The theory of "parallel pathways" predicts that, except for a sign reversal, ON and OFF ganglion cells are driven by a similar presynaptic circuit. To test this hypothesis, we measured synaptic inputs to ON and OFF cells as reflected in the subthreshold membrane potential. We made intracellular recordings from brisk-transient (Y) cells in the in vitro guinea pig retina and show that ON and OFF cells in fact express significant asymmetries in their synaptic inputs. An ON cell receives relatively linear input that modulates a single excitatory conductance; whereas an OFF cell receives rectified input that modulates both inhibitory and excitatory conductances. The ON pathway, blocked by L-AP-4, tonically inhibits an OFF cell at mean luminance and phasically inhibits an OFF cell during a light increment. Our results suggest that basal glutamate release is high at ON but not OFF bipolar terminals, and inhibition between pathways is unidirectional: ON --> OFF. These circuit asymmetries explain asymmetric contrast sensitivity observed in spiking behavior.