Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation

Polyaxonal (PA) amacrine cells are a new class of amacrine cell bearing one to six branching, axon‐like processes that emerge from the cell body or dendritic trees within 50 μm of the cell body. These slender processes of uniform caliber branch at right angles and in many respects closely resemble the axons of Golgi type II cells found elsewhere in the brain. Of the four types of polyaxonal amacrine cell that we have recognized in rabbit retina, two have been described previously in brief communications. One of these, the PA1 amacrine cell with its interstitially displaced cell body, located in the inner plexiform layer (IPL), has been analyzed extensively in two preceding reports. This paper concerns PA2, PA3, and PA4 amacrine cells. Type 2 polyaxonal (PA2) amacrine cells, identified in Golgi preparations of whole‐mounted rabbit retinas, have smaller cell bodies (9–14 μm) than the other three types and these are always displaced to the ganglion cell layer (GCL) or the inner border of the inner plexiform layer (IPL). The dendritic fields of PA2 cells are also smaller than those of other PA amacrine cells, and most of their sparse dendritic branching is narrowly stratified at the border of strata (S) 4 and 5. Some members of this more heterogeneous amacrine cell “type” are bistratified, however, and more highly branched with terminal branches rising to end in S1. PA2 amacrine cells bear a scattering of small dendritic spines and may also exhibit complex dendritic appendages arising at the ends of terminal branches in proximal regions of the dendritic tree. PA2 cells emit one to three axons from the proximal dendritic tree, and about half of the cells bear a single axon. Type 3 polyaxonal (PA3) amacrine cells resemble PA1 cells in the large size of their cells bodies (11–16 μm) and dendritic fields, but differ from the latter in placement of cell bodies, which is in the GCL, and dendritic and axonal stratification, which is multistratified, ranging from S4 to S1, with a concentration in S3 or S4 and a variable contribution to S1. PA3 cells differ from PA1 cells in several other respects, including dendritic branching which occurs at higher frequency and is biased toward temporal retina, and in characteristic bristling dendritic spines, clustered in the intermediate regions of the dendritic tree, that are longer, more variable in appearance and more tightly clustered than the small, uniform spines of PA1 cells that are clustered on proximal dendrities. Type 4 polyaxonal (PA4) amacrine cells, characterized in Golgi and immunocytochemical preparations, have large cell bodies located in the amacrine cell sublayer of the inner nuclear layer and dendritic branching in S1; the straight dendritic branches are highly varicose bearing a sparse complement of spines. A single axon may be usual in PA4 cells. The axon is apparently confined to S1 for most of its course, but may contribute a few branches to S3 and S5 of the IPL. The axon initial segment of PA4 cells, like that of PA1 cells, exhibits one or more swellings along its course. Electron microscopic study of a PA2 amacrine cell reveals largely if not exclusively postsynaptic dendrites and an axon initial segment with ultrastructural features differentiating it from the dendrites. Certain similarities are noted in a comparison of the axons of polyaxonal amacrine cells and both developing and regenerating axons of the central nervous system. Hence polyaxonal amacrine cell axons may be viewed in terms of a flexible genetic repertoire governing the form and function of neuritic outgrowth. The likely neurotransmitters of polyaxonal amacrine cells are considered and the correspondances suggested are: PA1 cells–epinephrine; PA2 cells–somatostatin and/or substance P; PA3 cells–unknown; PA4 cells–dopamine. It is proposed that the family of polyaxonal amacrine cells plays a “fast” neuromodulatory role in light adaptation, mediating information at mesopic levels about changing, uniform background illumination.