New directions in retinal research

https://doi.org/10.1016/S0166-2236(03)00167-XGet rights and content

Abstract

Direction-selective retinal ganglion cells (DSGCs) respond to image motion in a ‘preferred’ direction but not the opposite ‘null’ direction. Extracellular spike recordings from rabbit DSGCs suggested that the key mechanism underlying the directional responses is spatially offset inhibition projecting in the null direction. Recent patch-clamp recordings have shown that this inhibition, which acts directly on the DSGC, is already direction selective. Dual recordings established that the inhibition arises from starburst amacrine cells (SBACs) located on the null side of the DSGC but not from those on the preferred side. Thus, for each radially symmetric SBAC, processes pointing in different directions would provide the null-direction inhibition to subtypes of DSGCs with different preferred directions. Ca2+ imaging revealed that the SBAC terminal processes respond more strongly to image motion away from the soma than towards the soma, therefore accounting for the direction selectivity of the inhibitory input to the DSGCs.

Section snippets

Excitatory and inhibitory synaptic inputs

Apparent-motion stimuli also revealed that facilitation of excitatory inputs occurs for preferred-direction sequences 9, 15 but extracellular recordings of action potentials failed to disentangle the contributions of asymmetric inhibition and asymmetric facilitation to direction selectivity. However, patch-clamp recordings of synaptic currents in microscopically identified DSGCs have enabled the excitatory and inhibitory inputs to be examined directly, based on the assumptions that the

Starburst amacrine cells

Excitatory glutamate inputs to retinal ganglion cells arise from ∼10 types of cone bipolar cell, which provide vertical links with the photoreceptors, whereas inhibitory GABA or glycine inputs arise from 30–40 types of amacrine cell, which provide lateral links within the inner plexiform layer 24, 25, 26. In addition, two types of amacrine cell provide excitatory ACh inputs to some types of ganglion cell, most notably the DSGCs 27, 28, 29. The cholinergic amacrine cells have a distinctive

Direction-selective inhibition

Direct evidence that the SBACs provide an asymmetric inhibitory input to DSGCs has recently been obtained by Shelley Fried, Thomas Münch and Frank Werblin [16], who made simultaneous patch recordings from a DSGC and an overlapping On-SBAC. The soma of the SBAC was located on either the null side or the preferred side of the DSGC, which correspond to the flanks first encountered by null-direction or preferred-direction motion, respectively. Depolarization of SBAC somata located on the null side,

Direction-selective excitation

Extracellular recording studies indicated that DSGCs receive about half their excitatory drive from cone bipolar cells, largely through the glutamate-mediated activation of NMDA receptors, and receive the other half from SBACs, through the activation of nicotinic receptors by ACh 28, 53. Although recent patch-clamp studies have revealed that the excitatory inputs to DSGCs are direction selective 16, 17, 18, the relative contributions of the glutamatergic and cholinergic inputs have not been

Postsynaptic mechanisms

Given that the excitatory and inhibitory inputs to DSGCs are already directional 16, 17, 18, what role is played by the postsynaptic interactions between the spatially offset inputs in generating the responses of DSGCs? A hallmark of direction selectivity in the retina is the finding that DSGCs respond directionally to small displacements covering a fraction (a ‘subunit’) of the receptive field 9, 70. Postsynaptic models of direction selectivity rely upon the localized action of shunting

Concluding remarks

Recent studies have established that SBACs play the key role in the generation of direction selectivity in the retina. SBACs not only provide the direction-selective inhibitory inputs to DSGCs but also might account for the direction-selective excitatory inputs, either directly or indirectly. However, several important issues remain to be resolved, including the cellular mechanisms that generate direction-selective responses in the SBAC processes, the neuronal circuitry that underlies the

Acknowledgements

Our research on direction selectivity in the retina is supported by project grants from the National Health and Medical Research Council of Australia.

References (75)

  • K. Yoshida

    A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement

    Neuron

    (2001)
  • E.V. Famiglietti

    Functional architecture of cone bipolar cells in mammalian retina

    Vision Res.

    (1981)
  • S. He et al.

    Spatial–temporal response characteristics of the ON–OFF direction selective ganglion cells in the rabbit retina

    Neurosci. Lett.

    (2000)
  • H.B. Barlow et al.

