Primate horizontal cell dynamics: An analysis of sensitivity regulation inthe outer retina

The human cone visual system maintains sensitivity over a broad range of il lumination, from below 1 troland to 1,000,000 trolands. While the cone phot oreceptors themselves are an important locus for sensitivity regulation-or light adaptation-the degree to which they contribute in primates remains un clear. To determine the range of sensitivity regulation in the outer retina , the temporal dynamics, neural gain control, and response range compressio n were measured in second-order neurons, the H1 horizontal cells, of the ma caque retina. Situated at the first synapse in the retina, H1 cells receive input from a large population of cones. Lee et al. have previously shown t hat sensitivity regulation in H1 cells is both cone type-specific and spati ally restricted. The sensitivity regulation seen in H1 cells at moderate il luminances thus takes place before the summation of cone signals in these c ells, and the data establish the H1 cell as a convenient locus for analyzin g cone signals. In the present study, cone-driven responses of primate H1 c ells to temporally modulated sine-wave stimuli and to increment pulses were measured at steady levels of 1-1,000 trolands. The H1 cell gave a modulate d response to sine-wave stimuli and hyperpolarized to increment pulses with overshoots at stimulus onset and offset. The temporal amplitude sensitivit y function was primarily low-pass in shape, with a small degree of low-freq uency roll off and a resonance shoulder near 40 Hz. A model incorporating a cascade of first-order filters together with an underdamped second-order f ilter could describe both temporal sinusoidal and pulse hyperpolarizations. Amplitude sensitivity was estimated from both pulse and sine-wave data as a function of the steady adaptation level. Sensitivity at low light levels (1 troland) showed a slowing in temporal dynamics, indicating time-dependen t sensitivity regulation. Sensitivity was reduced at light levels above app roximately 10 trolands, reflecting both response range compression and neur al gain control. Thus the outer retina is a major locus for sensitivity reg ulation in primates.