The retinal photoreceptor topography and daily responses to illumination in a nocturnal and a diurnal South African rodent

Abstract

A number of daily rhythms were investigated under different lighting conditions and the topographical arrangements of visual (rods/cones) and non-visual retinal photoreceptors (ipRGCs) determined, in the Namaqua rock mouse (Micaelamys namaquensis) and the four striped field mouse (Rhabdomys pumilio). The present study provides evidence that M. namaquensis possesses a distinctly nocturnal locomotor activity rhythm that is endogenously entrained by the light-dark cycle, with a near 24h period length. Females also seem to be more active than males, this may be due to females having higher levels of estrogen. The current investigation reveals that M. namaquensis and R. pumilio possess duplex retinas that are rod-dominated, but cone to rod ratios reflect the temporal niches of the species. Micaelamys namaquensis possesses far more rods than cones, whereas R. pumilio possesses a high amount of both rods and cones. Both species also seem to have dichromatic colour vision and although different topographical distributions of the rods, cones and ipRGCs are observed, the adaptive values of these features remain to be elucidated. The ipRGCs are sparsely distributed across the retinas of both species but in R. pumilio they are distinctly concentrated in the dorso-nasal quadrant. The effects of different photophase illuminances on the photoentrainment of various daily rhythms were tested. Across the various photophase illuminances, both species expressed daily activity patterns that are generally typical to the species, but brighter illuminances might be needed to increase diurnal activity in R. pumilio to levels that reflect its activity under natural conditions. The amplitude, but not the temporal expression of daily activity is affected and M. namaquensis seems to be more susceptible to different illuminances than R. pumilio. Unexpectedly, dim photophase lighting reduces daily activity in M. namaquensis. These responses appear to reflect the photoenvironments of the species under natural conditions. Furthermore, day/night urine production values generally reflect the activity patterns of the species. In M. namaquensis, the 6-SMT rhythm is attenuated by a brighter as opposed to a dimmer photophase cycle and likely indicates a sensitivity threshold of the melatonin rhythm that is below 330 lux. Rhabdomys pumilio appears to express an ultradian 6-SMT rhythm with similar mean daily values, yet with different temporal patterns, under both dim and bright photophases. Lastly, the effects of differing photophase wavelengths on the photoentrainment of various daily rhythms were investigated. Long wavelength photophase lighting slightly increases daytime activity in both species. In M. namaquensis, this is probably due to the visual capabilities of the species, but in R. pumilio, lower stress levels under a long wavelength photophase, is the most likely cause. In both species, short wavelength photophase lighting attenuates the overall daily urine production rhythm, while medium and long wavelengths exert similar effects. Furthermore, there is an inverse correlation between the wavelength of the photophase and the level of daily 6-SMT as well as with corticosterone. The results also indicate the involvement of the ipRGCs, in mediating urine, melatonin and corticosterone production in M. namaquensis and in R. pumilio. It is clear that light plays an integral role in adjusting physiology and behaviour in these animals and a wide range of anatomical and physiological features reflect different adaptations according to their respective temporal niches.