Research articleBrief light exposure at night disrupts the circadian rhythms in eye growth and choroidal thickness in chicks
Introduction
Until the advent of artificial lighting over the past 2–3 centuries, life was adapted to daily 24-h cycles of darkness and light, and animals (including man) have developed endogenous circadian rhythms synchronized to this cycle, to optimize survival strategies. The modern use of artificial light indoors during both day and night has permanently altered the natural lighting cycle. The negative impact of the increasing prevalence of nighttime illumination resulting from city lights and modern conveniences such as luminous signs on the night environment (Cinzano et al., 2001) and nocturnal species may extend to the realm of human health concerns (Chepesiuk, 2009, Stevens et al., 2013). For instance, bedroom night-lights were associated with the development of myopia in children (Quinn et al., 1999) (however this remains controversial as two subsequent studies found no such association (Gwiazda et al., 2000, Zadnik et al., 2000). Scientific studies have recently linked light at night to increased risk for cancers (review: (Feillet et al., 2015), metabolic changes leading to obesity, mood disorders and cardiovascular disease (Chepesiuk, 2009, Anisimov et al., 2012, Stevens et al., 2013). Even dim light at night, for instance, from computer screens or televisions, can adversely affect the rhythm in melatonin, a hormone that influences sleep and daily rhythms of physiology, which then leads to alternations in the rhythms in loco–motor activity and core body temperature (Fonken et al., 2013, Borniger et al., 2014). The physiological basis of these adverse effects is the impingement of light on the clock driving endogenous rhythms (Wyse et al., 2011, Anisimov et al., 2012). It is well established that brief periods of light at certain times of night (dark part of the L/D cycle) have effects on the phases of circadian systems; these effects are generally most robust when close to dawn (lights on) or dusk (lights off), causing phase advances and delays, respectively. However, light in the middle of the night can also affect the clock, and cause a dampening of the rhythm amplitude, and/or acute affects.
Circadian disturbances, including phase shifts and effects on circadian clock outputs (e.g., melatonin or dopamine) (Stevens et al., 2013) may have profound effects on refractive development. This was first shown in chickens that were reared under constant light conditions: eyes grew excessively long and the corneas flattened (Lauber et al., 1961, Lauber and McGinnis, 1966, Li et al., 1995). Constant darkness too, caused excessive eye growth (Gottlieb et al., 1987). The resulting ametropias (refractive errors) depended on the length of time in the abnormal lighting condition, but it was undisputable that eye growth was altered. In chickens (Weiss and Schaeffel, 1993, Nickla et al., 1998b, Nickla et al., 1998a, Papastergiou et al., 1998) as well as in primates (Nickla et al., 2002) including humans (Stone et al., 2004, Wilson et al., 2006, Chakraborty et al., 2011), the length of the eye oscillates in a diurnal manner, increasing in length during the day and stopping growth, or even decreasing in length, at night. The thickness of the choroid also shows a diurnal rhythm, the phase of which is opposite that of eye length: choroids thicken at night and thin during the day (Nickla et al., 1998b, Nickla et al., 1998a, Brown et al., 2009, Chakraborty et al., 2011). It has been found that circadian disruptions in these rhythms are associated with alterations in ocular growth patterns and refractive development: their phases and/or amplitudes are altered in eyes growing too fast, in response to form deprivation (no image) or negative lens-induced hyperopic defocus (image focused behind the retina), or too slowly, in response to positive lens-induced myopic defocus (image focused in front of the retina) (Nickla et al., 1998b, Nickla et al., 1998a, Papastergiou et al., 1998, Nickla, 2006). In all of these previous experiments documenting the effects of abnormal visual conditions on eye growth, eyes were continuously exposed to the visual condition, which could be argued does not approximate the common visual experience of children, whose nighttime exposure to light would likely not be continuous, but rather for relatively brief periods. With this in mind, we examined the effects of 2 h of light exposure, in the middle of the night, on the circadian rhythms in axial length and choroid thickness, and on eye growth rate, in young chicks. We report that light at night disrupts the sinusoidal diurnal rhythms in axial length and choroidal thickness. Parts of this manuscript have been presented in abstract form (Nickla and Totonelly, 2013).
Section snippets
Subjects
White Leghorn chicks (Gallus gallus domesticus) were hatched in an incubator and raised from day one in temperature – controlled brooders. The light cycle was 14L/10D; the light level in the brooders was about 500 lux. Food and water were supplied ad libitum. Care and use of the animals conformed to the ARVO Resolution for the Care and Use of Animals in Research.
Diurnal rhythms in axial length and choroidal thickness
Starting at 12-days of age, birds received 2 h of light (700 lux) between 12:00 am and 2:00 am for 7 days (n = 12; only one eye was
Axial length
Time-of-day accounts for the differences in “interval” changes in axial length between chicks given light at night versus those in a dark night (Figure 1A, 2-way ANOVA: Full data set (white bars): F3,72 = 3.93; p = 0.012; Subset (circles): F3,54 = 6.5; p = 0.0008). Light at night caused an “acute” growth stimulation over the 6-h interval starting with the period of lights-on (between mid-night and 6 am) for both data sets (48 and 91 μm vs −28 μm; p = 0.012; p = 0.0019 respectively). There was
Discussion
We report that daily 2-h exposures to light in the middle of the night cause “acute” episodes of eye growth stimulation immediately upon exposure to the stimulus, that lasts for at least 6 h. This acute stimulation occurs within one week of the start of the night light exposure, and may be responsible for the increased growth rate seen four weeks later. The acute stimulation results in the loss of the diurnal sinusoidal rhythm in axial length found in control eyes in an uninterrupted night.
Acknowledgments
This work was funded by NIH-NEI-013636. The authors thank Dr. Li Deng (NECO) for help with the statistical analyses, and Pearl Thai and Rinita Zanzerkia for some data collection.
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