Abstract
We confirmed the classification of 15 morphological types of mouse bipolar cells by serial section transmission electron microscopy and characterized each type by identifying chemical synapses and gap junctions at axon terminals. Although whether the previous type 5 cells consist of two or three types was uncertain, they are here clustered into three types based on the vertical distribution of axonal ribbons. Next, while two groups of rod bipolar (RB) cells, RB1, and RB2, were previously proposed, we clarify that a half of RB1 cells have the intermediate characteristics, suggesting that these two groups comprise a single RB type. After validation of bipolar cell types, we examined their relationship with amacrine cells then particularly with AII amacrine cells. We found a strong correlation between the number of amacrine cell synaptic contacts and the number of bipolar cell axonal ribbons. Formation of bipolar cell output at each ribbon synapse may be effectively regulated by a few nearby inhibitory inputs of amacrine cells which are chosen from among many amacrine cell types. We also found that almost all types of ON cone bipolar cells frequently have a minor group of midway ribbons along the axon passing through the OFF sublamina as well as a major group of terminal ribbons in the ON sublamina. AII amacrine cells are connected to five of six OFF bipolar cell types via conventional chemical synapses and seven of eight ON (cone) bipolar cell types via electrical synapses (gap junctions). However, the number of synapses is dependent on bipolar cell types. Type 2 cells have 69% of the total number of OFF bipolar chemical synaptic contacts with AII amacrine cells and type 6 cells have 46% of the total area of ON bipolar gap junctions with AII amacrine cells. Both type 2 and 6 cells gain the greatest access to AII amacrine cell signals also share those signals with other types of bipolar cells via networked gap junctions. These findings imply that the most sensitive scotopic signal may be conveyed to the center by ganglion cells that have the most numerous synapses with type 2 and 6 cells.
Highlights
Transcriptomics experiments defined 15 types of bipolar cells in the mouse retina (Shekhar et al, 2016)
T5b cells have gap junctions with T5a cells in the mouse (Figures 12H, 15B). These findings suggest that T5b cells may communicate with AII amacrine cells through T5a cells (AII → 5a → 5b) in the mouse, as suggested for cat b3 and b4 cells (AII → b4 → b3; Cohen and Sterling, 1990)
Comparison with Helmstaedter et al.’s Data The top three ON bipolar cell types, T6 (46%), T7 (29%), and T5a (20%), shared 95% of the total area of gap junctions of all ON bipolar cells with AII amacrine cells according to our data
Summary
Transcriptomics experiments defined 15 types of bipolar cells in the mouse retina (Shekhar et al, 2016) These molecular genetic data are consistent with the reported morphological data. Ghosh et al (2004) first described cell types (T1–T9 and RB), Mataruga et al (2007) further divided the type 3 cells into T3a and T3b, Wässle et al (2009) presented a systematic survey of cone contacts, mosaics, and territories of the identified types of bipolar cells. These analyses combined several methods, including dye injection, immunostaining, and experimental manipulation of transgenic mice. Della Santina et al (2016) revealed a peculiar type of bipolar cell which has no dendrites using dye injection and further described the distribution of axonal ribbons by SBSEM
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