Two components of extracellularly-recorded photoreceptor potentials in the cephalopod retina: differential effects of Na+, K+ and Ca2+.

Abstract

The ERG of the isolated, superfused half-eye of the cephalopod Sepiola atlantica, evoked by a brief (10 micro second) light flash, has been studied by recording intraretinal potentials with glass microelectrodes. The intensity-response characteristics of the potentials recorded at an electrode fixed at the surface (Vs) can be fitted by a simple equation derived from an equivalent circuit model based on a sodium conductance increase mechanism. Raising the external potassium level reduces the maximal response (deltaVm), but does not alter the half-saturation intensity value (I0). Reducing external sodium does not affect deltaVm, but increase I0. Reducing external calcium also does not affect delta Vm, but decrease I0. These effects are adequately described by the model if it is also assumed (a) that changing the external sodium does not significantly alter the transmembrane sodium gradient, and (b) that sodium and calcium ions compete for the sensitivity control mechanism. Differential-depth recording between the fixed electrode at the surface and another electrode that could be moved into the retina revealed that the two component appearance of the transretinal ERG arose from the superposition of two vitreal-negative waveforms. An initial "fast" component was mainly recorded in the photoreceptive distal segments while a "slow" component was prominent in the more proximal regions of the retina. Perfusion with high K+ salines resulted in a decrease in the amplitudes of both fast and slow components of the response whereas reducing external Na+ reduced the amplitude of the fast component at all light intensities but reduced the amplitude of the slow component only at low intensities. The amplitudes of both the fast and slow components increased on reducing external calcium, but the rate of rise and fall of the fast component was independent of external calcium. The rate of rise of the slow component was also independent of the external Ca2+ level but a minimum in the recovery time (tF) was shifted to a lower intensity value at lower calcium concentrations. The shift of the minimum was to a higher intensity value with lowered sodium perfusing solutions. On the basis of the differential sensitivity of the two components to ion changes, as well as stimulus intensity and intraretinal distribution of the components, it is suggested that they reflect two distinct processes in the light-evoked potential of the photoreceptor cells.