Three Levels of Lateral Inhibition: A Space-Time Study of the Retina of the Tiger Salamander

The space-time patterns of activity generated across arrays of retinal neurons can provide a sensitive measurement of the effects of neural interactions underlying retinal activity. We measured the excitatory and inhibitory components associated with these patterns at each cellular level in the retina and further dissected inhibitory components pharmacologically. Using perforated and loose patch recording, we measured the voltages, currents, or spiking at 91 lateral positions covering approximately 2 mm in response to a flashed 300-microm-wide bar. First, we showed how the effect of well known lateral inhibition at the outer retina, mediated by horizontal cells, evolved in time to compress the spatial representation of the stimulus bar at ON and OFF bipolar cell bodies as well as horizontal cells. Second, we showed, for the first time, how GABA(C) receptor mediated amacrine cell feedback to bipolar terminals compresses the spatial representation of the stimulus bar at ON bipolar terminals over time. Third, we showed that a third spatiotemporal compression exists at the ganglion cell layer that is mediated by feedforward amacrine cells via GABA(A) receptors. These three inhibitory mechanisms, via three different receptor types, appear to compensate for the effects of lateral diffusion of activity attributable to dendritic spread and electrical coupling between retinal neurons. As a consequence, the width of the final representation at the ganglion cell level approximates the dimensions of the original stimulus bar.