GABA-Mediated Inhibition Between Amacrine Cells in the Goldfish Retina

Abstract

Retinal amacrine cells have abundant dendro-dendritic synapses between neighboring amacrine cells. Therefore an amacrine cell has both presynaptic and postsynaptic aspects. To understand these synaptic interactions in the amacrine cell, we recorded from amacrine cells in the goldfish retinal slice preparation with perforated- and whole cell-patch clamp techniques. As the presynaptic element, 19% of the cells recorded (15 of 78 cells) showed spontaneous tetrodotoxin (TTX)-sensitive action potentials. As the postsynaptic element, all amacrine cells ( n = 9) were found to have GABA-evoked responses and, under perforated patch clamp, 50 μM GABA hyperpolarized amacrine cells by activating a Cl− conductance. Bicuculline-sensitive spontaneous postsynaptic currents, carried by Cl−, were observed in 82% of the cells (64 of 78 cells). Since the source of GABA in the inner plexiform layer is amacrine cells alone, these events are likely to be inhibitory postsynaptic currents (IPSCs) caused by GABA spontaneously released from neighboring amacrine cells. IPSCs were classified into three groups. Large amplitude IPSCs were suppressed by TTX (1 μM), indicating that presynaptic action potentials triggered GABA release. Medium amplitude IPSCs were also TTX sensitive. Small amplitude IPSCs were TTX insensitive (miniature IPSCs; n = 26). All of spike-induced, medium amplitude, and miniature IPSCs were Ca2+ dependent and blocked by Co2+. Blocking of glutamatergic inputs bydl-2-amino-phosphonoheptanoate (AP7; 30 μM) and 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 2 μM) had almost no effect on spontaneous GABA release from presynaptic amacrine cells. We suggest that these dendro-dendrotic inhibitory networks contribute to receptive field spatiotemporal properties.