Center-surround organization of Xenopus horizontal cells and its modification by gamma-aminobutyric acid and strontium

Abstract

The properties of axon-bearing horizontal cells were studied by intracellular recording in the light-adapted Xenopus retina. In this adaptational state, the only receptor input was provided by red-sensitive cones. Measurements of response amplitude as a function of stimulus diameter indicated that different units were divisible into two compartments on the basis of their receptive field dimensions: one with a mean length constant, lambda, of 170 microns, the other with lambda = 450 microns. Lucifer Yellow dye injection revealed that units having small receptive fields invariably were cell bodies, whereas units having large receptive fields always were axons. For both horizontal cell bodies and axons, the waveform in response to large spots or annuli consisted of a hyperpolarizing on-transient, followed by a depolarizing rollback to a sustained plateau during light on, and a rapidly depolarizing off-transient that overshot the dark potential level. In contrast, in responses to small spots, the depolarizing rollback was much reduced or absent. However, for small field compartments only, when concentric annular stimuli were flashed around steadily illuminated, small, centered spots, the horizontal cell waveform consisted primarily of a depolarizing potential during light on. This depolarizing component was reduced selectively when the preparation was superfused with Ringer containing 5 mM gamma-aminobutyric acid (GABA). Following a brief exposure to 5-10 mM Sr2+, enhanced oscillatory potentials appeared in the horizontal cell light response during the depolarizing rollback and at light off. The modifications of the depolarizing rollback evoked by Sr2+ were antagonized by GABA. The strontium-induced alterations of the light response were not altered by 6 microM tetrodotoxin (TTX). The results are interpreted in terms of a feedback synaptic action exerted by horizontal cells upon cones, which is expressed as the depolarizing rollback component of the horizontal cell light-evoked waveform. The spatial properties of this component suggest that horizontal cell axons but not horizontal cell perikarya are capable of evoking a feedback signal in the cone. The actions of strontium indicate that calcium currents may play a role in shaping the feedback response. The ability of GABA to antagonize the Sr2+ effect upon the depolarizing rollback indicates that GABA may play a role in feedback.