Abstract
Purpose :
Center-surround antagonism(CSA) alters retinal ganglion cell(RGC) sampling of spatial inputs in bright light conditions but has appeared to be absent in scotopic light. While we confirm classical CSA in primate retina, we also observed non-classical effects due to surround input in dim light. Here, we investigated the non-classical spatial and temporal filtering properties of RGCs in dim light and probed the potential mechanisms mediating surround-dependent effects.
Methods :
Electrophysiological recordings were made from ON parasol RGCs in RPE-attached, flat-mounted macaque retinas. RGCs were stimulated with spatially- and temporally-defined patterns with scotopic to low-photopic light. CSA was probed using spot-annulus stimuli to independently control the stimulation of the center vs surround. Short contrast steps and noise sequences were used to explore the temporal dependence on surround inhibition.
Results :
Classic CSA was confirmed in RGC spatial receptive fields in mesopic and photopic conditions and was absent in scotopic conditions. Despite this, the center dimensions continued to narrow as background intensity increased. Pharmacology confirmed that the decreases in center persist without horizontal cell feedback. Subunits were also substantially larger in dim light and narrowed with increasing intensity. The time required for the receptive field to stabilize after the light was increased from 0.1 to 10 R*/rod/s was ~30s. We found that surround activation shaped the kinetics of RGC responses in dim light. The responses to contrast steps and the noise-derived linear filters reached a peak more quickly when surrounds were illuminated. We simulated the responses to the steps by convolving the appropriate linear filter with the step stimulus. The predicted responses showed most of the surround-dependent differences in the time to peak of the recorded waveforms, but they did not fully explain the transience of the response following step onset.
Conclusions :
CSA mechanisms drive temporal and spatial filtering in dim light. Alterations in kinetics are particularly notable in dim light since rod photoreceptor signaling is notoriously slow, providing ample opportunity for significant temporal filtering in downstream circuits. Modulation of inputs in the spatial and temporal domains are likely to determine threshold sensitivity for complex tasks like motion detection in dim light.
This abstract was presented at the 2022 ARVO Annual Meeting, held in Denver, CO, May 1-4, 2022, and virtually.