Electrical and Metabolic Manifestations of Receptor and Higher-Order Neuron Activity in Vertebrate Retina

The interstitial voltages, currents, and resistances of the receptor layer of the isolated rat retina have been investigated with arrays of micropipette electrodes inserted under direct visual observation by infrared microscopy. In darkness a steady current flows inward through the plasma membrane of the rod outer segments. It is balanced by equal outward current distributed along the remainder of each rod. Flashes of light produce a photocurrent which transiently reduces the dark current with a waveform resembling the PII and a-wave components of the electroretinogram. The photocurrent is produced by a local action of light within 12 mum of its point of absorption in the outer segments. The quantum current gain of the photocurrent is greater than 10(6). The electrical space constant of rat rods is greater than 25 mum, so that the electrical effects of the photocurrent are large enough at the rod synapses to permit single absorbed photons to be detected by the visual system. The photocurrent is apparently the primary sensory consequence of light absorption by rhodopsin.

1. Intracellular recordings have been made from single photoreceptors in the retina of the turtle. Histological sections of the retina made after injection of dye through the recording electrode reveal dye in the inner segments of single cones.2. Following a brief flash of light the cone undergoes a hyperpolarization which is graded with the intensity of the flash.3. The excitatory receptive field of a receptor is probably as small as the cross-section of a single cone, but accurate measurements are rendered difficult by scattering of light within the retina.4. The voltage drop produced by a current injected into the cell is increased during the response to light. Steady hyperpolarizing currents increase the size of the response to light; depolarizing currents of increasing strength reduce and then reverse the response.5. The results are consistent with the hypothesis that light activates the visual cell by decreasing the permeability of membrane channels which in darkness act as a shunt of the membrane.