Extreme responsiveness of the pupil of the dark-adapted mouse to steady retinal illumination

PURPOSE. To measure the dependence of the size of the pupils of mice on steady retinal illumination. METHODS. Anesthetized C57BL/6 mice aged 7 to 8 weeks were placed in a ganzfeld chamber in darkness, and in monochromatic (510 nm) and white light whose intensity was varied more than 6 log units. The pupils of the mice were photographed with an infrared video camera and recorded on videotape and the pupil areas determined by digital image analysis of the video recordings. RESULTS. Fully dark-adapted murine pupils had an area of 2.29 ± 0.35 mm². The minimum pupil size at saturating intensity was 0.10 ± 0.05 mm². The steady state pupil area declined to half its dark-adapted maximum when ganzfeld luminance was 10^-5 scotopic candela (scot. cd) per meter squared. Pupil area declined to 20% of the dark-adapted magnitude at approximately 10^-3 scot. cd/m². CONCLUSIONS. The mouse pupil can regulate retinal illumination by a factor exceeding 20. The neural circuitry that determines steady state murine pupil size is extremely sensitive to retinal illumination and under these experimental conditions is controlled almost exclusively by rod signals. This follows, because the ganzfeld illuminance (10^-5 scot. cd/m²) that causes the pupil to constrict to half its dark-adapted value corresponds to only approximately 0.01 photoisomerization per rod per second, whereas 80% reduction in pupil area occurs at approximately 1 photoisomerization per rod per sec. Based on this extreme responsiveness to steady illumination, the hypothesis is proposed that the murine pupil functions to protect a retinal circuit that can become saturated at extremely low photon capture rates. General principles of dark- adapted retinal circuitry support the identification of the first three neurons in the circuit as the rod, the rod bipolar, and the AII-amacrine. The rod and rod bipolar neurons do not approach saturation at the intensities at which the pupil constricts, however, and it seems unlikely that the AII- amacrine does. Thus the retinal neurons protected from saturation by the mouse pupil constrictions are probably ganglion cells with large receptive fields that have sustained responses.