Distribution and voltage dependence of ion channels shape single-neuron computations

Voltage-gated ion channels do not distribute evenly in the plasma membrane of a neuron; they localize to distinct domains where they govern the excitability of the cell and the computations it performs. Informed by electron microscopic reconstructions, models of morphologically realistic neurons offer the opportunity to study these computations, but they lack constraints on the subcellular localizations and functional properties of voltage-gated channels. Here, we address this problem in Drosophila melanogaster by developing tools to tag and visualize endogenous ion channels in genetically designated populations of cells and in single neurons. Focusing on a suite of highly expressed ion channels in visual motion-sensitive neurons, we report their subcellular localizations and their steady-state activation and inactivation curves. Integrating these structural and functional data into a biophysically constrained model reproduces the directional tuning of motion-sensitive T5 neurons and reveals the function of voltage-gated sodium channels in nonspiking neurons.