Phasic and tonic light responses provide a fundamental division of visual i
nformation that is thought to originate in the inner retina. However, evide
nce presented here indicates that this duality originates in the outer reti
na. In response to a steady light stimulus, the temporal responses of On-bi
polar cells fell into two groups. In one group, the light response peaked a
nd then rapidly declined (tau similar to 400 msec) close to the resting mem
brane potential. At light offset, these cells exhibited a transient afterhy
perpolarization. In the second group of On-bipolar cells, the light respons
e declined 10-fold more slowly and reached a steady depolarization that was
similar to 40% of the peak response. These neurons had a slowly decaying a
fterhyperpolarization at light offset. A metabotropic glutamate antagonist,
(RS)-alpha-cyclopropyl-4-phosphonophenylyglycine (CPPG), blocked light res
ponses in both types of On-bipolar cell. CPPG only slightly depolarized tra
nsient On-bipolar cells, whereas sustained On-bipolar cells were significan
tly depolarized. Inorganic calcium channel blockers disclosed that these di
stinct On-bipolar responses were inherent to the bipolar cell and not attri
butable to synaptic feedback. CPPG had distinct effects on sustained and tr
ansient ganglion cells, similar to its action on bipolar cells. The antagon
ist depolarized and blocked the light responses of sustained ganglion cells
. In transient ganglion cells, CPPG suppressed the On light response but di
d not depolarize the cell or block the Off light response. These results su
ggest that transient and sustained light responses in ganglion cells result
from selective bipolar cell input and that these two fundamental visual ch
annels originate at the dendritic terminals of bipolar cells.