Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit retina.

Abstract

1. Intracellular recordings were obtained from 21 amacrine cells and 12 ganglion cells in the isolated, superfused retina-eyecup of the rabbit. Cells were subsequently labeled with horseradish peroxidase (HRP) or N-(2-aminoethyl)-biotinamide hydrochloride (Neurobiotin) for morphologic identification. 2. Initial experiments performed on three amacrine cells and three ganglion cells showed that 1 microM tetrodotoxin (TTX) abolished all spiking. This included both large-amplitude and small-amplitude spikes recorded in many amacrine cells, indicating that they are mediated by voltage-gated sodium channels. 3. The center-receptive-field size of 18 amacrine cells and 9 ganglion cells was measured with the use of a 50-microns-wide/6.0-mm-long rectangular slit of light that was displaced along its minor axis (parallel to the visual streak) in steps as small as 3 microns. The retina was then bathed in 1 microM TTX, or individual cells were injected with 50 mM QX-314, a quatemary lidocaine derivative, to abolish all spiking, and the center-receptive field of each cell was then remeasured. 4. Although TTX blocked spiking in all ganglion cells (dendritic diameters ranging from 302 to 969 microns), it produced no significant change in the size of their center-receptive fields. This finding argues that passive, electrotonic spread of synaptic inputs to ganglion cell dendritic arbors is adequate for efficient propagation from terminal branches to the soma; active propagation via voltage-gated sodium channels plays no apparent role. 5. In contrast, TTX and QX-314 had variable effect on the receptive fields of amacrine cells, which was related to the size of their dendritic arbors. Whereas TTX had no significant effect on the receptive-field size of amacrine cells whose dendritic arbors were < 525 microns across, the center-receptive fields of larger amacrine cells were reduced, on average, by 40%; QX-314 produced a very similar average reduction of 39%. Moreover, for these larger cells, there was a direct relationship between the magnitude of the reduction in receptive-field size produced by TTX or QX-314 and the size of a cell's dendritic arbor. This relationship was true whether the change in receptive-field size was measured in absolute terms or as percent reduction from control values. 6. Interestingly, TTX and QX-314 also significantly reduced the amplitude of slow potentials recorded in amacrine cells by an average of 22 and 24%, respectively. However, the amplitude of slow potentials recorded in ganglion cells were relatively uneffected by TTX. 7. These findings are consistent with the idea that, for amacrine cells with dendritic arbors spanning > 525 microns, active propagation of synaptic signals mediated by voltage-gated sodium channels is necessary for efficient movement of information across a cell's dendritic arbor and thus plays a major role in shaping their receptive fields. Although the TTX effects may also reflect an indirect contribution from altered synaptic input derived from presynaptic spiking neurons, the strong similarity between the effects of TTX and QX-314 argues that any such contribution was minor. For smaller amacrine cells, passive, electrotonic spread of signals appears adequate for efficient propagation within their limited dendritic arbors.