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Can Retinal Ganglion Cell Dipoles Seed Iso-Orientation Domains in the Visual Cortex?

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  • Manuel Schottdorf
  • Stephen J Eglen
  • Fred Wolf
  • Wolfgang Keil

Abstract

It has been argued that the emergence of roughly periodic orientation preference maps (OPMs) in the primary visual cortex (V1) of carnivores and primates can be explained by a so-called statistical connectivity model. This model assumes that input to V1 neurons is dominated by feed-forward projections originating from a small set of retinal ganglion cells (RGCs). The typical spacing between adjacent cortical orientation columns preferring the same orientation then arises via Moiré-Interference between hexagonal ON/OFF RGC mosaics. While this Moiré-Interference critically depends on long-range hexagonal order within the RGC mosaics, a recent statistical analysis of RGC receptive field positions found no evidence for such long-range positional order. Hexagonal order may be only one of several ways to obtain spatially repetitive OPMs in the statistical connectivity model. Here, we investigate a more general requirement on the spatial structure of RGC mosaics that can seed the emergence of spatially repetitive cortical OPMs, namely that angular correlations between so-called RGC dipoles exhibit a spatial structure similar to that of OPM autocorrelation functions. Both in cat beta cell mosaics as well as primate parasol receptive field mosaics we find that RGC dipole angles are spatially uncorrelated. To help assess the level of these correlations, we introduce a novel point process that generates mosaics with realistic nearest neighbor statistics and a tunable degree of spatial correlations of dipole angles. Using this process, we show that given the size of available data sets, the presence of even weak angular correlations in the data is very unlikely. We conclude that the layout of ON/OFF ganglion cell mosaics lacks the spatial structure necessary to seed iso-orientation domains in the primary visual cortex.

Suggested Citation

  • Manuel Schottdorf & Stephen J Eglen & Fred Wolf & Wolfgang Keil, 2014. "Can Retinal Ganglion Cell Dipoles Seed Iso-Orientation Domains in the Visual Cortex?," PLOS ONE, Public Library of Science, vol. 9(1), pages 1-18, January.
  • Handle: RePEc:plo:pone00:0086139
    DOI: 10.1371/journal.pone.0086139
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    References listed on IDEAS

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    1. Jeffrey L Gauthier & Greg D Field & Alexander Sher & Martin Greschner & Jonathon Shlens & Alan M Litke & E J Chichilnisky, 2009. "Receptive Fields in Primate Retina Are Coordinated to Sample Visual Space More Uniformly," PLOS Biology, Public Library of Science, vol. 7(4), pages 1-9, April.
    2. F. Wolf & T. Geisel, 1998. "Spontaneous pinwheel annihilation during visual development," Nature, Nature, vol. 395(6697), pages 73-78, September.
    3. Kenichi Ohki & Sooyoung Chung & Prakash Kara & Mark Hübener & Tobias Bonhoeffer & R. Clay Reid, 2006. "Highly ordered arrangement of single neurons in orientation pinwheels," Nature, Nature, vol. 442(7105), pages 925-928, August.
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    Cited by:

    1. James Rankin & Frédéric Chavane, 2017. "Neural field model to reconcile structure with function in primary visual cortex," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-30, October.

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