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Shai Sabbah, Min Tae Kim, Gabrielle Manoff, Ananya Bhatia-Lin, Carin Papendorp, Kevin Briggman, David M Berson; Connectomics of irradiance-encoding ON bipolar-cell inputs to ipRGCs. Invest. Ophthalmol. Vis. Sci. 201657(12):.
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© ARVO (1962-2015); The Authors (2016-present)
Intrinsically photosensitive retinal ganglion cells (ipRGCs) are unique among ganglion cells in their capacity to encode environmental light intensity (irradiance). They do so even at light intensities sufficient to activate rods and cones, but too low to activate melanopsin. Which bipolar cell (BC) types transmit irradiance data from photoreceptors to ipRGCs and how do they do so?
We analyzed BC-to-ipRGC circuits in a serial blockface electron-microscopic dataset (k0725) from adult mouse retina (200x250x70 um2) stained to reveal organelles. We reconstructed several examples of most types of ipRGCs, recognizable from their branching patterns and levels of dendritic stratification. Ribbon contacts onto their dendrites were identified, the presynaptic BCs reconstructed, and other synaptic associations of these BCs mapped.
We confirmed earlier reports that ipRGCs receive ectopic en passant ribbon synapses from the shafts of ON cone BC axons near the outer margin of the inner plexiform layer (IPL). These were monads, usually with several ribbons each. All ipRGC types with dendrites in this layer (M1, M3, M6) were targets of such synapses, as were several amacrine-cell types. Overall, neurons postsynaptic to ectopic synapses restricted their dendrites to the melanopsin immunoreactive bands (accessory ON and inner half of conventional ON sublayers). Thus, these ectopic synapses appear closely linked to ipRGC networks. Type 6 ON cone BCs (n=52) were the main source of ectopic ribbons, but Type 8 and 9 BCs also contributed (n=35). Most Type 6, 8 and 9 BCs possessed ectopic ribbons, whereas Types 5 and 7 and rod BCs almost never did. Ectopic ribbons (n=233) had a spatial density of ~6000/mm2. BCs with ectopic ribbons made conventional dyad ribbon contacts in the ON sublayer of the IPL. Postsynaptic targets of these cells (n=18) included at least four ipRGC types (M2, M3, M5, M6); M3 and M6 cells received both ectopic and conventional ribbon inputs. However, neurons other than ipRGCs must receive input from these BCs because some stratified in the mid-IPL, which ipRGCs never do.
ipRGCs get input from three cone BC types (6, 8 and 9) through mixed conventional and ectopic ribbon synapses; the ectopic pathway may be unique to ipRGCs. Thus, both specific BCs and specialized synapses underlie the irradiance-encoding synaptic light responses of ipRGCs.
This is an abstract that was submitted for the 2016 ARVO Annual Meeting, held in Seattle, Wash., May 1-5, 2016.
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