The impact of daytime light exposure on diurnal and circadian rhythms in the diurnal rodent Rhabdomys pumillio

Throughout our evolutionary history, the rotation of the earth upon its axis imposed a highly predictable and large amplitude twenty four hour rhythm in the amount of light to which we were exposed. The advent of artificial lighting has fundamentally disrupted this relationship in two ways. Firstly, it allows us to experience unnaturally high levels of light at night. Secondly, it allows us to spend most of our waking time indoors, exposed to unnaturally low light levels during the day. Significant attention has been paid to the deleterious effects of light at night, with evidence from both animal and human studies that this disrupts the endogenous timing mechanisms (circadian clocks) that define 24hr rhythms in our physiology and behaviour and inhibits sleep, with knock-on consequences for general health and daytime performance. By contrast, the impact of reduced light intensity during the day has been much less studied. This is a shame because, while it is practically inconceivable that we could reverse the progress of the last >100 years and persuade people to avoid unnatural sources of light at night, increasing levels of daytime light could be readily achieved by changes to architectural lighting design or even just by encouraging people to spend more time outdoors. There is evidence from humans that increasing light during the day improves alertness and cognitive performance, and that in the long term it can change the phase, increase the amplitude, and reduce the photosensitivity of circadian rhythms. However, the literature is sparse and lacks a systematic study of the impact of daytime light levels on temporal physiology. Here we set out to address this deficit and ask what impact, if any, changing daytime light exposure has on 24hr rhythms in behaviour and physiology. We then continue to ask whether increases in daytime light intensity can ameliorate some of the disruptive effects of light at night.

We will address these questions by studying laboratory rodents. There is a rich history of translating findings from laboratory animals to humans in the field of circadian biology. Working in laboratory animals has the huge advantage of allowing researchers to carefully control environmental conditions over many days/weeks in a way that is difficult to achieve in human studies in the laboratory, let alone under field conditions. Fortunately, general principles established in the laboratory have proven to have good utility for understanding rhythmic physiology of humans in the real world. A substantial challenge in applying this well-worn approach to the questions posed in this proposal is that commonly employed laboratory rodents (mice, rats, hamsters) are nocturnal and would not normally experience bright daytime light. Indeed, in the lab they employ behavioural strategies to reduce their daytime light exposure - build nests, seek shade, shield their eyes during sleep. If we are to understand the impact of changing daytime light levels on circadian organisation and the disruptive effects of light at night we therefore need a species that, like humans, actively seeks daytime light exposure. We have established a colony of such animals in Manchester in preparation for this proposal. Rhabdomys pumillio is a species of mouse from Africa, slightly larger than ordinary lab mice. Importantly though, in both their natural environment and in the lab they are substantially day active. Accordingly, they also have a visual system that, like our own, is optimised for seeing in bright light. In this proposal we will carefully change the intensity of daytime light and monitor the impact on daily rhythms in behaviour and physiology in Rhabdomys. We will then ask whether increasing daytime light exposure ameliorates the disruptive effects of nighttime light exposure, with especial emphasis on the sort of nocturnal lighting patterns experienced by people.

In mammals a master circadian oscillator in the suprachiasmatic nuclei (SCN) orchestrates 24hr rhythms in almost every body system. The SCN generates an endogenous circadian rhythm, but the light:dark cycle provides important external regulation. On the one hand, the SCN clock is synchronised (or entrained) to the diurnal light:dark cycle, on the other, light has direct effects on many behavioural and physiological systems that serve to re-enforce differences between day and night. There is extensive data on the impact of nocturnal light on the circadian clock. Nocturnal light pulses shift clock phase and reduce amplitude of physiological and behavioural rhythms. Chronic light at night impairs mood and general health. By contrast, the influence of light exposure through the day on circadian physiology has received less attention. Some human studies indicate that increasing daytime light exposure can have beneficial effects and reduce sensitivity to the deleterious impact of light at night. Our goal is to test the hypothesis that increasing daytime irradiance has beneficial effects for temporal biology. Accordingly, we propose a rigorous examination of the impact of daytime irradiance on rhythmic physiology. As common laboratory rodents avoid light we propose using the diurnal murid Rhabdomys for these experiments. The independent variable for our experiments will be daytime irradiance, which we will vary from levels typical of dim indoor lighting to moderate daylight. As dependent variables we will measure phase, amplitude, and period of daily rhythms in behaviour, physiology and SCN electrical activity; synchrony of individual oscillators within the SCN and among oscillators in peripheral tissues; and sensitivity of the clock to light pulses at night. We will then assess whether increasing daytime irradiance can ameliorate the deleterious effects of chronic exposure to analytical and naturalistic patterns of exposure to nocturnal light.

We aim to determine whether increasing daytime light exposure has beneficial effects on circadian rhythms. This question is of immediate practical importance and will have impact directly addressing the BBSRC strategic priorities of: 'Research to inform public policy'; 'Welfare of managed animals'; and 'Healthy ageing across the life course'.

Strategic priorities 'Research to inform public policy' and 'Healthy ageing':
Across the industrialised world people spend most of the day indoors. This means that we as individuals, and the organisations and authorities producing and maintaining buildings, need to make decisions every day about what constitutes an optimal indoor environment. To date, the appropriate amount of light has been defined on the basis of the requirements of high acuity and colour vision, and the imperatives to reduce energy usage and carbon footprint (e.g. European Regulations 244/2009 and 859/2009 as well as 245/2009 and 347/2010). As a result, the light level (irradiance) in most indoor environments is far below that of natural daylight. There are suggestions from human experiments that increasing daytime light exposure could have beneficial effects for health and wellbeing by increasing the amplitude of daily rhythms in physiology and behaviour; advancing their phase with respect to local time; and reducing the detrimental impact of light exposure at night. If these findings prove robust then that would argue for a reconsideration of indoor lighting levels to more closely approximate natural daylight. However, that decision would cost money and in most cases also increase carbon usage. It is therefore not a decision to be taken lightly. We thus urgently need a more complete understanding of how increasing daytime light exposure impacts biological rhythms.

The current proposal aims to establish the fundamental relationship between daytime light exposure and circadian rhythm parameters in a carefully controlled laboratory setting using a diurnal animal. The outcome of these experiments will therefore provide a unique insight into this question. If our data indicate that higher daytime irradiance does indeed have beneficial effects then this should be included in considerations of appropriate artificial and architectural lighting, and in the regulatory framework surrounding it. Ultimately then, everyone who spends their days indoors may benefit from this development, although those who are particularly restricted to indoor environments in e.g. hospitals, nursing homes etc might be especially affected. If on the other hand, we find that under controlled conditions the impact of increased daytime irradiance is rather slight, that should contribute to arguments that other considerations in lighting design take priority. Again, we would all be beneficiaries of that outcome in view of the potential reduction in the cost and carbon footprint of lighting.

As reduced access to natural light is a particular problem for the elderly who may have limited mobility and/or require care in residential care homes/hospital these impacts will be especially relevant to the BBSRC priority of 'healthy ageing'. Moreover, as the internal environment is subject to government regulation, and as our findings will have special impact for lighting design in public buildings e.g. hospitals and schools, this impact will also be relevant to the 'Research to inform public policy' priority area.

Strategic priority 'Welfare of managed animals':
Many millions of farm animals around the world are kept indoors with restricted access to natural daylight for at least a part of their lives. The question of what is the appropriate amount of daytime light is at least as relevant to the welfare of these animals as it is to humans. Diurnal/circadian rhythmicity is a near universal feature of animal physiology. Conditions that optimise temporal order could improve mood and general health for farm animals just as they could for humans.