An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in the mouse retina

  1. Tahnbee Kim
  2. Florentina Soto
  3. Daniel Kerschensteiner  Is a corresponding author
  1. Washington University School of Medicine, United States

Abstract

Retinal circuits detect salient features of the visual world and report them to the brain through spike trains of retinal ganglion cells. The most abundant ganglion cell type in mice, the so called W3 ganglion cell, selectively responds to movements of small objects. Where and how object motion sensitivity arises in the retina is incompletely understood. Here, we use 2 photon guided patch clamp recordings to characterize responses of VGluT3 expressing amacrine cells to a broad set of visual stimuli. We find that VG3 ACs are object motion sensitive and analyze the synaptic mechanisms underlying this computation. Anatomical circuit reconstructions suggest that VGluT3 expressing amacrine cells form glutamatergic synapses with W3 ganglion cells and targeted recordings show that the tuning of W3 ganglion cells' excitatory input matches that of VGluT3 expressing amacrine cells' responses. Synaptic excitation of W3 ganglion cells is diminished and responses to object motion are suppressed in mice lacking VGluT3. Object motion thus is first detected by VGluT3 expressing amacrine cells, which provide feature selective excitatory input to W3 ganglion cells.

Article and author information

Author details

  1. Tahnbee Kim

    Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Florentina Soto

    Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel Kerschensteiner

    Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, United States
    For correspondence
    dkerschensteiner@wustl.edu
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All procedures in this study were approved by the Animal Studies Committee of Washington University School of Medicine (Protocol #: 20140095) and performed in compliance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals.

Copyright

© 2015, Kim et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,920
    views
  • 805
    downloads
  • 83
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Tahnbee Kim
  2. Florentina Soto
  3. Daniel Kerschensteiner
(2015)
An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in the mouse retina
eLife 4:e08025.
https://doi.org/10.7554/eLife.08025

Share this article

https://doi.org/10.7554/eLife.08025

Further reading

    1. Neuroscience
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.

    1. Neuroscience
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.