Eigenmannia, a genus of weakly electric fish, exhibits a specialized behavior known as the jamming avoidance response (JAR). The JAR results in a categorical difference between Eigenmannia that are in groups of conspecifics and those that are alone. Fish in groups exhibit the JAR behavior and thereby experience ongoing, global synchronous 20 - 50 Hz electrosensory oscillations, whereas solitary fish do not. Although previous work has shown that these ongoing signals do not significantly degrade electrosensory behavior, these oscillations nevertheless elicit short-term synaptic depression in midbrain circuits. Because short-term synaptic depression can have profound effects on the transmission of information through synapses, we examined the differences in intracellularly-recorded responses of midbrain neurons in awake, behaving fish to moving electrosensory images under electrosensory conditions that mimic solitary fish and fish in groups. In solitary conditions, moving objects elicited Gaussian or sinusoidal PSPs that commonly exhibited preferential responses to a direction of motion. Surprisingly, when the same stimulus was presented in the presence of the global oscillations, directional selectivity was increased in all neurons tested. The magnitudes of the differences in PSP amplitude for preferred and non-preferred directions were correlated with a measure of short-term synaptic depression in both conditions. The electrosensory consequences of the JAR appear to result in an enhancement of the representation of direction of motion in midbrain neurons. The data also support a role for short-term synaptic depression in the generation and modulation of directional responses.