Short-term depression at the reciprocal synapses between a retinal bipolar cell terminal and amacrine cells.

Visual adaptation is thought to occur partly at retinal synapses that are subject to plastic changes. However, the locus and properties of this plasticity are not well known. Here, we studied short-term plasticity at the reciprocal synapse between bipolar cell terminals and amacrine cells in goldfish retinal slices. Depolarization of a single bipolar cell terminal for 100 ms triggers the release of glutamate onto amacrine cell processes, which in turn leads to GABAergic feedback from amacrine cells onto the same terminal. We find that this release of GABA undergoes paired-pulse depression (PPD) that recovers in <1 min (single exponential time constant, tau approximately = 12 s). This disynaptic PPD is independent of mGluR-mediated plasticity and depletion of glutamatergic synaptic vesicle pools, because exocytosis assayed via capacitance jumps (deltaC(m)) recovered completely after 10 s (tau approximately = 2 s). Fast application of GABA (10 mM) onto outside-out patches excised from bipolar cell terminals showed that the recovery of GABA(A) receptors from desensitization depends on the duration of the application [fast recovery (<2 s) for short applications; slow (tau approximately = 12 s) for prolonged applications]. We thus blocked GABA(A) receptors and retested the GABAergic response mediated by nondesensitizing GABA(C) receptors to two rapid glutamate puffs onto the bipolar cell terminal. These responses consistently displayed PPD. Furthermore, blocking AMPA-receptor desensitization with cyclothiazide, or evoking GABA release with NMDA receptors, did not reduce PPD. We thus suggest that depletion of synaptic vesicle pools in GABAergic amacrine cells is a major contributor to PPD.