High-resolution electrical stimulation of primate retina for epiretinal implant design.

The development of retinal implants for the blind depends crucially on understanding how neurons in the retina respond to electrical stimulation. This study used multielectrode arrays to stimulate ganglion cells in the peripheral macaque retina, which is very similar to the human retina. Analysis was restricted to parasol cells, which form one of the major high-resolution visual pathways in primates. Individual cells were characterized using visual stimuli, and subsequently targeted for electrical stimulation using electrodes 9-15 microm in diameter. Results were accumulated across 16 ON and 9 OFF parasol cells. At threshold, all cells responded to biphasic electrical pulses 0.05-0.1 ms in duration by firing a single spike with latency lower than 0.35 ms. The average threshold charge density was 0.050 +/- 0.005 mC/cm(2), significantly below established safety limits for platinum electrodes. ON and OFF ganglion cells were stimulated with similar efficacy. Repetitive stimulation elicited spikes within a 0.1 ms time window, indicating that the high temporal precision necessary for spike-by-spike stimulation can be achieved in primate retina. Spatial analysis of observed thresholds suggests that electrical activation occurred near the axon hillock, and that dendrites contributed little. Finally, stimulation of a single parasol cell produced little or no activation of other cells in the ON and OFF parasol cell mosaics. The low-threshold, temporally precise, and spatially specific responses hold promise for the application of high-density arrays of small electrodes in epiretinal implants.