The superficial plexiform layer: A third retinal association area

Electron microscopy enables the identification of a new association area in the mammalian retina. It is a region whose processes and synaptic junctions form a diffuse and intermittent layer bridging the boundary between the optic nerve fibre layer and ganglion cell layer. It involves displaced amacrine cells, retinal ganglion cells and probably interplexiform cell processes. Because it is close to the vitreal surface of the retina and has several properties of a plexiform layer, it has been named the superficial plexiform layer. It is much more sparse than the outer or inner plexiform layers in the rabbit, but contains a significant and substantial density of 6,100 synapses/mm 2 near the visual streak. Morphological criteria distinguish two classes of synapses in the new association area. One has features of Colonnier's symmetric type and is formed by amacrine‐like processes or their terminals, onto other amacrine‐like processes or the cell bodies, dendrites and axon hillocks of some large ganglion cells. It makes up 79% of the population at a density of 4,800 synapses/mm 2 in the examined sample. The second class arises from large processes of the fibre layer, which resemble axons rather than amacrine cell branches, has Colonnier's asymmetric form, and synapses onto a variety of other neuronal processes and cells. At a local density of 1,300/mm 2 this type forms 21% of the population. A series of experiments including Wallerian degeneration, retrograde degeneration, electron microscopy and horseradish peroxidase (HRP) transport was employed to determine the nature of the large synapse‐forming processes of the fibre layer that were the most amenable to investigation. It is concluded that the processes project into the optic nerve because they can be filled with HRP by retrograde transport from the end of the transected optic nerve. Although this result is based on limited evidence, it is complemented by the observation that the majority of the fibres undergo retrograde degeneration within 25 days of optic nerve section. It is concluded that the processes are either centrifugal fibres or the axons of retinal ganglion cells. The persistence of a relatively normal density of synapse‐forming large fibres for seven days after optic nerve section, without Wallerian degeneration, argues that they are not the terminals of centrifugal axons. This conclusion is complemented by a separate class of profiles that did degenerate in this short period and are concluded to represent the centrifugal fibres. The large synapsing processes of the fibre layer are concluded to be the axons of some large ganglion cells. Their connections indicate the presence of feedback loops onto other large retinal ganglion cells both directly and indirectly through amacrine pathways. The superficial plexiform layer thus contains a rich variety of organised synaptic connections whose functional significance remains to be established.