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Theresa Puthussery, Sowmya Venkataramani, Jacqueline Gayet, W. Rowland Taylor; Differential Functional Expression Of Voltage-gated Channels In Bipolar Cells Within The Midget And Parasol Pathways Of The Primate Retina. Invest. Ophthalmol. Vis. Sci. 2012;53(14):3158.
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© ARVO (1962-2015); The Authors (2016-present)
Midget and parasol ganglion cells (GCs) account for over 80% of all GCs in the primate retina. The midget GCs relay high acuity form and color vision at relatively low temporal frequencies. In contrast, the parasol GCs are important for motion perception, but provide low spatial acuity, albeit with higher achromatic contrast sensitivity, at higher temporal frequencies. It is unclear to what extent the intrinsic membrane properties of presynaptic bipolar cells (BCs) shape the responses of these GC types.
Retinas from adult rhesus macaques were obtained from the Tissue Distribution Program at the Oregon National Primate Research Center. Whole-cell voltage-clamp and current-clamp recordings were made from BCs in light-adapted retinal slices. Immunohistochemistry was used to determine the sub-cellular localization of voltage-gated sodium, calcium and HCN channel subunits within different BC subtypes.
The diffuse cone BC types DB3 and DB4, which are thought to provide inputs to the OFF and ON parasol GCs respectively, exhibited fast, transient inward currents in response to voltage steps to -30mV from a holding potential of -70mV (DB3, -260±47pA, n=10; DB4, -208±21pA, n=25). These currents were blocked by tetrodotoxin. In both cell types, hyperpolarizing voltage steps activated inward currents that had activation kinetics consistent with expression of the HCN1 subunit. DB4 cells also showed a large, TTX-insensitive, transient inward current when stepped to -40mV from a holding potential of -90mV (-330±51pA, n=4). These currents were sensitive to the T-type calcium channel blocker, mibefradil. Under current-clamp, depolarizing current steps evoked action potentials in both BC types. Immunostaining revealed NaV1.1 in the axons of DB3 and DB4 BCs, whilst HCN1 was localized to the soma, dendrites and axon terminals of these cells. CaV3.1 was present in the somatodendritic compartment of DB4 but not DB3 cells. In contrast, the flat and invaginating midget BCs lacked prominent voltage gated sodium or T-type calcium currents and immunohistochemistry confirmed the absence of NaV1.1, CaV3.1 or HCN1 in these cells.
These data reveal clear differences in voltage-gated currents in BCs of the midget versus parasol pathways and suggest that sodium-dependent spikes in BCs may facilitate excitatory signaling in the parasol pathway of the primate retina.
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