Analyses of active and passive membrane properties predict an asymmetry in the spread of electrical current through a neuron. Simulated current injection into a large-diameter compartment of a biophysically realistic model neuron causes a local potential shift that can spread throughout the cell. In contrast, causing the same local potential shift in the dendritic tip of the same neuron results in only minimal changes in electrical potential in the rest of the cell. Using calcium as a reporter of electrical activity in neurons in the fly's lobula plate we find that current injected into the thick axon caused depolarization throughout the cell, whereas activation of a dendritic region remained local. These results have important implications for the ability of integrating neurons to perform local computations of synaptic input without additional hardware.