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Retinal direction selectivity after targeted laser ablation of starburst amacrine cells

Abstract

Directionally selective retinal ganglion cells respond strongly when a stimulus moves in their preferred direction, but respond little or not at all when it moves in the opposite direction1,2. This selectivity represents a classic paradigm of computation by neural microcircuits, but its cellular mechanism remains obscure. The directionally selective ganglion cells receive many synapses from a type of amacrine cell termed ‘starburst’ because of its regularly spaced, evenly radiating dendrites3,4. Starburst amacrine cells have a synaptic asymmetry that has been proposed as the source of the directional response in the ganglion cells5,6. Here we report experiments that make this unlikely, and offer an alternative concept of the function of starburst cells. We labelled starburst cells in living retinas, then killed them by targeted laser ablation while recording from individual directionally selective ganglion cells. Ablating starburst cells revealed no asymmetric contribution to the ganglion cell response. Instead of being direction discriminators, the starburst cells appear to potentiate generically the responses of ganglion cells to moving stimuli. The origin of direction selectivity probably lies with another type of amacrine cell.

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Figure 1: Starburst cells receive inputs from bipolar cells along the whole length of their dendrites, but their outputs to retinal ganglion cells are restricted to the distal third of the dendrites, leading to an asymmetric relationship between input and output.
Figure 2: Photoablating on-starburst cells by laser irradiation.
Figure 3: Effect of ablating starburst cells on the responses of directionally selective cells.
Figure 4: Effects of 50 µM D-tubocurarine on responses of directionally selective ganglion cells to 12 directions of motion.
Figure 5: Effects of a cholinergic receptor antagonist in a retina treated with picrotoxin (50 µM).

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Acknowledgements

We thank M. Chiang for help in developing the laser system, and S. Wallenstein for preparing cultured cells.

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Correspondence to Richard H. Masland.

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He, S., Masland, R. Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382 (1997). https://doi.org/10.1038/38723

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