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Increased Sensitivity of the Circadian System to Light in Early/Mid-Puberty

Abstract

Context:

Late adolescence is marked by a delay in sleep timing, which is partly driven by a delay shift of the circadian timing system. This study examined whether the sensitivity of the circadian system to light—the primary entraining stimulus to the circadian system—differs between pre- to mid-pubertal and late to postpubertal adolescents.

Objective:

The study was designed to determine the influence of puberty on the sensitivity of the circadian system to light in humans.

Methods:

Melatonin suppression to low and moderate light levels was assessed in 38 pre- to mid-pubertal (9.1–14.7 years) and 29 late to postpubertal (11.5–15.9 years) adolescents. They received 1 hour of four light levels on consecutive nights: approximately 0.1 (near-dark baseline condition), 15, 150, and 500 lux. One group received evening light beginning at 11:00 pm (n = 39); a second group received morning light beginning at 3:00 am (n = 28). Salivary melatonin was sampled every 30 minutes. Melatonin suppression for 15, 150, and 500 lux was calculated relative to unsuppressed baseline levels in the 0.1 lux setting, within individuals.

Results:

The pre- to mid-pubertal group showed significantly greater melatonin suppression to 15 lux (9.2 ± 20.5%), 150 lux (26.0 ± 17.7%), and 500 lux (36.9 ± 11.4%) during evening light exposure compared to the late to postpubertal group (−5.3 ± 17.7%, 12.5 ± 17.3%, and 23.9 ± 21.7%, respectively; P < .05). No significant differences were seen between developmental groups in morning melatonin suppression.

Conclusion:

These results indicate support for a greater sensitivity to evening light in early pubertal children. The increased sensitivity to light in younger adolescents suggests that exposure to evening light could be particularly disruptive to sleep regulation for this group.

The most prominent developmental change in sleep patterns during adolescence is a shift in the timing of sleep, such that sleep is markedly delayed (1–9). The adolescent phase delay is partly driven by psychosocial factors, such as peer and media influence, increased social opportunities, assertion of autonomy, withdrawal of parental control, and personal preference (10, 11). Several findings, however, indicate that a phase delay occurs in parallel with physical signs of puberty (12, 13), and the phase delay may therefore be initiated by a biological process involving developmental changes in the circadian timing system (14–16).

Whether the maturational process of adolescence is linked to a change in the underlying circadian timing mechanism that alters sleep timing relative to the 24-hour day/night cycle is unclear. One mechanism that can produce delayed phase position is modification of the circadian timing system's sensitivity to entraining light signals. In a previous field study of adolescents followed from ninth to tenth grades (a transition that involved a 65-minute advance of school starting time) (17), we predicted that circadian phase (salivary dim light melatonin onset) would move to an earlier hour because adolescents were exposed to more light in the early morning. In fact, however, these adolescents manifested a phase delay in spite of an earlier rising time and no change in sleep onset time (17). Thus, either the phase delay of adolescence continues into late/postpubertal development (all subjects in the study were generally late pubertal adolescents), the circadian timing mechanism is unresponsive to morning light, or the added morning light was not sufficient to produce a phase advance or to resist further delay.

The current study evaluated the hypothesis that pubertal development is associated with an increased sensitivity to evening light and decreased sensitivity to morning light. If a transformation of the circadian timing system is related to a pubertal phase delay, then more mature adolescents should show greater melatonin suppression to light in the evening and less mature adolescents should suppress more to morning light. Such a change could explain why mid- to late pubertal adolescents express a marked delay in sleep timing and why we found that waking early in the morning was ineffective in producing phase advances in circadian timing during late adolescence (17).