Motion vision circuits of the fly are organized into parallel ON and OFF pathways tuned to the direction and speed of motion. Directionally selective small-field columnar neurons innervate the third optic ganglion, the lobula plate, where their outputs are integrated by large dendritic fields that encode wide-field background motion. Wide-field lobula plate cells, in turn, coordinate gaze stabilization. By contrast, behavioral responses to visual features is believed to begin within the circuits of the fourth optic ganglion, the lobula. We investigated 19 lobula columnar neurons (LCs) with stimuli that are behaviorally salient to the fly. A comprehensive analysis of receptive field properties showed that LC15 encodes moving bars, whereas LC12 is relatively agnostic to object dimensions. Neither responds to optic flow, rather object responses in both LCs are suppressed by background motion. Further contrasting neurons of the motion pathway, LC12 and LC15 are both small-field cells indifferent to ON-OFF contrast polarity. LC15 responds equally to four directions of motion, whereas LC12 is selective for motion in the horizontal plane. Both are equally sensitive to object speeds ranging from 22 to 132° per second. Small objects strongly stimulate presynaptic fibers of lobula layer 2, which corresponds to the postsynaptic domains of object-detecting LCs. Finally, in direct contrast to the entire motion pathway, we were surprised to find that octopamine nullifies the inhibition of object responses generated by background motion; LC12 and LC15 remain sensitive to objects appearing against a moving background.