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Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells

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Abstract

Contrast is computed throughout the nervous system to encode changing inputs efficiently. The retina encodes luminance and contrast over a wide range of visual conditions and must adapt its responses to maintain sensitivity and to avoid saturation. We examined the means by which one type of adaptation allows individual synapses to compute contrast and encode luminance in biphasic responses to step changes in light levels. Light-evoked depletion of the readily releasable vesicle pool (RRP) at rod bipolar cell ribbon synapses in rat retina limited the dynamic range available to encode transient, but not sustained, responses, thereby allowing the transient and sustained components of release to compute temporal contrast and encode mean light levels, respectively. A release/replenishment model revealed that a single, homogeneous pool of synaptic vesicles is sufficient to generate this behavior and that a partial depletion of the RRP is the dominant mechanism for shaping the biphasic contrast/luminance response.

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Figure 1: RBC synaptic release encodes both contrast and luminance.
Figure 2: Contrast is computed at the RBC synapse.
Figure 3: RRP continuously varies with VRBC.
Figure 4: RRP occupancy is constant during sustained release.
Figure 5: RRP occupancy encodes luminance.
Figure 6: Synaptic simulations suggest that a homogeneous RRP is sufficient to encode a measure of contrast and luminance.
Figure 7: The synaptic release model can encode luminance and compute contrast from light-evoked RBC waveforms.

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Change history

  • 03 November 2011

    In the version of this article initially published online, Figure 6 panels b-e were misidentified. The error has been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank G. Murphy for helpful discussions, and W.W. Kothmann, A. Poleg-Polsky and A. Scimemi for comments on the manuscript. This work was supported by the National Institute of Neurological Disorders and Stroke Intramural Research Program (NS002986).

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N.W.O. and J.S.D. conceived the project and designed the experiments. N.W.O. performed the experiments, analyzed the data and designed the mathematical model. N.W.O. and J.S.D. wrote the manuscript.

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Correspondence to Jeffrey S Diamond.

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Oesch, N., Diamond, J. Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat Neurosci 14, 1555–1561 (2011). https://doi.org/10.1038/nn.2945

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