Night and day: distinct retinohypothalamic innervation patterns predict the development of nocturnality and diurnality in two murid rodent species

How does the brain develop differently to support nocturnality in some mammals, but diurnality in others? To answer this question, one might look to the suprachiasmatic nucleus (SCN), the pacemaker of the mammalian brain, which is required for all circadian biological and behavioral rhythms. Light arriving at the retina entrains the SCN to the daily light-dark cycle via the retinohypothalamic tract (RHT). However, in all mammals studied thus far, whether nocturnal or diurnal, the SCN exhibits a rhythm of increased activity during the day and decreased activity at night. Therefore, structures downstream of the SCN are likely to determine whether a species is nocturnal or diurnal. From an evolutionary perspective, nocturnality appears to be the primitive condition in mammals, with diurnality having reemerged independently in some lineages. However, it is unclear what mechanisms underlie the development of one or the other circadian phase preference. In adult Norway rats (Rattus norvegicus), which are nocturnal, the RHT also projects to the ventral subparaventricular zone (vSPVZ), an adjacent region that expresses an in-phase pattern of SCN-vSPVZ neuronal activity (in other words, activity in the SCN and vSPVZ increase and decrease together). In contrast, in adult Nile grass rats (Arvicanthis niloticus), a diurnal species that is closely related to Norway rats, an anti-phase pattern of SCN-vSPVZ neuronal activity is expressed (in other words, activity in the SCN increases as activity in the vSPVZ decreases, and vice versa). We hypothesized that these species differences in activity pattern result in part from a weak or absent RHT-to-vSPVZ projection in grass rats. Using a developmental comparative approach, we assessed differences in behavior, hypothalamic activity, and RHT and SCN connectivity to the vSPVZ between these two species. We report that a robust retina-to-vSPVZ projection develops in Norway rats around the end of the second postnatal week when nocturnal wakefulness and the in-phase pattern of SCN-vSPVZ activity emerge. In grass rats, however, such a projection does not develop and the emergence of the anti-phase SCN-vSPVZ activity pattern during the second postnatal week is accompanied by increased diurnal wakefulness. When considered within the context of previously published reports on RHT projections in a variety of other nocturnal and diurnal species, our current findings suggest that how and when the retina connects to the hypothalamus differentially shapes brain and behavior to produce animals that occupy opposing temporal niches.