Neurons of the human retina: A Golgi study

Abstract

Golgi techniques have been applied to post mortem specimens of human retina. Analysis was possible on 150 human retinas processed and viewed by light microscopy as wholemounts. Camera lucida drawings and photography were used to classify the impregnated neurons into 3 types of horizontal cell, 9 types of bipolar cell, 24 basic types of amacrine cell, a single type of interplexiform cell, and 18 types of ganglion cell. We have distinguished two types of midget bipolar cell: fmB (flat) and imB (invaginating). In central retina, both types are typically single‐headed, each clearly contacting a single cone. Peripherally, they may be two‐ or even three‐headed, obviously contacting more than one cone. Two types of small‐field diffuse cone bipolars occurring as flat and invaginating varieties are found across the entire retina from fovea to far periphery. The single rod bipolar type appears about 1 mm from the fovea and increases in dendritic tree diameter from there into the far periphery. The putative „ON‐center”︁ blue cone bipolar and the giant bistratified bipolar first described by Mariani are also present in human retina and we add two previously undescribed bipolar cell types: a putative giant diffuse invaginating and a candidate „OFF‐center”︁ blue cone bipolar. Taking into account the variation of cell size with eccentricity at all points on the retina, we observed three distinct varieties of horizontal cell. The HI is the well known, long‐axon‐bearing cell of Polyak. HII is the more recently described multibranched, wavy‐axoned horizontal cell. The third variety, HIII, introduced here, has been separated from the HI type on morphological criteria of having a larger, more asymmetrical dendritic field and in contacting 30% more cones than the HI at any point on the retina. Amacrine cells proved to be most diverse in morphology. Many of the amacrine cell types that have been described in cat retina (Kolb et al., '81: Vision Res. 21;1081–1114) were seen in this study. Where there are no equivalent cells in cat, we have adopted the descriptive terminology used by Mariani in monkey retina. Thus eight varieties of small‐field amacrines (under 100 μm dendritic trees), eight varieties of medium‐field cells (100–500 μm dendritic span), and eight large‐field varieties (over 500 μm dendritic trees) have been classified. Often a broadly described variety of amacrine cell can be subdivided into as many as three subtypes dependent on stratification levels of their dendrites in the inner plexiform layer. Only a single morphological type of interplexiform cell has been seen in this study. Its diffusely branched dendritic tree in the inner plexiform layer and loosely branched, appendage‐ladened process in the outer plexiform layer suggest that it is homologous to the GABAergic interplexiform cell of the cat retina. As with amacrine cells, wherever possible, ganglion cells in human retina have been classified according to the scheme in cat retina. However, the major groups of ganglion cells are unique to the primate. Ganglion cells with the smallest dendritic trees, originally called midget ganglion cells, are herein called P1 cells, to denote that they are a type of ganglion cell that projects to the parvocellular layers of the lateral geniculate nucleus. P1 ganglion cells occur in high branching (a‐type) and low branching (b‐type) pairs across the entire retina. They have dendritic trees varying from 5 μm at the fovea to 20 μm diameter at 10 mm eccentricity. P1 cells of peripheral retina can become double‐headed presumably to contact two midget bipolar cells. P2 cells are so named because they also project to the parvocellular layers of the LGN and occur as a‐ and b‐types. In human retina this cell type has a dendritic tree ranging from 10 to 100 μm in size over an eccentricity of 14 μm. In contrast, the magnocellular projecting ganglion cells, herein called M cells, have dendritic trees increasing in diameter from 20 to 330 μm with eccentricity to 14 mm. All but six of the ganglion cell types G3 to G23 of cat have also been seen in the human retina.