Circuitry analysis of the outer plexiform layer in the rabbit retina: I. Extension of analysis of circuits interpreted to be associated with directional sensitivity and edge detection

Abstract

The earlier analysis of the circuitry of the outer plexiform layer in the rabbit retina [ Sjostrand, 1969 , Sjostrand, 1974 , Sjostrand, 1976 , Sjostrand, 1976 ] has been extended with respect to the circuitry that was proposed to be associated with directional sensitivity and edge detection. This circuitry involved one bipolar cell, here referred to as bipolar cell 1, which was connected to horizontal cells according to a characteristic pattern that appeared suitable for a detector for directional sensitivity and for an edge. The same characteristics of the pattern of connections were found repeated at the contacts of this bipolar cell at a second photoreceptor cell of the β type (α and β type cells are usually identified with rod and cone cells, respectively). The similarities involve the presence of collateral branches of bipolar cell 1 that contact horizontal cell processes outside the subsynaptic neuropil, connections in the subsynaptic neuropil which involve both bipolar cell and horizontal cell processes, contacts with efferent bipolar cells in the subsynaptic neuropil, contact relations with horizontal cell processes at synaptic ribbon complexes, and contacts with the photoreceptor cells. Collateral branches are a unique feature of bipolar cell 1 among all bipolar cells contacting these two photoreceptor cells. As in the previous papers, the interpretation of the functional significance of the circuitry was based on distinguishing between two types of horizontal cell-bipolar cell connections. Horizontal cells were thus classified as contributing either processes that showed a structural polarity or processes that were lacking any structural polarity. In five synaptic ribbon complexes analyzed at photoreceptor cell β2, one of the two horizontal cell endings of each complex was contributed by a horizontal cell process with structural polarity, while the other was contributed by a process lacking structural polarity. This is in agreement with the most common arrangement observed in earlier analysis ( Sjostrand, 1974 ). It could also be confirmed that the bipolar cell process to a synaptic ribbon complex was a side branch of the end branch which itself was received in a separate invagination of the plasma membrane of the terminal. There were five horizontal cell processes with structural polarity that contacted or were contacted by bipolar cell 1 in synaptic ribbon complexes, in the subsynaptic neuropil, and outside the subsynaptic neuropil. All these processes showed the same polarity which agreed with the polarity of corresponding horizontal cell processes' contacts at photoreceptor cell β1. The systematic repetition of similar contact relations of bipolar cell 1 at both photoreceptor cells and the fact that the similarities involved a characteristic, nonrandom but rather specific type of contact pattern support the concept that the neurons are connected according to well-defined patterns designed for a particular type of information processing. As a consequence, circuit analysis of this kind together with electrophysiological analysis should form a concrete basis for revealing how information is processed in nervous centers. The subsynaptic neuropil showed an even more complex circuitry at this photoreceptor cell than at photoreceptor cell β1, supporting the earlier conclusion that the subsynaptic neuropil is the site of a major part of retinal circuitry ( Sjostrand, 1974 , Sjostrand, 1976 , Sjostrand, 1976 ). A pairing of contacts of endings of neurons was observed to be a general rule for contacts not only in the synpatic ribbon complexes but also in the subsynaptic neuropil and outside the subsynaptic neuropil. For horizontal cells this pairing involved one horizontal cell process with polarity paired with one lacking polarity like the most common combination at synaptic ribbon complexes. From a functional point of view the horizontal cell processes lacking structural polarity were interpreted to be involved in neural adaptation of the retina while the horizontal cell processes with structural polarity were interpreted to act in an inhibitory way on bipolar cells on the basis of local, one-sided conditions of illumination of the retina. This functional interpretation was the basis for proposing that the observed circuitry could be associated with directional sensitivity and edge detection. These proposals appear to have gained additional support from the fact that the same type of connections were found at both photoreceptor cell β1 and β2.