Retinal ganglion cell maps in the brain: implications for visual processing

Abstract

Everything the brain knows about the content of the visual world is built from the spiking activity of retinal ganglion cells (RGCs). As the output neurons of the eye, RGCs include ∼20 different subtypes, each responding best to a specific feature in the visual scene. Here we discuss recent advances in identifying where different RGC subtypes route visual information in the brain, including which targets they connect to and how their organization within those targets influences visual processing. We also highlight examples where causal links have been established between specific RGC subtypes, their maps of central connections and defined aspects of light-mediated behavior and we suggest the use of techniques that stand to extend these sorts of analyses to circuits underlying visual perception.

Figure 1

Intrinsically photosensitive retinal ganglion cell subtypes (ipRGCs), their connections in the brain and their influence on various aspects of light-mediated behaviors.

Figure 2

Retinal ganglion cell maps in the superior colliculus identified from genetic labeling studies in the mouse. (a) Four subtypes of RGCs, each encoding a different specific feature of the visual environment. W3 RGCs encode local object motion [42]. On-Off DSGCs encode directional motion [38^••,41]. J-RGCs are Off-DSGCs [37^••] and alpha RGCs respond to center-surround stimuli [43^•]. (b) Diagram of mouse head and brain showing the position of the two eyes, optic nerves and tracts and the two bilateral superior colliculi. On the right is a higher magnification view of one superior colliculus with the four RGC axonal maps stacked across its depth. (c) View of the four different RGC axon layers across the depth of the retinorecipient SC (comprised of upper and lower stratum griseum superficialis; uSGS, and lSGS respectively). Examples of collicular neurons that restrict their dendrites to individual or few sublaminae as well as a collilcular neuron that extends its arbor across all four RGC axon layers are shown to illustrate the possible modes of convergence for the various RGC maps.

Figure 3

Calcium imaging of activity in RGC axons in the zebrafish tectum revealed direction and orientation maps. (a) Schematic of basic experimental design: larval zebrafish sequentially viewed bars moving in one of 12 different directions while the activity of RGCs was measured at the level of their axon terminals within the tectum. (b) Response maps to three different orientations and directions (see Ref. [51^••] for details). (c) Composite maps of direction tuned RGC axons and orientation tuned RGC axons in the tectum, color-coded and combined.

Figure 4

Laminar specific mapping and target neuron responses in the lateral geniculate of the mouse. (a) Diagram of the mouse dLGN with its shell and core regions and the termination zones where the axons of the various genetically identified subtypes of DSGCs synapse. The terminations of axons from alpha RGCs in the core region are also shown. (b) Schematic of the RGC inputs to dLGN neurons. (c) Polar plots of direction selective, orientation selective, and center-surround neurons that were recorded from the mouse dLGN. See Ref. [59^••] for details.

Figure 5

Schematic of the accessory optic system in the mouse (adapted from [83] and [74^••]). The axes of directional motion encoded by the four genetically identified subtypes of DSGCs that connect to the AOS are shown. The diagram on the right depicts the subcortical visual pathway with two optic nerves (on), optic tract and accessory optic tracts, as well as various AOS targets such as the medial terminal nucleus (MTN), nucleus of the optic tract (NOT) and dorsal terminal nucleus (DTN). The superior colliculus (SC) is also shown. The color scheme matches the different DSGC subtypes (left panel with mouse) that project along each pathway and target. Sup. fac. of AOT = superior fasciculus of the accessory optic tract and inf. fasc. of AOT = inferior fasciculus of the AOT.