Cone synapses in macaque fovea: II. Dendrites of OFF midget bipolar cells exhibit Inner Densities similar to their Outer synaptic Densities in basal contacts with cone terminals

Abstract

As described in the companion paper, the synaptic terminal of a cone photoreceptor in macaque monkey makes an average of 35 or 46 basal contacts with the tips of the dendrites of its OFF midget bipolar cell. Each basal contact has one or more symmetrically thickened dense regions. These "Outer Densities," averaging 48 or 67 in number, harbor clusters of ionotropic glutamate receptors and are ~0.8 μm (and ~1-ms diffusion time) from active zones associated with synaptic ribbons. Here, we show similarly appearing "Inner Densities," averaging 53 or 74 in number, located more proximally on the dendrites of these OFF midget bipolar cells, ~0.4 μm inward from the tips of the dendrites and out of contact with the basal surface of the cone terminal. Compared to desmosome-like junctions, Inner Densities are closer to the terminal and are less dense and less thick. Each Inner Density is shared with another cell, the partners including diffuse bipolar cells, ON midget bipolar cells, and horizontal cells. Given the diversity of the partners, the OFF midget bipolar cells are unlikely to be in a synaptic relationship with the partners. Instead, Inner Densities are near enough to the active zones associated with synaptic ribbons to receive pulses of glutamate at concentrations effective for glutamate receptors. The role of Inner Densities is not known, but they might represent additional clusters of glutamate receptors.

Cone synapses in macaque fovea: I. Two types of non-S cones are distinguished by numbers of contacts with OFF midget bipolar cells

“…There, the hybrid synaptic contour detours from the terminal to the regions of apposition between the central elements and the lateral elements, hence the word "hybrid." For further details, see Herr et al (2003Herr et al ( , 2011. From digitized tracings of sequential hybrid synaptic contours, we reconstruct the "hybrid synaptic surface" of the presynaptic face of a cone terminal in three dimensions by use of the Montage program (Smith, 1987).…”

“…These contacts, also called "invaginating" (Dowling & Boycott, 1966;, have asymmetrically dense regions that are thicker on the presynaptic side (Raviola & Gilula, 1975;Vardi et al, 1998;Ahmad et al, 2003). The OFF midget bipolar cell dendrites occupy the triad-associated position (Kolb, 1970;Boycott & Hopkins, 1991;Hopkins & Boycott, 1992), and their contacts, called "basal," harbor one or more symmetrically dense regions (Vardi et al, 1998;Ahmad et al, 2003), here called "Outer Densities" in contrast to "Inner Densities" located more proximally on OFF midget bipolar cell dendrites (see below; Herr et al, 2011).…”

Connectomics of synaptic microcircuits: lessons from the outer retina

“…; Herr et al . ; Szmajda & DeVries, ). In future, the application of such a combined approach to photoreceptor synapses could assess the prevalence and role of these synaptic motifs, exploring modes of convergence and divergence (Wässle, ), non‐linear signalling properties (Field & Rieke, ; Berntson et al .…”