Layers of inhibitory networks shape receptive field properties of AII amacrine cells

In the retina, rod and cone pathways mediate visual signals over a billion-fold range in luminance. AII (“A-two”) amacrine cells (ACs) receive signals from both pathways via different bipolar cells, enabling AIIs to operate at night and during the day. Previous work has examined luminance-dependent changes in AII gap junction connectivity, but less is known about how surrounding circuitry shapes AII receptive fields across light levels. Here, we report that moderate contrast stimuli elicit surround inhibition in AIIs under all but the dimmest visual conditions, due to actions of horizontal cells and at least two ACs that inhibit presynaptic bipolar cells. Under photopic (daylight) conditions, surround inhibition transforms AII response kinetics, which are inherited by downstream ganglion cells. Ablating neuronal nitric oxide synthase type-1 (nNOS-1) ACs removes AII surround inhibition under mesopic (dusk/dawn), but not photopic, conditions. Our findings demonstrate how multiple layers of neural circuitry interact to encode signals across a wide physiological range. [Display omitted] •AII (“A-two”) amacrine cell (AC) receptive fields (RFs) change with increasing luminance•Surround inhibition, absent in scotopic (dim light) AII RFs, emerges at higher light levels•nNOS1 ACs provide inhibitory surround to AIIs under mesopic, but not photopic, conditions•Inhibitory surround observed in some downstream ganglion cell RFs is inherited from AIIs Nath et al. show that receptive fields of AII (“A-two”) amacrine cells (ACs) are shaped by strong surround suppression under mesopic and photopic conditions. Ablating nNOS1 ACs removes mesopic surround only. Changes in AII surround suppression are inherited by downstream RGCs, thereby influencing the retinal output.