Shaker K⁺ channels contribute early nonlinear amplification to the light response in Drosophila photoreceptors

We describe the contribution of rapidly inactivating Shaker K⁺ channels to the dynamic membrane properties of Drosophila photoreceptors. Phototransduction was measured in wild-type and Shaker mutant (Sh¹⁴) Drosophila photoreceptors by stimulating with white noise- modulated light contrast and recording the resulting intracellular membrane potential fluctuations. A second-order Volterra kernel series was used to characterize the nonlinear dynamic properties of transduction in the two situations. First-order kernels were indistinguishable in wild-type and Sh¹⁴ photoreceptors, indicating that the basic light transduction machinery was always intact. However, second-order kernels of Shaker mutants lacked a large, early amplification, indicating a novel role for Shaker K⁺ channels in amplifying and accelerating the voltage response of wild-type photoreceptors. A cascade model of two nonlinear static components surrounding one linear dynamic component was able to partially reproduce the experimental responses. Parameters obtained by fitting the model to the experimental data supported the hypothesis that normal Shaker K⁺ channels contribute an early, positive nonlinearity that partially offsets a later attenuating nonlinearity caused by membrane shunting.