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The contribution of Shaker K+ channels to the information capacity of Drosophila photoreceptors

Abstract

An array of rapidly inactivating voltage-gated K+ channels is distributed throughout the nervous systems of vertebrates and invertebrates1,2,3,4,5. Although these channels are thought to regulate the excitability of neurons by attenuating voltage signals, their specific functions are often poorly understood. We studied the role of the prototypical inactivating K+ conductance, Shaker6,7, in Drosophila photoreceptors8,9 by recording intracellularly from wild-type and Shaker mutant photoreceptors. Here we show that loss of the Shaker K+ conductance produces a marked reduction in the signal-to-noise ratio of photoreceptors, generating a 50% decrease in the information capacity of these cells in fully light-adapted conditions. By combining experiments with modelling, we show that the inactivation of Shaker K+ channels amplifies voltage signals and enables photoreceptors to use their voltage range more effectively. Loss of the Shaker conductance attenuated the voltage signal and induced a compensatory decrease in impedance. Our results demonstrate the importance of the Shaker K+ conductance for neural coding precision and as a mechanism for selectively amplifying graded signals in neurons, and highlight the effect of compensatory mechanisms on neuronal information processing.

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Figure 1: Shaker K+ channels amplify photoreceptor voltage responses.
Figure 2: Comparison of the information and gain of wild-type and ShKS133 photoreceptors.
Figure 3: A photoreceptor model predicts accurately the dynamic responses of wild-type and Shaker membranes.
Figure 4: Shaker-mediated signal amplification is dependent on the activation–inactivation properties of the Shaker and delayed rectifier channels.
Figure 5: Shaker K+ channel inactivation and the size of the leak conductance contribute to the voltage range of the WT and ShKS133 photoreceptors.

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Acknowledgements

We thank G. Garcia de Polavieja and H. Robinson for comments on an earlier version of this manuscript. The work was supported by the Royal Society (M.J. and R.C.H.) and the Wellcome Trust (M.J., J.N. and R.C.H.).

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Correspondence to Mikko Juusola.

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Niven, J., Vähäsöyrinki, M., Kauranen, M. et al. The contribution of Shaker K+ channels to the information capacity of Drosophila photoreceptors. Nature 421, 630–634 (2003). https://doi.org/10.1038/nature01384

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