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Sign‐preserving and sign‐inverting synaptic interactions between rod and cone photoreceptors in the dark‐adapted retina

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The Journal of Physiology

Published online on

Abstract

•  Five types of rods and cones in the dark‐adapted salamander retina are electrically coupled with linear and symmetrical junctional conductances Gj of different average values. •  The average Gj values of the five types of rod–cone pairs recorded at day and night times suggest that the the circadian‐dependent changes in rod–cone coupling observed in the fish and rodent retinas are not present in the tiger salamander. •  In addition to rod–cone coupling, there is a sign‐inverting, unidirectional rod→cone current IRC, and the current–voltage (IRC–VCone) relations are linear, with a reversal potential near the chloride reversal potential ECl. •  I RC can be observed in rods and cones separated by at least 260 μm, and its waveform resembles that of the rod‐elicited horizontal cell (HC) response IHC; a glutamate transporter‐associated chloride channel blocker TBOA suppresses IRC without affecting IHC. •  These results suggest that IRC is largely mediated by HCs via a sign‐inverting feedback chemical synapse associated with a chloride channel in cones. Abstract  We show that various types of rods and cones in the dark‐adapted salamander retina are electrically coupled with linear and symmetrical junctional conductances Gj (40–223 pS) and a rank order: RodC–large single cone, rod–large single cone, rod–small single cone, rod–accessory double cone and rod–principal double cone. By systematically comparing the transjunctional current–voltage (Ij–Vj) relations and average Gj values of the five types of rod–cone pairs recorded at day and night times, our results suggest that the differences in Gj values among various types of rod–cone pairs are not caused by circadian differences, and the circadian‐dependent changes in rod–cone coupling observed in the fish and rodent retinas are not present in the tiger salamander. In addition to rod–cone coupling, there is a sign‐inverting, unidirectional rod→cone current IRC, and the IRC–VCone relations are linear, with a reversal potential near the chloride reversal potential ECl. IRC can be observed in rods and cones separated by at least 260 μm, and its waveform resembles that of the rod‐elicited horizontal cell (HC) response IHC. A glutamate transporter‐associated chloride channel blocker TBOA suppresses IRC but not IHC. These results suggest that IRC is largely mediated by HCs via a sign‐inverting feedback chemical synapse associated with a chloride channel. IRC significantly reduced rod→cone coupling in the frequency range below 15 Hz, allowing better separation of rod and cone signals in the dark‐adapted retina.