Enhanced phase resetting in the synchronized suprachiasmatic nucleus network

The suprachiasmatic nucleus (SCN) adapts to both the external light-dark (LD) cycle and seasonal changes in day length. In short photoperiods, single-cell activity patterns are tightly synchronized (i.e., in phase); in long photoperiods, these patterns are relatively dispersed, causing lower amplitude rhythms. The limit cycle oscillator has been used to describe the SCN's circadian rhythmicity and predicts that following a given perturbation, high-amplitude SCN rhythms will shift less than low-amplitude rhythms. Some studies reported, however, that phase delays are larger when animals are entrained to a short photoperiod. Because phase advances and delays are mediated by partially distinct (i.e., nonoverlapping) biochemical pathways, we investigated the effect of a 4-h phase advance of the LD cycle in mice housed in either short (LD 8:16) or long (LD 16:8) photoperiods. In vitro recordings revealed a significantly larger phase advance in the SCN of mice entrained to short as compared to long photoperiods (4.2 ± 0.3 h v. 1.4 ± 0.9 h, respectively). Surprisingly, in mice with long photoperiods, the behavioral phase shift was larger than the phase shift of the SCN (3.7 ± 0.4 h v. 1.4 ± 0.9 h, respectively). To exclude a confounding influence of running-wheel activity on the magnitude of the shifts of the SCN, we repeated the experiments in the absence of running wheels and found similar shifts in the SCN in vitro in short and long days (3.0 ± 0.5 h v. 0.4 ± 0.9 h, respectively). Interestingly, removal of the running wheel reduced the phase-shifting capacity of mice in long days, leading to similar behavioral shifts in short and long photoperiods (1.0 ± 0.1 h v. 1.0 ± 0.4 h). As the behavioral shifts in the presence of wheels were larger than the shift of the SCN, it is suggested that additional, non-SCN neuronal networks in the brain are involved in regulating the timing of behavioral activity. On the basis of the phase shifts observed in vitro, we conclude that highly synchronized SCN networks with high-amplitude rhythms show a larger phase-shifting capacity than desynchronized networks of low amplitude.