Phase misalignment between suprachiasmatic neuronal oscillators impairs photic behavioral phase shifts but not photic induction of gene expression

The ability of the circadian pacemaker within the suprachiasmatic nucleus (SCN) to respond to light stimulation in a phase-specific manner constitutes the basis for photic entrainment of circadian rhythms. The neural basis for this phase specificity is unclear. We asked whether a lack of synchrony between SCN neurons, as reflected in phase misalignment between dorsomedial (dmSCN) and ventrolateral (vlSCN) neuronal oscillators in the rat, would impact the ability of the pacemaker to respond to phase-resetting light pulses. Light pulses delivered at maximal phase misalignment between the vlSCN and dmSCN oscillators increased expression of Per1 mRNA, regardless of the circadian phase of the dmSCN. However, phase shifts of locomotor activity were only observed when the vlSCN and dmSCN were phase aligned at the time of stimulation. Our results fit a model in which a vlSCN oscillator phase gates its own response to light and in turn relays light information to a dmSCN oscillator. This model predicts that the phase misalignment that results from circadian internal desynchronization could preserve the ability of light to induce gene expression within the master circadian clock but impair its ability to induce behavioral phase shifts.