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The Journal of Neuroscience, March 8, 2006, 26(10):2652-2660; doi:10.1523/JNEUROSCI.3316-05.2006

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Cellular/Molecular
Robustness of Neural Coding in Drosophila Photoreceptors in the Absence of Slow Delayed Rectifier K⁺ Channels

Mikko Vähäsöyrinki,¹ Jeremy E. Niven,² Roger C. Hardie,³ Matti Weckström,¹ and Mikko Juusola²

¹Department of Physical Sciences, Division of Biophysics and Biocenter Oulu, University of Oulu, 90014 Oulun Yliopisto, Oulu, Finland, ²Physiological Laboratory, University of Cambridge, Cambridge CB2 3EG, United Kingdom, and ³Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, United Kingdom

Correspondence should be addressed to Dr. Matti Weckström, Department of Physical Sciences, Division of Biophysics, and Biocenter Oulu, University of Oulu, P.O. Box 3000, 90014 Oulun Yliopisto, Oulu, Finland. Email: matti.weckstrom{at}oulu.fi

Determining the contribution of a single type of ion channel to information processing within a neuron requires not only knowledge of the properties of the channel but also understanding of its function within a complex system. We studied the contribution of slow delayed rectifier K⁺ channels to neural coding in Drosophila photoreceptors by combining genetic and electrophysiological approaches with biophysical modeling. We show that the Shab gene encodes the slow delayed rectifier K⁺ channel and identify a novel voltage-gated K⁺ conductance. Analysis of the in vivo recorded voltage responses together with their computer-simulated counterparts demonstrates that Shab channels in Drosophila photoreceptors attenuate the light-induced depolarization and prevent response saturation in bright light. We also show that reduction of the Shab conductance in mutant photoreceptors is accompanied by a proportional drop in their input resistance. This reduction in input resistance partially restores the signaling range, sensitivity, and dynamic coding of light intensities of Shab photoreceptors to those of the wild-type counterparts. However, loss of the Shab channels may affect both the energy efficiency of coding and the processing of natural stimuli. Our results highlight the role of different types of voltage-gated K⁺ channels in the performance of the photoreceptors and provide insight into functional robustness against the perturbation of specific ion channel composition.

Key words: vision; nonspiking; information; intracellular; patch clamp; modeling

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Received Aug. 8, 2005; revised Jan. 16, 2006; accepted Jan. 16, 2006.

Correspondence should be addressed to Dr. Matti Weckström, Department of Physical Sciences, Division of Biophysics, and Biocenter Oulu, University of Oulu, P.O. Box 3000, 90014 Oulun Yliopisto, Oulu, Finland. Email: matti.weckstrom{at}oulu.fi

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