The human circadian system adapts to prior photic history

Abstract

Light is the most potent stimulus for synchronizing the endogenous circadian timing system to the 24 h day. The timing, intensity, duration, pattern and wavelength of light are known to modulate photic resetting of the circadian system and acute suppression of melatonin secretion. The effect of prior photic history on these processes, however, is not well understood. Although previous studies have shown that light history affects the suppression of melatonin in response to a subsequent light exposure, here we show for the first time that a very dim light history, as opposed to a typical indoor room illuminance, amplifies the phase-shifting response to a subsequent sub-saturating light stimulus by 60–70%. This greater efficacy provides evidence for dynamic adaptive changes in the sensitivity of circadian ocular photoreception. This plasticity has important implications for the optimization of light therapy for the treatment of circadian rhythm sleep disorders.

Figure 1. Double-plotted raster of the 32 day protocol

This raster represents one of the two study designs, i.e. with the sequence of the prior light history being 1 lux for the first half and 90 lux for the second half of the protocol, as an example for a subject with a habitual bedtime of 24.00 h. Different light levels are represented by the following coloured bars: white (450 lux on days 2–4 and 17–19), light grey (90 lux on days 1, 20–23, and 26–28), dark grey (1 lux on days 5–7 and 11–14), and black (sleep episodes in 0 lux). Constant posture conditions are denoted by bars with horizontal stripes. Four 6.5 h LE sessions are represented by bars with a sun symbol: 2 control LE (days 8 and 23) and 2 experimental LE (days 14 and 29).

Figure 2. Melatonin profiles under different light conditions

Individual melatonin profiles from 13 subjects during 4 different light conditions: 1 lux prior light history and 90 lux LE (A), 90 lux prior light history and 90 lux LE (B), 1 lux prior light history and 1 lux LE (C), and 90 lux prior light history and 1 lux LE (D). Hourly plasma melatonin levels are shown for 72 h (3 consecutive days) beginning on the day prior to LE (hour 0) in each condition. The vertical bar from 27 to 33.5 h on each panel shows the 6.5 h LE and the top horizontal bar shows the light history and the light conditions prior to and following the LE. Panel C shows the control condition for panel A, and panel D is the control condition for panel B. Note the strong suppression in panel A, compared with weak suppression in panel B.

Figure 3. Adaptation of the response of melatonin suppression and phase shifts by prior light history

The effect of different prior light history conditions on individual melatonin suppression (A), and phase shifts (B), induced by a 90 lux LE. Data from 13 individuals are shown in the black filled symbols and the group means ±s.d. are represented by the open symbols. The melatonin suppression and phase shift data were corrected for the corresponding control LE.