    Selective sensitivity to direction of motion in ganglion cells of the rabbit's retina

    Science

    (1963)
  • H.B. Barlow

    Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit

    J. Physiol.

    (1964)
  • Vaney, D.I. et al. (2001) Direction-selective ganglion cells in the retina. In Motion Vision: Computational, Neural,...
  • C.W. Oyster et al.

    Direction-selective units in rabbit retina: distribution of preferred directions

    Science

    (1967)
  • D.I. Vaney

    Territorial organization of direction-selective ganglion cells in rabbit retina

    J. Neurosci.

    (1994)
  • F.R. Amthor et al.

    Spatial organization of retinal information about the direction of image motion

    Proc. Natl. Acad. Sci. U. S. A.

    (1995)
  • H.B. Barlow et al.

    The mechanism of directionally selective units in rabbit's retina

    J. Physiol.

    (1965)
  • H.J. Wyatt et al.

    Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed

    J. Neurophysiol.

    (1975)
  • F.R. Amthor et al.

    Inhibition in ON–OFF directionally selective ganglion cells of the rabbit retina

    J. Neurophysiol.

    (1993)
  • S.F. Stasheff et al.

    Functional inhibition in direction-selective retinal ganglion cells: spatiotemporal extent and intralaminar interactions

    J. Neurophysiol.

    (2002)
  • H.J. Wyatt et al.

    Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina

    Science

    (1976)
  • J.H. Caldwell

    Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields

    J. Physiol.

    (1978)
  • N.M. Grzywacz et al.

    Facilitation in ON–OFF directionally selective ganglion cells of the rabbit retina

    J. Neurophysiol.

    (1993)
  • S.I. Fried

    Mechanisms and circuitry underlying directional selectivity in the retina

    Nature

    (2002)
  • L.J. Borg-Graham

    The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell

    Nat. Neurosci.

    (2001)
  • W.R. Taylor et al.

    Diverse synaptic mechanisms generate direction selectivity in the rabbit retina

    J. Neurosci.

    (2002)
  • W.R. Taylor

    Dendritic computation of direction selectivity by retinal ganglion cells

    Science

    (2000)
  • G. Yang et al.

    Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells

    Science

    (1992)
  • G. Yang et al.

    Receptive fields and dendritic structure of directionally selective retinal ganglion cells

    J. Neurosci.

    (1994)
  • V. Torre et al.

    A synaptic mechanism possibly underlying directional selectivity to motion

    Proc. R. Soc. Lond. B Biol. Sci.

    (1978)
  • DeVoe, R.D. et al. (1989) Not by ganglion cells alone: directional selectivity is widespread in identified cells of the...
  • R.H. Masland et al.

    Responses to acetylcholine of ganglion cells in an isolated mammalian retina

    J. Neurophysiol.

    (1976)
  • M. Ariel et al.

    Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells

    J. Physiol.

    (1982)
  • B.T. Reed

    Rabbit retinal ganglion cell responses mediated by α-bungarotoxin-insensitive nicotinic acetylcholine receptors

    Vis. Neurosci.

    (2002)

    • Cited by (94)

    • A novel motion direction detection mechanism based on dendritic computation of direction-selective ganglion cells

      2022, Knowledge-Based Systems

    • 1.19 - Retinal Mosaics

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition

    • Muscarinic acetylcholine receptor-mediated stimulation of retinal ganglion cell photoreceptors

      2016, Neuropharmacology

    • Retinal ganglion cell neuroprotection induced by activation of alpha7 nicotinic acetylcholine receptors

      2015, Neuropharmacology

    • Wavelet transform and texture recognition based on spiking neural network for visual images

      2015, Neurocomputing

    • Functional architecture of the retina: Development and disease

      2014, Progress in Retinal and Eye Research
      Citation Excerpt :

      The DS retinal ganglion cells respond to motion of a stimulus in one direction (preferred direction) but not to motion in the opposite direction (null direction) (Barlow and Hill, 1963; Vaney et al., 2012). Inhibition from starburst amacrine cells is crucial for generation of this direction-selective response (Taylor and Vaney, 2003). In particular, asymmetric GABAergic inhibition is generated in the null-direction motion to generate direction-selectivity (Briggman et al., 2011; Fried et al., 2002; Zhou and Lee, 2008).

    View all citing articles on Scopus
    View full text
    Copyright © 2003 Elsevier Science Ltd. All rights reserved.