We serendipitously discovered that the preferred-direction responses of ON–OFF directionally selective (DS) ganglion cells in the rabbit retina fall as a function of contrast when the contrast of a moving bar exceeds about 100%. Null-direction responses did not fall for contrasts up to 400%. Because the non-monotonic (rise-then-fall) behavior as a function of contrast occurred only for preferred-direction responses, it must depend on the mechanism of directional selectivity. It became thus of interest to investigate how this non-monotonicity depends on the major synapses involved in directional selectivity. Blockades of nicotinic acetylcholine (ACh) and NMDA glutamate receptors reduced responses without eliminating preferred-response non-monotonicity. Blocking GABAergic inhibition, however, did eliminate non-monotonicity. These results pose a difficult puzzle, since in the accompanying paper (Grzywacz et al., 1998), we showed that residual responses under combined nicotinic and NMDA blockades are not statistically significantly directionally selective. How is it possible that null-direction GABAergic inhibition affects non-nicotinic-non-NMDA residual responses without generating directional selectivity? This may happen if there exists an asymmetric GABAergic input to distal dendrites of the DS cell while the excitatory, non-nicotinic-non-NMDA input is to proximal dendrites. In support of this hypothesis, bath-applied GABA reduces responses to exogenous ACh under synaptic block, providing for the first time in the rabbit's retina, direct evidence of GABA receptors on DS cells.