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Kumiko Anne Percival, Sowmya Venkataramani, Robert G Smith, William Rowland Taylor; Directional tuning of excitatory responses in ON-OFF direction selective ganglion cells are not due to voltage clamp artifacts. Invest. Ophthalmol. Vis. Sci. 2015;56(7 ):4376.
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© ARVO (1962-2015); The Authors (2016-present)
It is widely agreed that the directional tuning of inhibitory conductances in direction selective ganglion cells (DSGCs) arise from the preferential release of GABA from starburst amacrine cells during null direction motion. The mechanisms for the directional bias in the excitatory responses however are currently unknown, with two recent reports suggesting a lack of directionally tuned glutamate release onto DSGCs. We recorded stimulus evoked excitatory and inhibitory responses in ON-OFF DSGCs to determine whether directional tuning of excitatory responses result from artifacts due to poor voltage clamp.
We made in vitro voltage-clamp recordings from seventy ON-OFF DSGCs in the visual streak of rabbit retina. Membrane currents were recorded at nine holding potentials in response a dark bar moving in the cell’s preferred and null directions. Excitatory and inhibitory conductances were measured from current-voltage relations measured at 10ms intervals. We determined whether the strength of the directional signals for peak excitatory conductances (peak preferred excitation/peak null excitation) were positively correlated with the directional signal observed for inhibitory conductances (peak null inhibition/peak preferred inhibition), as would be predicted if the directional excitatory signal were an artifact of asymmetric voltage-clamp errors produced by the asymmetry in the total membrane conductance, due to large directional asymmetry in the inhibitory conductance.
Our sample of 70 cells showed highly variable preferred/null ratios for excitatory signals with averages of 1.45 ± 0.37 and 1.40 ± 0.31 for OFF and ON responses respectively. When cells were sorted into quartiles, according to the magnitude of their excitatory preferred/null ratio, the average ratio increased linearly from 1.06 in the first to 1.9 in the 4th quartile, while the corresponding inhibitory null/preferred ratios for the four groups did not show the predicted positive correlation.
Our results show that directional excitation is not correlated with inhibition, indicating that directional excitation in ON-OFF DSGCs cannot be explained simply by voltage clamp artifacts.
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