Perinatal photoperiod imprints the circadian clock

Abstract

Using real-time gene expression imaging and behavioral analysis, we found that the perinatal photoperiod has lasting effects on the circadian rhythms expressed by clock neurons as well as on mouse behavior, and sets the responsiveness of the biological clock to subsequent changes in photoperiod. These developmental gene × environment interactions tune circadian clock responses to subsequent seasonal photoperiods and may contribute to the influence of season on neurobehavioral disorders in humans.

Figure 1

Persistent effects of perinatal seasonal photoperiod on SCN slice, on SCN neuronal rhythms, and on behavior. Duration of the SCN peak (a) and neuronal peak (b) in Per1::GFP expression, measured as the time from 50% maximum on the rising phase to 50% maximum on the falling phase of the molecular circadian rhythm. c, Neuronal phase variance calculated from the peak times of individual SCN neurons using Rayleigh circular statistics. d, Neuronal period calculated on the first full circadian cycle recorded ex vivo. e, SCN period calculated from the first full circadian cycle recorded ex vivo. f, Behavioral period calculated from the first three days in DD. Short-day developmental photoperiod (black bar), equinox developmental photoperiod (grey bar), long-day developmental photoperiod (white bar); asterisks (*) denote significance (two-way ANOVA, main effect for perinatal photoperiod, p < 0.05).

Figure 2

Interactions of perinatal seasonal photoperiod with subsequent seasonal photoperiod. a, Two-way ANOVA interaction plot for peak times of Per1::GFP expression in SCN. Developmental photoperiod on X-axis; continuation photoperiod: short-day (LD 8:16) represented by black circles, equinox (LD 12:12) represented by grey inverted triangles and long-day (LD 16:8) represented by open triangles (see inset legend). b, Timing of SCN molecular rhythm peaks relative to dusk. White background represents “lights-on,” while grey background represents “lights-off.” Photoperiodic paradigm represented as “Developmental:Continuation” with “L” representing long-day photoperiod, “E” representing equinox photoperiod and “S” representing short-day photoperiod. c, Two-way ANOVA interaction plot for waveform duration from 50% rise to 50% fall of the first peak ex vivo. d, Behavioral duration of activity per circadian cycle in the first three days of constant darkness. Error bars represent SEM. Significance is indicated by letters such that means sharing a letter are not significantly different. Significance ascribed at p < 0.05.