Neural mechanism of lateral inhibition in the retina

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The feedback mechanism from horizontal cells to cone photoreceptors was investigated by the whole cell patch clamp recording from cones in newt retinal slices. GABA-mediated effect has been removed by 100μM picrotoxin. Illumination of the receptive field surround evoked depolarization in cones and shifted the activation voltage of cone calcium current (I_<Ca>) to negative voltages. This effect appeared similar to what was reported by Verweij et al. (1996) as field effect, but the shift of the current-voltage (I-V) relation of I_<Ca> was not merely the parallel shift along the voltage axis as expected for the field effect, because surround illumination increased Ica even at the voltages more positive than I_<Ca> peak. Focal application of high pH solution to the cone terminal layer increased I_<Ca> in a similar manner as the surround illumination. These observations suggest a possibility that surround illumination lowered the proton concentration in the cone terminal region. In fact, enrichment of the pH buffering capacity of extracellular solution by adding 10mM HEPES or 15mM Tris to the bicarbonate buffer increased I_<Ca>, in which additional I_<Ca> increase by surround illumination was not seen. CNQX hyperpolarized horizontal cells (HCs) and augmented cone I_<Ca>. Kainate depolarized HCs and suppressed cone I_<Ca>. Surround responses of cones were not seen in the presence of either kainite or CNQX. Therefore, it is highly likely that cone I_<Ca> is intimately related to the membrane voltage of HCs. From the present results we propose that an external proton mediates feedback for surround inhibition in the outer retina. The mechanisms regulating proton concentration in relation to HC membrane voltage needs to be elucidated.