S-potentials: the first intracellularly recorded photoresponses in the vertebrate retina

S-potentials were the first light-evoked electrical responses recorded with intracellular microelectrodes from nerve cells in the vertebrate retina (Svaetichin, 1953). As shown in Figure 24.1, S-potentials are negative-going changes in membrane potential that last for as long as the light stimulus is present. The graded character of the S-potential is evident in Figure 24.1A. The brighter the stimulus, the larger the amplitude of the S-potential until a saturation level is reached. In Figure 24.1B, the duration of a light stimulus of fixed intensity is altered to examine the effects of this parameter on the S-potential. For long stimuli, the S-potential changes in duration but the amplitude remains constant (the two leftmost responses in Fig. 24.1B). Further reduction in the stimulus duration causes a decrease in amplitude (Fig. 24.1B). This illustrates the temporal summation of the S-potential, following the psychophysical Bloch's law (Roufs, 1972). Up to a certain stimulus duration, the amplitude is directly related to the quantal content of the stimulus (quantal flux × duration); while for stimuli of longer duration, the amplitude is related to the quantal flux. It is likely that S-potentials were named in honor of their discoverer, Gunnar Svaetichin, although S-potentials have come to mean slow potentials.

Figure 24.1..  

The S-potential of the fish retina. Light stimuli of fixed duration and different intensities (A) and light stimuli of fixed intensity but different durations (B) were used to elicit these potentials. Lower traces in A and B record light-stimulus duration and provide 100-msec tick-marks (from Svaetichin, 1953).

S-potentials evoked puzzlement among neurophysiologists of the late 1950s when they were first described. At that time, neurons were thought only to be depolarized (inside becoming more positive relative to outside) by excitatory synaptic inputs. If the depolarization was of sufficient amplitude, action potentials, or nerve spikes, were generated to transfer signals down the length of the axon. S-potentials, however, had neither light-induced depolarizations nor nerve impulses.

At first, the cell type of origin of S-potentials was not really known other than that they were recorded somewhere in the outer retina. In fact, initially S-potentials were thought to arise from cones, as indicated by the title of the 1953 article by Gunar Svaetichin (“The cone action potential”). However, later intracellular marking techniques, in which dyes were injected from electrode tips into the cytoplasm of the recorded neuron, revealed horizontal cells to be the source of the S-potentials (Kaneko, 1970; Werblin and Dowling, 1969). Since first described in fish retinas, S-potentials have been recorded from retinal horizontal cells in all vertebrate classes, including cold-blooded vertebrates (Byzov and Trifonov, 1968; Fuortes and Simon, 1974; Itzhaki and Perlman, 1984; Naka, 1976; Naka and Rushton, 1966, 1967; Normann and Perlman, 1979; Norton et al., 1968; Werblin and Dowling, 1969), mammals (Bloomfield and Miller, 1982; Dacheux and Raviola, 1982; Nelson, 1977; Nelson et al., 1975; Niemeyer and Gouras, 1973; Steinberg, 1969a, 1969b), and primates (Dacey et al., 1996; Dacheux and Raviola, 1990; Verweije et al., 1999). Horizontal cells have now been studied by numerous investigators using anatomical, biochemical, pharmacological, and electrophysiological techniques. In this chapter, we shall try to summarize our current knowledge of horizontal cells in the vertebrate retina.