Diurnality reconfigures circadian network dynamics in the suprachiasmatic nucleus

Abstract

Diurnal and nocturnal mammals occupy opposite temporal niches, but whether the suprachiasmatic nucleus (SCN), the central circadian pacemaker, follows the same intrinsic rules for timing adjustment and network coordination across species is unknown. Because SCN clock gene rhythms and population-level activity measurements look broadly similar across species, the prevailing interpretation in comparative studies has been that temporal niche differences are implemented upstream or downstream of the SCN. However, these coarse readouts do not test how clock resetting depends on circadian phase or how neuronal timing is coordinated across SCN space. Here, we combined long-duration ex vivo SCN recordings with optogenetic stimulation to compare SCN network dynamics in the nocturnal mouse (Mus musculus) and the diurnal four-striped grass mouse (Rhabdomys pumilio). Rhabdomys SCN molecular clock rhythms exhibited a longer intrinsic period and, under the same daily stimulation protocol, converged on a larger absolute phase angle relative to the stimulus. Molecular clock phase response curves differed in overall structure across circadian time between species, including pronounced early subjective day delays in Rhabdomys when Mus responses were minimal. Phase mapping of single-cell SCN calcium rhythms revealed species-specific spatial timing organization, with a graded dorsomedial-to-ventrolateral phase progression in Rhabdomys and a sharper transition in Mus. The Mus and Rhabdomys SCN can thus appear similar by coarse readouts yet diverge in phase-dependent molecular clock resetting and network timing organization. These results indicate that models placing temporal niche divergence solely outside the SCN are mechanistically incomplete.