Abstract
Purpose :
Extracting oriented structure in natural scenes is a fundamental and highly conserved computation in the visual system. Orientation selective (OS) ganglion cells (osRGCs) have been identified in the retina, but many features of their responses remain unclear. Thus, we sought to understand the receptive field (RF) structure of osRGCs, how the retina produces OS, and whether OS is maintained across rod and cone vision.
Methods :
We measured RGC responses to visual stimuli from ex vivo rat retinas using a large-scale multi-electrode array. We used drifting and contrast reversing gratings to identify osRGCs and determine their spatial frequency tuning. We used checkerboard noise to estimate RF structure. A linear-nonlinear model based on the estimated RF was used to determine the extent to which osRGCs perform linear spatial integration.
Results :
Consistent with previous work, we found osRGCs with peak tuning along either the horizontal or vertical meridians. However, among osRGCs, we identified two distinct types of RFs. Some osRGCs exhibited RFs reminiscent of cortical simple cells: their responses had narrow spatial frequency tuning and were highly phase-dependent. Importantly, they had an OFF-center RF flanked by ON-responsive zones, producing an even-symmetric RF that accurately predicted visual responses, indicating a relatively linear RF. Other osRGCs exhibited RFs similar to cortical complex cells: their responses had broad spatial frequency tuning that weakly depended on phase. Furthermore, like cortical complex cells, their linear RF had a speckled organization with small ON and OFF subzones that poorly predicted their visual responses, indicating a nonlinear RF. Both kinds of osRGCs maintained tuning down to rod-mediated light levels, and tuning was largely eliminated by blocking GABAa receptors.
Conclusions :
We demonstrate two distinct RF structures among osRGCs that parallel the division of simple and complex cells in primary visual cortex. These results suggest that the emergence of simple and complex OS tuning emerges first in the retina, at least in rodents. Both forms of tuning span rod to cone vision. Finally, both forms of tuning depend on GABAa receptors, suggesting that they are mediated by feedforward inhibition onto RGCs. Intracellular measurements will be needed to understand how these simple- and complex-like responses are achieved by retinal circuits.
This abstract was presented at the 2022 ARVO Annual Meeting, held in Denver, CO, May 1-4, 2022, and virtually.