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Retinal origin of orientation maps in visual cortex

Abstract

The orientation map is a hallmark of primary visual cortex in higher mammals. It is not yet known how orientation maps develop, what function they have in visual processing and why some species lack them. Here we advance the notion that quasi-periodic orientation maps are established by moiré interference of regularly spaced ON- and OFF-center retinal ganglion cell mosaics. A key prediction of the theory is that the centers of iso-orientation domains must be arranged in a hexagonal lattice on the cortical surface. Here we show that such a pattern is observed in individuals of four different species: monkeys, cats, tree shrews and ferrets. The proposed mechanism explains how orientation maps can develop without requiring precise patterns of spontaneous activity or molecular guidance. Further, it offers a possible account for the emergence of orientation tuning in single neurons despite the absence of orderly orientation maps in rodents species.

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Figure 1: Orientation maps as moiré interference patterns between retinal ganglion cell mosaics.
Figure 2: Moiré scaling factor and orientation map periodicity.
Figure 3: Hexagonal structure of orientation maps.
Figure 4: Robustness of seeded map to positional noise.
Figure 5: Robustness of receptive field shapes at different operating regimes of the model.

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Acknowledgements

We are grateful to A. Benucci and M. Carandini (University College London) for sharing their imaging data of cat primary visual cortex, supported by research grant EY017396 to M. Carandini. We also thank D. Fitzpatrick (Max Planck Florida Institute), L. White (Duke University), W. Bosking (University Texas at Austin) and Y. Li (UC Berkeley) for sharing existing ferret and tree shrew maps. We thank M. Carandini, D. Fitzpatrick, R. Shapley, J.-M. Alonso and E. Callaway for providing comments on earlier versions of this manuscript. This work was supported by research grant EY018322 (D.L.R.).

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Both S.-B.P. and D.L.R. were responsible for the theoretical concepts, computer simulations and writing.

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Correspondence to Dario L Ringach.

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Paik, SB., Ringach, D. Retinal origin of orientation maps in visual cortex. Nat Neurosci 14, 919–925 (2011). https://doi.org/10.1038/nn.2824

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