage clamp recordings. PLoS One. 2011; 6(4):e19463. PMC: 3085473. DOI: 10.1371/journal.pone.0019463. View

Greene M, Kim J, Seung H . Analogous Convergence of Sustained and Transient Inputs in Parallel On and Off Pathways for Retinal Motion Computation. Cell Rep. 2016; 14(8):1892-900. PMC: 6404534. DOI: 10.1016/j.celrep.2016.02.001. View

Sethuramanujam S, McLaughlin A, deRosenroll G, Hoggarth A, Schwab D, Awatramani G . A Central Role for Mixed Acetylcholine/GABA Transmission in Direction Coding in the Retina. Neuron. 2016; 90(6):1243-1256. DOI: 10.1016/j.neuron.2016.04.041. View

Martersteck E, Hirokawa K, Evarts M, Bernard A, Duan X, Li Y . Diverse Central Projection Patterns of Retinal Ganglion Cells. Cell Rep. 2017; 18(8):2058-2072. PMC: 5357325. DOI: 10.1016/j.celrep.2017.01.075. View

Sivyer B, Williams S . Direction selectivity is computed by active dendritic integration in retinal ganglion cells. Nat Neurosci. 2013; 16(12):1848-56. DOI: 10.1038/nn.3565. View

Fransen J, Borghuis B . Temporally Diverse Excitation Generates Direction-Selective Responses in ON- and OFF-Type Retinal Starburst Amacrine Cells. Cell Rep. 2017; 18(6):1356-1365. DOI: 10.1016/j.celrep.2017.01.026. View

10.

Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K, Teixeira M . The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron. 2013; 79(6):1078-85. DOI: 10.1016/j.neuron.2013.08.005. View

11.

Park S, Kim I, Looger L, Demb J, Borghuis B . Excitatory synaptic inputs to mouse on-off direction-selective retinal ganglion cells lack direction tuning. J Neurosci. 2014; 34(11):3976-81. PMC: 3951696. DOI: 10.1523/JNEUROSCI.5017-13.2014. View

12.

OYSTER C . The analysis of image motion by the rabbit retina. J Physiol. 1968; 199(3):613-35. PMC: 1365363. DOI: 10.1113/jphysiol.1968.sp008671. View

13.

Sivyer B, van Wyk M, Vaney D, Taylor W . Synaptic inputs and timing underlying the velocity tuning of direction-selective ganglion cells in rabbit retina. J Physiol. 2010; 588(Pt 17):3243-53. PMC: 2976019. DOI: 10.1113/jphysiol.2010.192716. View

14.

Duan X, Krishnaswamy A, Laboulaye M, Liu J, Peng Y, Yamagata M . Cadherin Combinations Recruit Dendrites of Distinct Retinal Neurons to a Shared Interneuronal Scaffold. Neuron. 2018; 99(6):1145-1154.e6. PMC: 6284407. DOI: 10.1016/j.neuron.2018.08.019. View

15.

Baden T, Esposti F, Nikolaev A, Lagnado L . Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr Biol. 2011; 21(22):1859-69. PMC: 3235547. DOI: 10.1016/j.cub.2011.09.042. View

16.

Saszik S, DeVries S . A mammalian retinal bipolar cell uses both graded changes in membrane voltage and all-or-nothing Na+ spikes to encode light. J Neurosci. 2012; 32(1):297-307. PMC: 3503151. DOI: 10.1523/JNEUROSCI.2739-08.2012. View

17.

Sun L, M Brady C, Cahill H, Al-Khindi T, Sakuta H, Dhande O . Functional assembly of accessory optic system circuitry critical for compensatory eye movements. Neuron. 2015; 86(4):971-984. PMC: 4441577. DOI: 10.1016/j.neuron.2015.03.064. View

18.

Manookin M, Puller C, Rieke F, Neitz J, Neitz M . Distinctive receptive field and physiological properties of a wide-field amacrine cell in the macaque monkey retina. J Neurophysiol. 2015; 114(3):1606-16. PMC: 4563022. DOI: 10.1152/jn.00484.2015. View

19.

Bahl A, Ammer G, Schilling T, Borst A . Object tracking in motion-blind flies. Nat Neurosci. 2013; 16(6):730-8. DOI: 10.1038/nn.3386. View

20.

Briggman K, Helmstaedter M, Denk W . Wiring specificity in the direction-selectivity circuit of the retina. Nature. 2011; 471(7337):183-8. DOI: 10.1038/nature09818. View