Inhibitory mechanisms that generate centre and surround properties in ON and OFF brisk-sustained ganglion cells in the rabbit retina

Key points ON and OFF cells in the retina are excited by increases and decreases in visual contrast, respectively. ON and OFF brisk-sustained ganglion cells (BSGCs) have antagonistic centre-surround receptive fields; a visual stimulus that excites the centre is inhibitory in the surround. Such lateral inhibition enhances sensitivity to contrast borders. This study provides the first detailed comparison of visually evoked, excitatory and inhibitory synaptic inputs driving the centres and surrounds of ON and OFF BSGCs. GABAergic lateral inhibition suppresses excitatory inputs to BSGCs presynaptically, via GABAC receptors at ON BSGCS and GABAA and GABAC receptors at OFF BSGCs. Feed-forward glycinergic inhibition, driven through the ON pathway, contributes to centre but not surround responses in both cell types. Centre excitation is mediated by AMPA receptors in ON BSGCs, and NMDA and AMPA receptors in OFF BSGCs. The results reveal mechanistic differences in homologous neural circuits that perform a similar neural computation in the visual system. Abstract Lateral inhibition produces the centre-surround organization of retinal receptive fields, in which inhibition driven by the mean luminance enhances the sensitivity of ganglion cells to spatial and temporal contrast. Surround inhibition is generated in both synaptic layers; however, the synaptic mechanisms within the inner plexiform layer are not well characterized within specific classes of retinal ganglion cell. Here, we compared the synaptic circuits generating concentric centre-surround receptive fields in ON and OFF brisk-sustained ganglion cells (BSGCs) in the rabbit retina. We first characterized the synaptic inputs to the centre of ON BSGCs, for comparison with previous results from OFF BSGCs. Similar to wide-field ganglion cells, the spatial extent of the excitatory centre and inhibitory surround was larger for the ON than the OFF BSGCs. The results indicate that the surrounds of ON and OFF BSGCs are generated in both the outer and the inner plexiform layers. The inner plexiform layer surround inhibition comprised GABAergic suppression of excitatory inputs from bipolar cells. However, ON and OFF BSGCs displayed notable differences. Surround suppression of excitatory inputs was weaker in ON than OFF BSGCs, and was mediated largely by GABAC receptors in ON BSGCs, and by both GABAA and GABAC receptors in OFF BSGCs. Large ON pathway-mediated glycinergic inputs to ON and OFF BSGCs also showed surround suppression, while much smaller GABAergic inputs showed weak, if any, spatial tuning. Unlike OFF BSGCs, which receive strong glycinergic crossover inhibition from the ON pathway, the ON BSGCs do not receive crossover inhibition from the OFF pathway. We compare and discuss possible roles for glycinergic inhibition in the two cell types.