Synchronous period-doubling in flicker vision of salamander and man

Periodic flashes of light have long served to probe the temporal properties of the visual system. Here we show that during rapid flicker of high contrast and intensity the eye reports to the brain only every other flash of light. In this regime, retinal ganglion cells of the salamander fire spikes on alternating flashes. Neurons across the entire retina are locked to the same hashes. The effect depends sharply on contrast and flash frequency. It results from a period-doubling bifurcation in retinal processing, and a simple model of nonlinear feedback reproduces the phenomenon. Pharmacological studies indicate that the critical feedback interactions require only cone photoreceptors and bipolar cells. Analogous period-doubling is observed in the human visual system. Under bright full-field flicker, the electroretinogram (ERG) shows a regime of period-doubling between 30 and 70 Hz. In visual evoked potentials from the occiput, the subharmonic component is even stronger. By analyzing the accompanying perceptual effects, we find that retinal period-doubling begins in the periphery of the visual field, and that it is the cause of a long mysterious illusory flicker pattern.