A search for the circuitry of directional selectivity and neural adaptation through three-dimensional analysis of the outer plexiform layer of the rabbit retina

Abstract

The circuitry of a part of the outer plexiform layer in the rabbit retina was studied by means of three-dimensional analysis based on electron micrographs of serial sections. 1. A methodology was worked out for such analysis involving large volumes of nervous tissue. Such analysis was evaluated as feasible and technically possible to pursue. 2. The analysis involved the complete circuitry of one β-type photoreceptor cell and was extended to involve all contact relations within the serially sectioned volume of retinal tissue of all processes contacting this photoreceptor cell. 3. The β-type photoreceptor cell was contacted by ten bipolar cell processes and nine horizontal cell processes. Several different contact relations were observed: contacts through endings at synaptic ribbon complexes, through invaginated endings not contacting synaptic ribbon complex components, through endings making superficial contacts without being invaginated. 4. A thorough analysis of the topographic relationships at synaptic ribbon complexes showed a consistent pattern of arrangement of horizontal cell and bipolar cell endings. 5. At the base of the photoreceptor cell terminal, the processes contacting the terminal formed a compact aggregation of branching processes. This structure was referred to as the subsynaptic neuropil and was proposed to play a role in the circuitry of the outer plexiform layer as indicated by the presence of special end branches confined to this region. 6. Bipolar cell endings were observed containing large amounts of synaptic vesicles and other cytoplasmic structures and were proposed to furnish presynaptic endings of efferent bipolar cells. These cells would allow a feedback from the inner plexiform layer to the outer plexiform layer. 7. These bipolar cell endings contacted horizontal cell endings lateral to the synaptic ribbon complexes. 8. An interpretation of the functional significance of the synaptic ribbon complexes was discussed. According to this interpretation, these complexes would form parts of the circuitry for neural adaptation of the retina. 9. Tight junctions and gap junctions were observed between the largest horizontal cell processes. 10. One bipolar cell process of the ten analyzed differed from the others by sending off lateral branches contacting several horizontal cells as well as one bipolar cell of the efferent type. 11. This bipolar cell was associated with a circuit that could possibly furnish the basis for directional selectivity of certain retinal units.