Modeling circadian rhythm splitting under chronic light and the asymmetric transition kinetics between lighting conditions

In various vertebrates, chronic light splits the single daily 24-h circadian activity bout into two 12-h behavioral components per cycle, yet the underlying mechanism remains unresolved. Here, we develop a two-lobe biophysical model of the suprachiasmatic nucleus (SCN) to understand this phenomenon. By representing the master clock as interacting ventral core and dorsal shell populations of Kuramoto-type oscillators across bilateral lobes, we suggest that chronic light changes the excitation/inhibition (E/I) balance orchestrated by GABA, which either inhibits or excites SCN neurons. Under constant darkness, excitation dominates and provides in-phase synchronization of the populations. Under chronic light, inhibition dominates, and the ipsilateral and contralateral couplings among the core and shell populations become negative. Consequently, the shells in the left and right lobes oscillate in antiphase, producing the 12-h behavioral rhythm in downstream tissues. We suggest that this E/I balance is shifted by a light-induced change in the expression of chloride cotransporters in SCN neurons. Another key novelty is the introduction of the biologically motivated dynamics of chloride cotransporter expression, which explains the sign inversion of ipsilateral and contralateral couplings under time-varying lighting conditions. The model also reproduces the effects of unilateral SCN lesions: if one lobe is abolished, the remaining intact lobe autonomously stabilizes into a single-bout circadian output with a period comparable to that of the intact system. Finally, we compare our results with experimental data and demonstrate a close agreement.