Abstract
Purpose: :
Blue-yellow color discrimination in mammals depends on circuits that compare the activity in short (S-) versus middle (M-) or long (L-) wavelength-sensitive cones. Many species contain retinal ganglion cells (RGCs) that respond to an increase in S-cone and a decrease in M (and/or L) cone stimulation (i.e., S-on/M(L)-off). The small bistratified ganglion cell in the primate is the well-studied example. The S-on signal in these RGCs is relayed from S-cones via a specific S-on bipolar cell. RGCs with (S-off/M(L)-on) responses are observed infrequently in mammals, and the origin of the S-off response is unclear. Non-primates appear to lack S-off bipolar cells, so the S-off ganglion cell responses require an inversion of the S-on bipolar cell response. This hypothesis has never been tested.
Methods: :
We investigated the functional properties and retinal circuitry of S-off/M-on RGCs in the cone dominant ground squirrel (Ictidomys tridecemlineatus) retina by recording with a large-scale multi-electrode array. In each recording, we simultaneously measured the spatiotemporal and chromatic spike triggered-average response of several hundred RGCs to a white noise visual stimulus.
Results: :
S-on/M-off and S-off/M-on RGCs were found in all recordings with as much as several dozens of S-off/M-on cells identified in a single preparation. The receptive fields of both cell types tiled the retina to form independent mosaics. Within a mosaic, receptive fields of neighboring cells had uniform degree of overlap. Relative to the S-on cells, S-off cells had slightly smaller (10-20%) receptive field diameters and consequently higher densities. Metabotropic mGluR6 receptor block by a combination of agonist L-AP4 and antagonist LY341495 suppressed both S-on and S-off responses consistent with a blocking effect at S-on bipolar cells. The S-off responses of the S-off/M-on RGC were blocked by strychnine but not picrotoxin consistent with an inverting role for a glycinergic amacrine cell. Neither strychnine nor picrotoxin blocked the M-on responses of S-off/M-on cells and both had no significant effect on S-on/M-off cells.
Conclusions: :
We conclude that the ground squirrel retina contains a regular mosaic of small receptive field S-off/M-on and S-on/M-off ganglion cells. This finding indicates that these retinal pathways are balanced to relay spatial color information. The S-off response is communicated by an inverting glycinergic amacrine cell, whereas the M-on response most likely arises from a direct innervation by diffuse On bipolar cells.
Keywords: retinal connections, networks, circuitry • color vision • retina: proximal (bipolar, amacrine, and ganglion cells)