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Vertical interactions across ten parallel, stacked representations in the mammalian retina

Nature volume 410, pages 583–587 (2001)Cite this article

Abstract

The mammalian visual system analyses the world through a set of separate spatio-temporal channels1,2. The organization of these channels begins in the retina1,3, where the precise laminations of both the axon terminals of bipolar cells and the dendritic arborizations of ganglion cells suggests the presence of a vertical stack of neural strata at the inner plexiform layer (IPL)3,4,5,6,7,8,9,10,11. Conversely, many inhibitory amacrine cell classes are multiply or diffusely stratified12, indicating that they might convey information between strata. On the basis of the diverse stratification and physiological properties of ganglion cells, it was suggested that the IPL contains a parallel set of representations of the visual world3,7 embodied in the strata and conveyed to higher centres by the classes of ganglion cells whose dendrites ramify at that stratum. Here we show that each stratum receives unique and substantively different excitatory and inhibitory neural inputs that are integrated to form at least ten different, parallel space-time spiking outputs. The response properties of these strata are ordered in the time domain. Inhibition through GABAC receptors extracts spatial edges in neural representations and seems to separate the functional properties of the strata. We describe a new form of neuronal interaction that we call ‘vertical inhibition’ that acts not laterally, but between strata.

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Figure 1: Space-time pattern measurements.
Figure 2: Spiking patterns in each row (measured from four different members of the same cell class) for five different classes of ganglion cells.
Figure 3: Seven of the ten parallel measured representations correlated with depth within the IPL.
Figure 4: Order in the IPL.
Figure 5: Vertical inhibition in the IPL.

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Acknowledgements

We thank J. E. Dowling, M. M. Poo, R. H. Kramer and S. Picaud for their comments on the manuscript, and C. Chen for his assistance with the experiments. This study was supported by the ONR and NIH.

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  1. Department of Molecular and Cell Biology, University of California at Berkeley, 145 LSA, Berkeley, 94720, California, USA

    Botond Roska & Frank Werblin

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  1. Botond Roska
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Correspondence to Frank Werblin.

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Roska, B., Werblin, F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587 (2001). https://doi.org/10.1038/35069068

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