Voltage-gated K⁺ channels are important in neuronal signaling, but little is known of their interactions with receptor currents or their behavior during natural stimulation. We used nonparametric and parametric nonlinear modeling of experimental responses, combined with Hodgkin-Huxley style simulation, to examine the roles of K⁺ channels in forming the responses of wild type (WT) and Shaker mutant (Sh¹⁴) Drosophila photoreceptors to naturalistic stimulus sequences. Naturalistic stimuli gave different results than similar experiments with white noise stimuli. Sh¹⁴ responses were larger and faster than WT. Simulation indicated that, in addition to eliminating the Shaker current, the mutation changed the current flowing through light dependent channels (Light Induced Current, or LIC) and increased the delayed rectifier current. Part of the change in LIC could be attributed to direct feedback from the voltage-sensitive ion channels to the light-sensitive channels via the membrane potential. However, we argue that other changes occur in the light detecting machinery of Sh¹⁴ mutants, possibly during photoreceptor development.