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Shai Sabbah, Carin M Papendorp, Elizabeth Koplas, Marjo Beltoja, Cameron Etebari, Ali N Gunesch, Luis Carrete, Min Tae Kim, Gabrielle Manoff, Ananya Bhatia-Lin, Henry Dowling, Kevin L Briggman, David M Berson; All bipolar cells encode irradiance in their output. Invest. Ophthalmol. Vis. Sci. 2017;58(8):2973.
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© ARVO (1962-2015); The Authors (2016-present)
Intrinsically photosensitive retinal ganglion cells (ipRGCs) are the only retinal output cells that encode light intensity (irradiance). This capacity supports circadian, pupillary and neuroendocrine modulation by daylight. We asked which types of bipolar cells (BCs) transmit irradiance signals from rods and cones to ipRGC dendrites in the inner plexiform layer (IPL), and how they do so.
By serial electron microscopy (k0725), we identified 1-3 examples of each type of ipRGC based on dendritic form, then reconstructed and classified BCs making ribbon contacts with them. We assessed glutamate release from BCs in response to 30s full-field light steps of various intensities by 2-photon imaging of iGluSnFR, expressed either selectively in ipRGCs or non-selectively in many RGCs and amacrine cells.
In the inner IPL (classic ON sublayer), M2-M6 ipRGCs received input mostly from Type 6 ON BCs, with minor Type 7–9 input. Such contacts were mostly standard dyads, with occasional monads. The weighting of inputs from these BC types was predictable from stratification patterns of BC axon terminals and ipRGC dendrites, assuming no cell-type specificity. By contrast, ipRGC dendrites in the outer IPL (‘accessory ON sublayer’; M1 and M6 cells) always avoided OFF BCs and received ribbon contacts only from ectopic ON-BC axons, in the form of monads. The ON-BC types providing such input mirrored those for inner ipRGC dendrites (Type 6 >> Types 7-9). Imaging confirmed sustained, irradiance-encoding glutamate release onto ipRGC dendrites, but surprisingly this was not unique to them. The glutamate signal was sustained and irradiance-encoding throughout the IPL, even in the outer part of the classic ON sublayer where transient RGCs stratify, and in the classic OFF sublayer (in the form of tonic reductions in glutamate release). Nonetheless, irradiance signals did vary modestly with IPL depth, suggesting differences among BC types.
Our data show that Type 6 BCs dominate the synaptic input to ipRGCs, regardless of ipRGC subtype, or synapse location or form. This input clearly encodes irradiance, but this capacity is not unique to Type 6 BCs; indeed, it may be shared by all BCs. This implies that the key locus for temporal filtering of sustained irradiance-coding signals in non-ipRGCs is postsynaptic to the BC axon terminal, perhaps through glutamate receptor kinetics, intrinsic membrane properties and/or feed-forward inhibition.
This is an abstract that was submitted for the 2017 ARVO Annual Meeting, held in Baltimore, MD, May 7-11, 2017.
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