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Rapid global shifts in natural scenes block spiking in specific ganglion cell types

Abstract

The mammalian retina contains more than a dozen different ganglion cell types, each with dendrites ramifying at different strata within the inner plexiform layer (IPL) and each carrying a unique representation of the visual world. We studied the inhibitory and excitatory inputs, as well as the spiking output, of each of the rabbit retinal ganglion cell type during rapid global shifts in 'natural' videos designed to mimic saccadic eye movements. These shifts generated stratum-specific transient inhibitory activity, affecting only those ganglion cells whose dendrites ramify within the central strata of the IPL. The inhibition was GABA-mediated, acted both pre- and postsynaptically and was fast enough to either prevent or delay spiking. These findings indicate that the fast, transient elevation of visual threshold during rapid shifts in scene has a significant retinal component.

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Figure 1: Global scene shifts elicit inhibition.
Figure 2: Parallel processing of global image shifts: suppressed cell types.
Figure 3: Parallel processing of global image shifts: non-suppressed cell types.
Figure 4: The dendritic stratification of suppressed and non-suppressed cells in the IPL.
Figure 5: Isolating the shift inhibition.
Figure 6: Properties of the fast inhibition to suppressed cells.
Figure 7: Spatial summation of the global change–evoked inhibition.

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Acknowledgements

We thank D. Takacs and M. Jaszberenyi for their technical assistance, D. Balya for his comments on the experiments and R. Zucker for his comments on the manuscript. This study was supported by the Office of Naval Research.

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Correspondence to Botond Roska.

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Supplementary information

Supplementary Fig. 1.

Properties of the stimulus movies. (a) The first frame from each movie. (b) The distribution of gray scale values of each movie. Horizontal axis: gray scale values, vertical axis: the % of the specified grayscale value in the movie. (c) The distribution of contrast values (see Methods) of each movie measured at the level of the retina. Horizontal axis: contrast values, vertical axis: the % of the specified contrast value in the movie. (d) Spatial frequency distribution of each movie. The amplitude of the 2D Fourier transform of each frame of each movie was calculated and normalized to the maximum amplitude. The mean (of all frames) amplitude distribution is shown as a grayscale plot. (e) The row shown by the arrow in (d) is plotted. (f) Temporal frequency distribution of each movie. The series of grayscale values as a function of time (frame number) at each pixel were Fourier transformed and normalized to the maximum amplitude. The mean amplitude distribution is shown. (g) The normalized contrast content (cc(t)) as a function of time (horizontal axis: frame number) during each stimulus movie. The contrast content was calculated by the following function: cc(t) = Σx,y (p(t,x,y) - p(t - 1,x,y))2 where t is the frame number, x and y are the spatial coordinates of a pixel and p(t,x,y) is the grayscale value of a pixel at (t,x,y). This function was normalized to its maximum value. The arrows point to the scene shifts. In the supplementary figure, if the horizontal axes of plots in a column had the same units the units are labeled only at the bottom row. (JPG 92 kb)

Supplementary Methods (PDF 17 kb)

Supplementary Video (MOV 2876 kb)

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Roska, B., Werblin, F. Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nat Neurosci 6, 600–608 (2003). https://doi.org/10.1038/nn1061

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