Feedback from luminosity horizontal cells mediates depolarizing responses of chromaticity horizontal cells in the Xenopus retina

Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3556-60. doi: 10.1073/pnas.92.8.3556.

Abstract

It has been proposed that the depolarizing responses of chromaticity horizontal cells (C-HCs) to red light depend on a feedback signal from luminosity horizontal cells (L-HCs) to short-wavelength-sensitive cones in the retinas of lower vertebrates. In this regard we studied the C-HCs of the Xenopus retina. C-HCs and L-HCs were identified by physiological criteria and then injected with neurobiotin. The retina then was incubated with peanut agglutinin, which stains red-but not blue-sensitive cones. Electron microscopic examination revealed that L-HCs contact all cone classes, whereas C-HCs contact only blue-sensitive cones. Simultaneous recordings from C-HC/L-HC pairs established that when the L-HC was saturated by a steady bright red light, C-HCs alone responded to a superimposed blue stimulus. In response to red test flashes, the C-HC response was delayed by approximately 30 msec with respect to the L-HC response. Isolated HCs of both subtypes were examined by whole-cell patch clamp. Both responded to kainate with sustained inward currents and to quisqualate or alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) with desensitizing currents from a negative holding potential; i.e., both have AMPA-type glutamate receptors. gamma-Aminobutyric acid or glycine opened a chloride channel in the L-HC, whereas the C-HC was unresponsive to either inhibitory amino acid. Since glycine has been shown to abolish selectively the depolarizing response of the C-HC, this finding and other pharmacological data strongly implicate the L-HC in the underlying circuit. Moreover, because the C-HC does not respond to gamma-aminobutyric acid, the neurotransmitter of the L-HC, by elimination, a feedback synapse from L-HC to blue cone is the most plausible mechanism for the creation of depolarizing responses in C-HCs.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Cell Communication / physiology*
  • Cobalt / pharmacology
  • Evoked Potentials, Visual / physiology*
  • Evoked Potentials, Visual / radiation effects
  • Feedback
  • Glycine / pharmacology
  • Light
  • Male
  • Neurons / physiology*
  • Neurons / radiation effects
  • Patch-Clamp Techniques
  • Receptors, Glutamate / metabolism
  • Retina / cytology*
  • Retina / physiology*
  • Retina / radiation effects
  • Retinal Cone Photoreceptor Cells / cytology
  • Xenopus
  • gamma-Aminobutyric Acid / pharmacology

Substances

  • Receptors, Glutamate
  • Cobalt
  • gamma-Aminobutyric Acid
  • Glycine