Circadian modulation of temporal properties of the rod pathway in larval Xenopus

Circadian clocks are integral components of visual systems. They help adjust an animal's vision to diurnal changes in ambient illumination. To understand how circadian clocks may adapt visual sensitivity, we investigated the spatial and temporal properties of optomotor responses of young Xenopus laevis tadpoles (Nieuwkoop and Faber, developmental stage 48) using a modified 2-alternative preferential-viewing method. We maintained animals in constant darkness and measured temporal sensitivity during their subjective day and night. We found that their behavioral responses can be explained in terms of 2 mechanisms with different temporal properties. The more sensitive mechanism operates at low temporal frequencies and intermediate wavelengths (λ_max = 520 nm), properties consistent with rod signals. Threshold for this mechanism is approximately 0.04 photoisomerizations rod ^-1 s^-1, consistent with single-photon detection. A less-sensitive mechanism responds to higher temporal frequencies (cutoff = 12 Hz) and has broad spectral sensitivity (370-720 nm), consistent with multiple classes of cone signals. This cone mechanism does not change, but the cutoff frequency of the more sensitive rod mechanism shifts from 0.35 Hz at night to 1.1 Hz during the subjective day, thereby enhancing the animal's sensitivity to dim rapidly changing stimuli. This day-night shift in rod temporal cutoff frequency cycles in complete darkness, characteristic of an endogenous circadian rhythm. The temporal properties of the behaviorally measured rod mechanism correspond closely with those of the electrophysiologically measured retinal response, indicating that the rod signals are modulated at the level of the outer retina.