Transmission from photoreceptors to ganglion cells in turtle retina

Abstract

Synaptic transfer between photoreceptors and impulse-generating cells was studied in isolated eyecups from turtles [Pseudemys scripta elegans and Chelydra serpentina]. Single red-sensitive cones or rods were stimulated by current passed through an intracellular electrode, and impulses generated by the resulting synaptic action were recorded with an external microelectrode. This technique permitted study of retinal transmission without the operation of the visual transduction mechanism. Antidromic stimulation of the optic nerve indicated that most of the impulse-generating cells were ganglion cells. Individual ganglion cells responded transiently to changes in the membrane potential of a receptor and could be classified into 3 groups on the basis of the direction of the effective change in potential. Off center ganglion cells responded selectively to depolarizations of a receptor, while on center ganglion cells responded selectively to hyperpolarizations. On-off ganglion cells responded to both depolarizations and hyperpolarizations of a receptor. Ganglion cells gave the same pattern of response to electrical hyperpolarization of a receptor and to light in the center of their receptive fields. Subthreshold depolarizing currents passed in a receptor antagonized the ganglion cell''s response to light, and subthreshold hyperpolarizing currents reinforced the response. The hyperpolarization generated by visual transduction may be responsible for regulating the release of transmitter at the 1st retinal synapse. When a receptor was stimulated with weak current pulses of fixed intensity the number and latency of the ganglion cell impulses fluctuated randomly in successive trials. The relation between the fraction of trials yielding a response and the stimulus intensity was broad. The link between retinal input and output is apparently noisy. In the most sensitive pairs of cells, a response of 1 or more impulses could be obtained in half the trials with a current of about 2 .times. 10-11 A, which changed the potential of the receptor by 1-2 mV. A current of similar magnitude would be developed by about 130 photoisomerizations in a red-sensitive cone or 50 photoisomerizations in a rod. Dim background light producing a steady hyperpolarization of a few millivolts in the rods raised the threshold for electrically-evoked transmission from a rod to a ganglion cell. In experiments on red-sensitive cones, background light raised the threshold in the off pathway, in which depolarization was the effective stimulus, and lowered the threshold in the on pathway, in which hyperpolarization was the effective stimulus. These changes in sensitivity were not accompanied by obvious changes in the input resistance of the stimulated receptor. Regulation of retinal sensitivity in background light thus involves changes in synaptic transfer and in the sensitivity of the visual transduction mechanism.