Influence of light at night on murine anxiety- and depressive-like responses

Abstract

Individuals are increasingly exposed to light at night. Exposure to constant light (LL) disrupts circadian rhythms of locomotor activity, body temperature, hormones, and the sleep-wake cycle in animals. Other behavioural responses to LL have been reported, but are inconsistent. The present experiment sought to determine whether LL produces changes in affective responses and whether behavioural changes are mediated by alterations in glucocorticoid concentrations. Relative to conspecifics maintained in a light/dark cycle (LD, 16:8 light/dark), male Swiss-Webster mice exposed to LL for three weeks increased depressive-like behavioural responses as evaluated by the forced swim test and sucrose anhedonia. Furthermore, providing a light escape tube reversed the effects of LL in the forced swim test. LL mice displayed reduced anxiety as evaluated by the open field and elevated-plus maze. Glucocorticoid concentrations were reduced in the LL group suggesting that the affective behavioural responses to LL are not the result of elevated corticosterone. Additionally, mice housed in LD with a clear tube displayed increased paired testes mass as compared to LL mice. Taken together, these data provide evidence that exposure to unnatural lighting can induce significant changes in affect, increasing depressive-like and decreasing anxiety-like responses.

Introduction

With the advent of electrical lighting at the turn of the 20th century, individuals of many species, including humans, became exposed to bright and unnatural light at night. Urban development has further exacerbated the issue of light at night as lighting from infrastructure strays into the atmosphere. This “light pollution” is now affecting 99% of the population in the US and Europe and 62% of the world population [26]. Electric lights have not only created light pollution, but have permitted shift work at night, generally perturbing the sleep-wake patterns of humans [33]. Individuals exposed to light at night are at increased risk for heart disease [17], cancer [10], [35], sleep disturbances [12], [20], circadian rhythm dysfunctions [3], disrupted rhythmicity of neuroendocrine function (such as corticotrophin releasing hormone, glucocorticoids, and prolactin) [7], [30], mood disorders [13], and reproductive dysfunction [14], [36].

Housing animals in constant light (LL) conditions is useful for studying the effects of light at night in animal models. The majority of studies indicate that maintaining animals in LL conditions is deleterious, but the mechanisms underlying these harmful effects remain unspecified [26]. Continuous exposure to light strongly suppresses circadian rhythms of locomotion, body temperature, and the sleep-wake cycle of rodents [18], as well as generally elevating corticosterone concentrations [1], [38]. It is possible that exposure to light at night produces harmful effects on animals directly via disruption of biological clock function [28]. Another possibility, albeit not mutually exclusive, is that light exposure at night represents a chronic stressor [22] which can indirectly affect physiological and behavioural processes [21].

Seasonal lighting, abnormalities in circadian clock [2], and sleep disorders are associated with depression in some subpopulations [5]. Although depression is traditionally considered maladaptive in humans, depressive-like behavioural responses persist in other species and may be advantageous under certain conditions. For example, symptoms of human seasonal affective disorder (SAD), such as lethargy, anxiety, altered food intake, and loss of sexual behaviour may be adaptive and conserve energy during the reduced day lengths of winter for individuals of some rodent populations [32]. This study is designed to address whether another form of circadian disruption, light at night, also negatively impacts affective behaviour. Depressive behaviours in humans may have evolved under a similar seasonal context as that of rodents and remain susceptible to changes in environmental lighting. The unnatural light cycles to which humans are now exposed, and the irregular sleep patterns evoked by light at night, may interfere with typical responses to the annual cycle of changing day lengths.

Reports on the interaction of LL with depressive- and anxiety-like responses have been inconsistent. Although previous studies have reported altered brain morphology due to LL [21] and other forms of circadian disruption such as sleep deprivation [43], previously reported behavioural effects of LL are inconsistent. For example, LL has been reported to both influence memory [22] and have no effect on memory [6]. Additionally, although circadian disruption has been reported to lessen anxiety [34], the effect of LL on anxiety has not been well established [6], [22].

In the present experiment, we examined behavioural and glucocorticoid responses to LL exposure, focusing on the possible link between altered lighting and affective responses. Male Swiss-Webster mice were housed in either LL or a light/dark cycle. We attempted to ameliorate the stress-evoking effects of constant light by providing half the mice with an opaque tube to serve as a light escape. As a control for the environmental-enriching effects of the tube, half of the mice were provided with a clear tube. We hypothesized that LL would increase corticosterone concentrations and elevate depressive-like behavioural responses and that providing light escape would partially reverse these effects.