The two major excitatory synapses onto ON–OFF
directionally selective (DS) ganglion cells of the rabbit
retina appear to be nicotinic cholinergic and NMDA glutamatergic.
Blockade of either of these synapses with antagonists does
not eliminate directional selectivity. This suggests that
these synapses may have complementary roles in the computation
of the direction of motion. To test this hypothesis, quantitative
features of the DS cell excitatory pathways were determined
by collecting responses, under nicotinic and/or NMDA blockade,
to a sweeping bar, hyperacute apparent motions, or a drifting
sinusoidal grating. Sweeping bar responses were reduced,
but directional selectivity not eliminated, by blockade
of either excitatory path, as previously shown (Cohen &
Miller, 1995; Kittila & Massey, 1997). However, residual
responses under combined blockades were not statistically
significantly DS. NMDA blockade reduced responses more
than nicotinic blockade for each protocol, and shifted
hyperacute motion thresholds to higher values. This supported
the notion that glutamate provides the main excitatory
drive to DS cells, that is, the one responsible for contrast
sensitivity. In turn, nicotinic, but not NMDA blockade
eliminated directional selectivity to a drifting low spatial-frequency
sinusoidal grating in these cells. This suggested that
acetylcholine (ACh) is the main excitatory input with regards
to directional selectivity for some textured stimuli, that
is, those with multiple peaks in their spatial luminance
profile. Moreover, nicotinic blockade raised the low temporal-frequency
cutoff of the grating responses, consistent with the proposal
that preferred-direction facilitation, which is temporally
sustained, is dependent on the cholinergic input. These
different properties of the NMDA and nicotinic pathways
are consistent with a recently proposed two-asymmetric-pathways
model of directional selectivity.