Reexamination of photoreceptor-bipolar connectivity patterns in carp retina: HRP-EM and Golgi-EM studies

Abstract

On- and off-center bipolar cells were identified in the carp retina by means of intracellular recording, intracellular injection of HRP, and Golgi silver-chromate impregnation. Light and electron microscopy revealed that these functionally different bipolar cells make synaptic contacts with both rods and cones, and that both on- and off-center cells can be further divided into two subtypes (I and II) according to the relationship between the position of their dendritic processes and the synaptic ribbons in the photoreceptor terminal. The type I on-center bipolar cell is characterized by a large cell body, a thick primary dendrite, and a big swelling of the axon terminal in the innermost part of the inner plexiform layer (IPL). Dendritic processes of this cell type make predominantly ribbon contacts with rods and nonribbon contacts with cones. The type II on-center cell, having a large dendritic tree in the outer plexiform layer and a large ramification of the axon terminal extending over the inner part of the IPL makes mostly nonribbon contacts with rods and cones. Many of these type II cell processes, however, terminate very close to cone synaptic ribbons. The type I off-center cell shows two varieties in the axon terminal structure; a large terminal swelling or a large flat ramification of the terminal in the outermost part of the IPL. These cells make predominantly ribbon contacts with rods and cones. Usually, but not always, the process of a type I off-center cell runs parallel to the synaptic ridge apex of cones. The type II off-center cell, showing a large ramification of the axon terminal extending over the outer half of the IPL, makes mainly nonribbon contacts with rods and cones. The results from the HRP-EM study generally agree with those from the Golgi-EM study. A few discrepancies between the results obtained with these two techniques are noted and their implication is discussed.