Bipolar input to melanopsin containing ganglion cells in primate retina

Abstract

Two morphological types of melanopsin-expressing ganglion cells have been described in primate retina. Both types show intrinsic light responses as well as rod- and cone-driven ON-type responses. Outer stratifying cells have their dendrites close to the inner nuclear layer (OFF sublamina); inner stratifying cells have their dendrites close to the ganglion cell layer (ON sublamina). Both inner and outer stratifying cells receive synaptic input via ribbon synapses, but the bipolar cell types providing this input have not been identified. Here, we addressed the question whether the diffuse (ON) cone bipolar type DB6 and/or rod bipolar cells contact melanopsin-expressing ganglion cells. Melanopsin containing ganglion cells in marmoset (Callithrix jacchus) and macaque (Macaca fascicularis) retinas were identified immunohistochemically; DB6 cells were labeled with antibodies against the carbohydrate epitope CD15, rod bipolar cells were labeled with antibodies against protein kinase C, and putative synapses between the two cells types were identified with antibodies against piccolo. For one inner cell, nearly all of the DB6 axon terminals that overlap with its dendrites in the two-dimensional space show areas of close contact. In vertical sections, the large majority of the areas of close contact also contain a synaptic punctum, suggesting that DB6 cells contact inner melanopsin cells. The output from DB6 cells accounts for about 30% of synapses onto inner melanopsin cells. Synaptic contacts between rod bipolar axons and inner dendrites were not observed. In the OFF sublamina, about 10% of the DB6 axons are closely associated with dendrites of outer cells, and in about a third of these areas, axonal en passant synapses are detected. This result suggests that DB6 cells may also provide input to outer melanopsin cells.