Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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


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.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. Hille, B. Ionic Channels of Excitable Membranes 3rd edn (Sinauer Associates, Sunderland, Massachusetts, 2001)

    Google Scholar 

  2. Rudy, B. Diversity and ubiquity of K+ channels. Neuroscience 25, 729–749 (1988)

    CAS  Article  Google Scholar 

  3. Coetzee, W. A. et al. Molecular diversity of K+ channels. Ann. NY Acad. Sci. 868, 233–285 (1999)

    ADS  CAS  Article  Google Scholar 

  4. Sheng, M., Liao, Y. J., Jan, Y. N. & Jan, L. Y. Presynaptic A-current based on heteromultimeric K+ channels detected in vivo. Nature 365, 72–75 (1993)

    ADS  CAS  Article  Google Scholar 

  5. Wang, H., Kunkel, D. D., Martin, T. M., Schwartzkroin, P. A. & Tempel, B. L. Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 365, 75–79 (1993)

    ADS  CAS  Article  Google Scholar 

  6. Salkoff, L. & Wyman, R. Genetic modification of potassium channels in Drosophila Shaker mutants. Nature 293, 228–230 (1981)

    ADS  CAS  Article  Google Scholar 

  7. Kaplan, W. D. & Trout, W. E. The behaviour of four neurological mutants of Drosophila. Genetics 61, 399–409 (1961)

    Google Scholar 

  8. Hardie, R. C., Voss, D., Pongs, O. & Laughlin, S. B. Novel potassium channels encoded by the Shaker gene in Drosophila photoreceptors. Neuron 6, 477–486 (1991)

    CAS  Article  Google Scholar 

  9. Hardie, R. C. Voltage-sensitive potassium channels in Drosophila photoreceptors. J. Neurosci. 11, 3079–3095 (1991)

    CAS  Article  Google Scholar 

  10. Hardie, R. C. & Raghu, P. Visual transduction in Drosophila. Nature 413, 186–193 (2001)

    ADS  CAS  Article  Google Scholar 

  11. Weckström, M. & Laughlin, S. B. Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci. 18, 17–21 (1995)

    Article  Google Scholar 

  12. Juusola, M. & Hardie, R. C. Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 °C. J. Gen. Physiol. 117, 3–25 (2001)

    CAS  Article  Google Scholar 

  13. Laurent, G. Voltage-dependent nonlinearities in the membrane of locust nonspiking local interneurons, and their significance for synaptic integration. J. Neurosci. 10, 2268–2280 (1990)

    CAS  Article  Google Scholar 

  14. Hoffman, D. A., Magee, J. C., Colbert, C. M. & Johnston, D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869–875 (1998)

    ADS  Article  Google Scholar 

  15. Magee, J., Hoffman, D., Colbert, C. & Johnston, D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu. Rev. Physiol. 60, 327–346 (1998)

    CAS  Article  Google Scholar 

  16. Connor, J. A. & Stevens, C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural soma. J. Physiol. (Lond.) 213, 21–30 (1971)

    CAS  Article  Google Scholar 

  17. Debanne, D., Guérineau, N. C., Gähwiler, B. H. & Thompson, S. M. Action-potential propagation gated by an axonal IA-like K+ conductance in hippocampus. Nature 389, 286–289 (1997)

    ADS  CAS  Article  Google Scholar 

  18. de Ruyter van Steveninck, R. R. & Laughlin, S. B. The rate of information transfer in graded-potential neurons and chemical synapses. Nature 379, 642–645 (1996)

    ADS  CAS  Article  Google Scholar 

  19. Laughlin, S. B. A simple coding procedure enhances a neurone's information capacity. Z. Naturforsch. 36, 910–912 (1981)

    CAS  Article  Google Scholar 

  20. Kouvalainen, E., Weckström, M. & Juusola, M. Determining photoreceptor signal-to-noise ratio in the time and frequency domains with a pseudorandom stimulus. Vis. Neurosci. 95, 1221–1225 (1994)

    Article  Google Scholar 

  21. Shannon, C. E. Communication in the presence of noise. Proc. Inst. Radio Eng. 37, 10–21 (1948)

    MathSciNet  Google Scholar 

  22. Bendat, J. S. & Piersol, A. G. Random Data: Analysis and Measurement Procedures (Wiley & Sons, New York, 1971)

    MATH  Google Scholar 

  23. Hodgkin, A. L. & Huxley, A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117, 500–544 (1952)

    CAS  Article  Google Scholar 

  24. Johnston, D. & Wu, S. M.-S. Foundations of Cellular Neurophysiology (MIT Press, Cambridge, Massachusetts, 1995)

    Google Scholar 

  25. Desai, N. S., Cudmore, R. H., Nelson, S. B. & Turrigiano, G. G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nature Neurosci. 5, 783–789 (2002)

    CAS  Article  Google Scholar 

  26. Stemmler, M. & Koch, C. How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate. Nature Neurosci. 2, 521–527 (1999)

    CAS  Article  Google Scholar 

  27. Brickley, S. G., Revilla, V., Cull-Candy, S. G., Wisden, W. & Farrant, M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409, 88–92 (2001)

    ADS  CAS  Article  Google Scholar 

  28. Henderson, S. R., Reuss, H. & Hardie, R. C. Single photon responses in Drosophila photoreceptors and their regulation by Ca2+. J. Physiol. (Lond.) 524, 179–194 (2000)

    CAS  Article  Google Scholar 

  29. Hevers, W. & Hardie, R. C. Serotonin modulates the voltage dependence of delayed rectifier and Shaker potassium channels in Drosophila photoreceptors. Neuron 14, 845–856 (1995)

    CAS  Article  Google Scholar 

  30. Shampine, L. F. & Reichelt, M. W. The MATLAB ODE suite. SIAM J. Sci. Comput. 18, 1–22 (1997)

    MathSciNet  Article  Google Scholar 

Download references


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.).

Author information

Authors and Affiliations


Corresponding author

Correspondence to Mikko Juusola.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing