Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities

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Abstract
The intrinsically photosensitive melanopsin-expressing retinal ganglion neurons are important for nonvisual responses to light, such as circadian photoentrainment. These cells, however, require high light intensities to be activated and it has been unclear how photoentrainment to low light levels works. This study finds that rod photoreceptors are essential to photoentrainment at low and middle light intensities. In mammals, synchronization of the circadian pacemaker in the hypothalamus is achieved through direct input from the eyes conveyed by intrinsically photosensitive retinal ganglion cells (ipRGCs). Circadian photoentrainment can be maintained by rod and cone photoreceptors, but their functional contributions and their retinal circuits that impinge on ipRGCs are not well understood. Using mice that lack functional rods or in which rods are the only functional photoreceptors, we found that rods were solely responsible for photoentrainment at scotopic light intensities. Rods were also capable of driving circadian photoentrainment at photopic intensities at which they were incapable of supporting a visually guided behavior. Using mice in which cone photoreceptors were ablated, we found that rods signal through cones at high light intensities, but not at low light intensities. Thus, rods use two distinct retinal circuits to drive ipRGC function to support circadian photoentrainment across a wide range of light intensities.