Skip to main content

A retinal circuit model accounting for wide-field amacrine cells

Cognitive Neurodynamics volume 3, pages 25–32 (2009)Cite this article

Abstract

In previous experimental studies on the visual processing in vertebrates, higher-order visual functions such as the object segregation from background were found even in the retinal stage. Previously, the “linear–nonlinear” (LN) cascade models have been applied to the retinal circuit, and succeeded to describe the input-output dynamics for certain parts of the circuit, e.g., the receptive field of the outer retinal neurons. And recently, some abstract models composed of LN cascades as the circuit elements could explain the higher-order retinal functions. However, in such a model, each class of retinal neurons is mostly omitted and thus, how those neurons play roles in the visual computations cannot be explored. Here, we present a spatio-temporal computational model of the vertebrate retina, based on the response function for each class of retinal neurons and on the anatomical inter-cellular connections. This model was capable of not only reproducing the spatio-temporal filtering properties of the outer retinal neurons, but also realizing the object segregation mechanism in the inner retinal circuit involving the “wide-field” amacrine cells. Moreover, the first-order Wiener kernels calculated for the neurons in our model showed a reasonable fit to the kernels previously measured in the real retinal neuron in situ.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Baccus SA (2007) Timing and computation in inner retinal circuitry. Annu Rev Physiol 69:271–290

    PubMed  Article  CAS  Google Scholar 

  • Baccus SA, Olveczky BP, Manu M, Meister M (2008) A retinal circuit that computes object motion. J Neurosci 28(27):6807–6817. doi:10.1523/JNEUROSCI.4206-07.2008

    PubMed  Article  CAS  Google Scholar 

  • Burkhardt DA, Fahey PK, Sikora M (1998) Responses of ganglion cells to contrast steps in the light-adapted retina of the tiger salamander. Vis Neurosci 15(2):219–229. doi:10.1017/S0952523898152021

    PubMed  Article  CAS  Google Scholar 

  • Cook PB, McReynolds JS (1998) Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nat Neurosci 1(8):714–719. doi:10.1038/3714

    PubMed  Article  CAS  Google Scholar 

  • Dacey DM (1989) Axon-bearing amacrine cells of the macaque monkey retina. J Comp Neurol 284:275–293. doi:10.1002/cne.902840210

    PubMed  Article  CAS  Google Scholar 

  • Enroth-Cugell C, Jakiela HG (1980) Suppression of cat retinal ganglion cell responses by moving patterns. J Physiol 302:49–72

    PubMed  CAS  Google Scholar 

  • Famiglietti EV (1992a) Polyaxonal amacrine cells of rabbit retina: morphology and stratification of PA1 cells. J Comp Neurol 316:391–405. doi:10.1002/cne.903160402

    PubMed  Article  CAS  Google Scholar 

  • Famiglietti EV (1992b) Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. J Comp Neurol 316:422–446. doi:10.1002/cne.903160404

    PubMed  Article  CAS  Google Scholar 

  • Gaudiano P (1994) Simulations of X and Y retinal ganglion cell behavior with a nonlinear push–pull model of spatiotemporal retinal processing. Vision Res 34(13):1767–1784

    PubMed  Article  CAS  Google Scholar 

  • Lin B, Masland RH (2006) Populations of wide-field amacrine cells in the mouse retina. J Comp Neurol 499(5):797–809

    PubMed  Article  Google Scholar 

  • Marmarelis PZ, Naka KI (1973) Nonlinear analysis and synthesis of receptive-field responses in the catfish retina. II. One-input white-noise analysis. J Neurophysiol 36(4):619–633

    PubMed  CAS  Google Scholar 

  • Masland RH (2003) Vision: the retina’s fancy tricks. Nature 423(6938):387–388

    PubMed  Article  CAS  Google Scholar 

  • Naka KI, Itoh MA, Chappel RL (1987) Dynamics of turtle cones. J Gen Physiol 89(2):321–337

    PubMed  Article  CAS  Google Scholar 

  • Olveczky BP, Baccus SA, Meister M (2003) Segregation of object and background motion in the retina. Nature 423(6938):401–408; Prog Brain Res 147:205–218

    Google Scholar 

  • Passaglia CL, Enroth-Cugell C, Troy JB (2001) Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells. J Neurosci 21(15):5794–5803

    PubMed  CAS  Google Scholar 

  • Roska B, Werblin F (2003) Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nat Neurosci 6(6):600–608

    PubMed  Article  CAS  Google Scholar 

  • Sakai HM, Naka KI (1987) Signal transmission in the catfish retina. V. Sensitivity and circuit. J Neurophysiol 58(6):1329–1349

    PubMed  CAS  Google Scholar 

  • Sakai HM, Machuca H, Naka KI (1997a) Processing of color- and noncolor-coded signals in the gourami retina. I.Horizontal cells. J Neurophysiol 78(4):2002–2017

    PubMed  CAS  Google Scholar 

  • Sakai HM, Machuca H, Naka KI (1997b) Processing of color- and noncolor-coded signals in the gourami retina. II. Amacrine cells. J Neurophysiol 78(4):2018–2033

    PubMed  CAS  Google Scholar 

  • Sakai HM, Machuca H, Korenberg MJ, Naka KI (1997c) Processing of color- and noncolor-coded signals in the gourami retina. III. Ganglion cells. J Neurophysiol 78(4):2034–2047

    PubMed  CAS  Google Scholar 

  • Shields CR, Lukasiewicz PD (2003) Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. J Neurophysiol 89(5):2449–2458

    PubMed  Article  CAS  Google Scholar 

  • Solomon SG, Lee BB, Sun H (2006) Suppressive surrounds and contrast gain in magnocellular pathway retinal ganglion cells of macaque. J Neurosci 26(34):8715–8726

    PubMed  Article  CAS  Google Scholar 

  • Teeters J, Jacobs A, Werblin F (1997) How neural interactions form neural responses in the salamander retina. J Comput Neurosci 4(1):5–27

    PubMed  Article  CAS  Google Scholar 

  • Thiel A, Greschner M, Ammermuller J (2006) The temporal structure of transient ON/OFF ganglion cell responses and its relation to intra-retinal processing. J Comput Neurosci 21(2):131–151

    PubMed  Article  Google Scholar 

  • Zaghloul KA, Manookin MB, Borghuis BG, Boahen K, Demb JB (2007) Functional circuitry for peripheral suppression in mammalian Y-type retinal ganglion cells. J Neurophysiol 97(6):4327–4340

    PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Human and Environmental Informatics, Graduate School of Science and Technology, Kumamoto University, 2-39-1 Kurokami , Kumamoto, 860-8555, Japan

    Murat Sağlam, Yuki Hayashida & Nobuki Murayama

Authors
  1. Murat Sağlam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuki Hayashida
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nobuki Murayama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuki Hayashida.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sağlam, M., Hayashida, Y. & Murayama, N. A retinal circuit model accounting for wide-field amacrine cells. Cogn Neurodyn 3, 25–32 (2009). https://doi.org/10.1007/s11571-008-9059-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-008-9059-8

Keywords

  • Circuit model
  • Vertebrate retina
  • Amacrine cells
  • Wiener kernel
  • Visual function