The diversity of ganglion cells in a mammalian retina

Abstract

We report a survey of the population of ganglion cells in the rabbit retina. A random sample of 301 neurons in the ganglion cell layer was targeted for photofilling, a method in which the arbors of the chosen neurons are revealed by diffusion of a photochemically induced fluorescent product from their somas. An additional 129 cells were labeled by microinjection of Lucifer yellow. One hundred and thirty-eight cells were visualized by expression of the gene encoding a green fluorescent protein, introduced by particle-mediated gene transfer. One hundred and sixty-six cells were labeled by particle-mediated introduction of DiI. In the total population of 734 neurons, we could identify 11 types of retinal ganglion cell. An analysis based on retinal coverage shows that this number of ganglion cell types would not exceed the available total number of ganglion cells. Although some uncertainties remain, this sample appears to account for the majority of the ganglion cells present in the rabbit retina. Some known physiological types could easily be mapped onto structural types, but half of them could not; a large set of poorly known codings of the visual input is transmitted to the brain.

Fig. 1.

ON-OFF directionally selective ganglion cells (G7 in this nomenclature) as shown by each of our cell-filling methods. The cells are distinguished by their bistratified, medium-field, arbor and recurving dendrites (Amthor et al., 1989b; Vaney, 1994; Yang and Masland, 1994). The cells are bistratified, and an out-of-focus arbors can be glimpsed for the Lucifer-filled cell, which was photographed using an objective with low numerical aperture.

Fig. 2.

The major types of ganglion cells identified in our series. Methods of filling were as follows: G1, Top, Lucifer, immunolabeled to diaminobenzidine; bottom, DiI;G2, top and bottom, DiI;G3, ON and OFF Arbor, DiI;G4 ON, Lucifer immunolabeled to diaminobenzidine;G4 OFF, DiI; G5, top, GFP;bottom, DiI; G6, top, DiI;bottom, photofill; G8, top andbottom, photofill; G9,topand bottom, GFP; G10, top andbottom, GFP; G11 ON, Lucifer yellow;G11 OFF, DiI. Scale bars, 100 μm. (Figure 2continues.)

Fig. 2.

The major types of ganglion cells identified in our series. Methods of filling were as follows: G1, Top, Lucifer, immunolabeled to diaminobenzidine; bottom, DiI;G2, top and bottom, DiI;G3, ON and OFF Arbor, DiI;G4 ON, Lucifer immunolabeled to diaminobenzidine;G4 OFF, DiI; G5, top, GFP;bottom, DiI; G6, top, DiI;bottom, photofill; G8, top andbottom, photofill; G9,topand bottom, GFP; G10, top andbottom, GFP; G11 ON, Lucifer yellow;G11 OFF, DiI. Scale bars, 100 μm. (Figure 2continues.)

Fig. 2.

The major types of ganglion cells identified in our series. Methods of filling were as follows: G1, Top, Lucifer, immunolabeled to diaminobenzidine; bottom, DiI;G2, top and bottom, DiI;G3, ON and OFF Arbor, DiI;G4 ON, Lucifer immunolabeled to diaminobenzidine;G4 OFF, DiI; G5, top, GFP;bottom, DiI; G6, top, DiI;bottom, photofill; G8, top andbottom, photofill; G9,topand bottom, GFP; G10, top andbottom, GFP; G11 ON, Lucifer yellow;G11 OFF, DiI. Scale bars, 100 μm. (Figure 2continues.)

Fig. 2.

The major types of ganglion cells identified in our series. Methods of filling were as follows: G1, Top, Lucifer, immunolabeled to diaminobenzidine; bottom, DiI;G2, top and bottom, DiI;G3, ON and OFF Arbor, DiI;G4 ON, Lucifer immunolabeled to diaminobenzidine;G4 OFF, DiI; G5, top, GFP;bottom, DiI; G6, top, DiI;bottom, photofill; G8, top andbottom, photofill; G9,topand bottom, GFP; G10, top andbottom, GFP; G11 ON, Lucifer yellow;G11 OFF, DiI. Scale bars, 100 μm. (Figure 2continues.)

Fig. 2.

The major types of ganglion cells identified in our series. Methods of filling were as follows: G1, Top, Lucifer, immunolabeled to diaminobenzidine; bottom, DiI;G2, top and bottom, DiI;G3, ON and OFF Arbor, DiI;G4 ON, Lucifer immunolabeled to diaminobenzidine;G4 OFF, DiI; G5, top, GFP;bottom, DiI; G6, top, DiI;bottom, photofill; G8, top andbottom, photofill; G9,topand bottom, GFP; G10, top andbottom, GFP; G11 ON, Lucifer yellow;G11 OFF, DiI. Scale bars, 100 μm. (Figure 2continues.)

Fig. 3.

Unclassified cells. A shows a small cell, clearly filled but rarely encountered by any of our methods; these appear to be developmental accidents. B–D show medium-field cells that we were unable confidently to assign to one of the other types. All are labeled with DiI. Scale bars, 100 μm.

Fig. 4.

The branching and level of stratification for the 11 types of neuron identified. Scale bar, 100 μm.