Axon-bearing amacrine cells of the macaque monkey retina

Abstract

A new and remarkable type of amacrine cell has been identified in the primate retina. Application of the vital dye acridine orange to macaque retinas maintained in vitro produced a stable fluorescence in the somata of apparently all retinal neurons in both the inner nuclear and ganglion cell layers. Large somata (∼15-20 μm diam) were also consistently observed in the approximate center of the inner plexiform layer (IPL). Intracellular injections of horseradish peroxidase (HRP) made under direct microscopic control showed that the cells in the middle of the IPL constitute a single, morphologically distinct amacrine cell subpopulation. An unusual and characteristic feature of this cell type is the presence of multiple axons that arise from the dendritic tree and project beyond it to form a second, morphologically distinct arborization within the IPL; these cells have thus been referred to as axon-bearing amacrine cells. The dendritic tree of the axon-bearing amacrine cell is highly branched (∼40-50 terminal dendrites) and broadly stratified, spanning the central 50% of the IPL so that the soma is situated between the outermost and innermost branches. Dendritic field size increases from ∼200 μm in diameter within 2 mm of the fovea to ∼500 μm in the retinal periphery. HRP injections of groups of neighboring cells revealed a regular intercell spacing (∼200-300 μm in the retinal periphery), suggesting that dendritic territories uniformly cover the retina. One to four axons originate from the proximal dendrites as thin (<0.5 μm). smooth processes. The axons increase in diameter (∼1-2 μm) as they course beyond the dendritic field and bifurcate once or twice into secondary branches. These branches give rise to a number of thin, bouton-bearing collaterals that extend radially from the dendritic tree for1-3 mm without much further branching. The result is a sparsely branched and widely spreading axonal tree that concentrically surrounds the smaller, more highly branched dendritic tree. The axonal tree is narrowly stratified over the central 0-20% of the IPL; it is approximately ten times the diameter of the dendritic tree, resulting in a 100 times greater coverage factor. The clear division of an amacrine cell's processes into distinct dendritic and axonal components has recently been observed in other, morphologically distinct amacrine cell types of the cat and monkey retina and therefore represents a property common to a number of functionally distinct cell types. It is hypothesized that the axon-bearing amacrine cells, like classical neurons, use action potentials to transmit signals over long distances in the IPL and, on the basis of previous immunohistochemical results, contain the inhibitory neurotransmitter GABA.