AII amacrine cells (AIIACs) are crucial relay stations for rod-mediated signals in the mammalian retina and they receive synaptic inputs from depolarizing and hyperpolarizing bipolar cells (DBCs and HBCs) as well as other amacrine cells. Using whole-cell voltage clamp technique in conjunction with pharmacological tools, we found that the light-evoked current response of AIIACs in the mouse retina is almost completely mediated by two DBC synaptic inputs: a DNQX-resistant component mediated by cone DBCs (DBCCs) through an electrical synapse and a DNQX-sensitive component mediated by rod DBCs (DBC¬Rs). This scheme is supported by AIIAC current responses recorded from two knockout mice. The dynamic range of the AIIAC light response in the Bhlhb4 -/- mouse (which lacks DBCRs) resembles that of the DNQX-resistant component and that of the connexin36 (Cx36) -/- mouse resembles the DNQX-sensitive component. By comparing the light responses of the DBCCs with the DNQX-resistant AIIAC component and light responses of the DBCRs with the DNQX-sensitive AIIAC component, we obtained the input-output relations of the DBCCAIIAC electrical synapse and the DBCRAIIAC chemical synapse. Similar to other glutamatergic chemical synapses in the retina, the DBCRAIIAC synapse is nonlinear. Its highest voltage gain (approximately 5) is found near the dark membrane potential, and it saturates for presynaptic signals larger than 5.5 mV. The DBCCAIIAC electrical synapse is approximately linear (voltage gain of 0.92), consistent with the linear junctional conductance found in retinal electrical synapses. Moreover, relative DBCR and DBCC contributions to the AIIAC response at various light intensity levels are determined.