Distinct Components of Photoperiodic Light Are Differentially Encoded by the Mammalian Circadian Clock.

Abstract

Seasonal light cycles influence multiple physiological functions and are mediated through photoperiodic encoding by the circadian system. Despite our knowledge of the strong connection between seasonal light input and downstream circadian changes, less is known about the specific components of seasonal light cycles that are encoded and induce persistent changes in the circadian system. Using combinations of 3 T cycles (23, 24, 26 h) and 2 photoperiods per T cycle (long and short, with duty cycles scaled to each T cycle), we investigate the after-effects of entrainment to these 6 light cycles. We measure locomotor behavior duration (α), period (τ), and entrained phase angle (ψ) in vivo and SCN phase distribution (σφ), τ, and ψ ex vivo to refine our understanding of critical light components for influencing particular circadian properties. We find that both photoperiod and T-cycle length drive determination of in vivo ψ but differentially influence after-effects in α and τ, with photoperiod driving changes in α and photoperiod length and T-cycle length combining to influence τ. Using skeleton photoperiods, we demonstrate that in vivo ψ is determined by both parametric and nonparametric components, while changes in α are driven nonparametrically. Within the ex vivo SCN, we find that ψ and σφ of the PER2∷LUCIFERASE rhythm follow closely with their likely behavioral counterparts (ψ and α of the locomotor activity rhythm) while also confirming previous reports of τ after-effects of gene expression rhythms showing negative correlations with behavioral τ after-effects in response to T cycles. We demonstrate that within-SCN σφ changes, thought to underlie α changes in vivo, are induced primarily nonparametrically. Taken together, our results demonstrate that distinct components of seasonal light input differentially influence ψ, α, and τ and suggest the possibility of separate mechanisms driving the persistent changes in circadian behaviors mediated by seasonal light.