Selective Ablation of a Class of Amacrine Cells Alters Spatial Processing in the Retina

Abstract

Several recent studies have suggested that the spatial tuning of retinal ganglion cells may be a more complex process than previously thought. The working hypothesis for many years was that the tuning was shaped by operations performed in the first synaptic layer of the retina, but recent work shows that operations in the second synaptic layer, involving amacrine cells, also play a significant role (Cook and McReynolds, 1998; Taylor, 1999; Flores-Herr et al., 2001). Although it is clear that amacrine cells are involved, the precise roles of the different amacrine subtypes in the many aspects of spatial tuning have not yet been established. Here we used a cell class ablation method to remove one subtype, the neuropeptide Y-expressing cells (NPY cells), and tapped into a part of the circuitry that tunes ganglion cells toward large spatial patterns (low spatial frequencies). When the subtype was ablated, ganglion cells tuned toward low spatial frequencies, both ON- and OFF-type cells, lost this preferential tuning. The effect was specific because ablation of another amacrine subtype did not produce it. Further analysis showed that the change in tuning was attributable to a decrease in the receptive field surround size of the ganglion cell. Other parameters, such as the size, strength, and asymmetry of the center and the strength of the surround, were not statistically significantly affected. These results thus show a mechanism for tuning cells to low spatial frequencies; an operation in the second synaptic layer, mediated by NPY cells, extends the surround of the ganglion cell.