Multiple Invagination Patterns and Synaptic Efficacy in Primate and Mouse Rod Synaptic Terminals

Optical retina images are scaled based on eye size, which results in a linear scale ratio of 10:1 for human versus mouse and 7:1 for macaque monkey versus mouse. We examined how this scale difference correlates with the structural configuration of synaptic wiring in the rod spherule (RS) between macaque and mouse retinas compared with human data.

Rod bipolar cell (BC) dendrites and horizontal cell (HC) axonal processes, which invaginate the RS to form synaptic ribbon-associated triads, were examined by serial section transmission electron microscopy.

The number of rod BC invaginating dendrites ranged 1∼4 in the macaque RS but only 1∼2 in the mouse. Approximately 40% of those dendrites bifurcated into two central elements in the macaque, but 2% of those dendrites did in the mouse. Both factors gave rise to 10 invagination patterns of BC and HC neurites in the macaque RS but only two in the mouse. Five morphological parameters: the lengths of arciform densities and ribbons, the area of the BC-RS contact, and the surface areas of BC and HC invaginating neurites, were all independent of the invagination patterns in the macaque RS. However, those parameters were significantly greater in the macaque than in the mouse by ratios of 1.5∼1.8.

The primate RS provides a more expansive BC-RS interface associated with the longer arciform density and more branched invaginating neurites of BCs and HCs than the mouse RS. The resulting greater synaptic contact area may contribute to more efficient signal transfer.