A chromatic horizontal cell in the Xenopus retina: intracellular staining and synaptic pharmacology

Abstract

1. We identified a chromatic-type horizontal cell (C-cell) in the Xenopus retina by intracellular dye injection with Lucifer yellow or horseradish peroxidase (HRP). C-cells hyperpolarized in response to blue light and depolarized in response to red light. 2. In either photopic or mesopic states, moderate-intensity blue and red stimuli evoked responses that were inverted with respect to each other but of similar waveform and latency. In the presence of a bright green adapting field, the maximal voltage (Vmax) of the hyperpolarizing and depolarizing response component approached 30 mV; the kinetics of both waveforms were fast, and the hyperpolarizing response was followed by a small depolarizing overshoot at light OFF. Thus the blue-sensitive photoreceptor is capable of initiating large visual signals under photopic conditions when transmission from green-sensitive rods is suppressed. Under mesopic conditions (no adapting field) the kinetics of both waveforms were slower. The Vmax of the hyperpolarizing response reached 30-40 mV, whereas the cone-mediated depolarization saturated at 15 mV. 3. Both response components of the C-cell showed large receptive fields with no center-surround antagonism. 4. The C-cell perikaryon was located in the distal inner nuclear layer. It emitted four to seven long, tapering processes that ran horizontally for 90-100 microns. Two kinds of terminal dendrites, short and long, extended from the tapering processes toward the layer of photoreceptor bases. 5. Glycine (5-10 mM) completely eliminated the depolarizing response of the C-cell, whereas the hyperpolarizing component was unaffected. In contrast, gamma-aminobutyric acid (GABA; 5-10 mM) had no obvious effect on either component. 6. The C-cell light response was modified in two stages by cis-2,3-piperidine dicarboxylic acid (cis-PDA; 0.5-5 mM): first the depolarizing response disappeared; then the membrane potential hyperpolarized concomitant with a large reduction or elimination of the hyperpolarizing light response. In contrast, DL-2-amino-4-phosphonobutyric acid (APB) had no obvious effect on either response component or the membrane potential of the cell. 7. Our pharmacological findings are consistent with the view that the hyperpolarizing response in the C-cell is mediated by direct synaptic input from a blue-sensitive photoreceptor. The depolarizing response mediated by the red-sensitive cone could be explained by a direct synapse from the red cone or an indirect pathway involving luminosity (L-type) horizontal cells.