Attenuated effect of increased daylength on activity rhythm in the old mouse lemur, a non-human primate

Abstract

Adaptation of physiological and behavioral functions to seasonal changes in daylength is of major relevance for optimal fitness and survival. Because aging is characterized by changes in biological rhythms, it may be hypothesized that old animals fall short of showing a full adaptation to prolonged changes in the duration of daily light exposure, as naturally occurring in relation to season in younger individuals. To test this hypothesis, we analyzed changes in the patterns of daily locomotor activity and body temperature rhythms of young and old mouse lemurs (Microcebus murinus, Primates) exposed to short and long daylengths. The effect of an increase in the duration of daily light exposure was attenuated in old animals, as compared to younger lemurs. Although some age-related differences in the locomotor activity rhythm could be seen under exposure to short daylength, they were predominant under long daylength. Some mechanisms allowing adaptation to changing daylength thus seem to be impaired at old age. Changes in coupling of circadian oscillators to the light–dark cycle and disturbances in the physiological responses to change in light duration should be further investigated.

Introduction

Aging is associated with changes in circadian rhythmicity of endocrine, metabolic and behavioral parameters in humans (Weinert, 2000, Van Someren and Riemersma-Van Der Lek, 2007). It has been demonstrated for various circadian rhythms that aging is characterized by a decrease in amplitude, a phase advance and an impaired resynchronization following abrupt phase shifts in the light–dark cycle. In humans, aging modifies the daily rhythm of rest–activity. Aging is typically associated with (1) an increased fragmentation into shorter alternating periods of rest and activity; (2) an increased activity level during the major sleep period, (3) a decreased activity level during the major active period, and as a consequence (4) a decreased amplitude (Witting et al., 1990, Myers and Badia, 1995, Huang et al., 2002). The amplitude, pattern and phasing of the 24-h profile of body temperature also change with aging (Monk et al., 1995, Duffy et al., 1998, Gubin et al., 2006). However, some of the age-related changes can be ameliorated by increasing the exposure to artificial bright light (Van Someren et al., 2002). Moreover, there is now some evidence that human rhythms are influenced by season through changes in the duration of daylength (Bronson, 2004), and it appears of interest to experimentally test the effect of daylength changes on the circadian rhythms of young and old subjects. However, changes in the duration of light exposure have rarely been taken into account in studies on circadian rhythms of old humans.

The effects of age on the circadian clock system have also been extensively studied in rodents (e.g. (Zee et al., 1992, Penev et al., 1997, Valentinuzzi et al., 1997, Mailloux et al., 1999, Zhang et al., 2000)), confirming rhythm disturbances such as an increased fragmentation and decreased amplitude of the daily locomotor activity rhythm, as well as a decreased precision in the onset of activity phase. Previous work in rodents and primates indicates that the sensitivity of the circadian timing system to short-term manipulation of light exposure may decrease with age (Zhang et al., 1996, Benloucif et al., 1997, Aujard et al., 2001). Taken together, these data suggest that age could have profound effects on the synchronization of circadian rhythms to changes in daylength. Rodent studies have shown that the effect of photoperiod on the temporal organization of daily rhythms is modulated by age (Scarbrough et al., 1997, Benstaali et al., 2002). In primates, the importance of daylength in the expression of activity patterns (Hill et al., 2004) and reproductive function (Chik et al., 1992) has been demonstrated in young adults only. It remains to investigate whether circadian rhythms responses to long-term changes in the duration of light exposure are comparable between old and younger primates.

The mouse lemur (Microcebus murinus, Primates) is a small nocturnal primate (body weight: 60–90 g) originating from Madagascar. This primate exhibits photoperiod-dependent seasonal and daily rhythms in most of its biological functions. Daily exposure to light for longer than 12 h promotes sustained behavioral activity, whereas daily exposure to light for less than 12 h reduces behavioral activity and leads to an increase in fat deposits (Perret, 1992). The life span of this species is about 8–10 years in captivity (Perret, 1997). Old animals show a decrease in amplitude of the seasonal variations in body mass, sexual hormones (Aujard and Perret, 1998), melatonin (Aujard et al., 2001) and DHEA-S (Perret and Aujard, 2005, Perret and Aujard, 2006). Moreover, a recent study demonstrated that thermoregulation differed according to photoperiod and age in this species (Aujard et al., 2006), see comments in (Van Someren, 2007). Several of these studies indicate that daily and seasonal biological rhythms are altered in old mouse lemurs in ways that are remarkably similar to what is observed in human aging (Huang et al., 2002, Cayetanot et al., 2005): a decrease in amplitude of the locomotor activity level, an increased activity during the resting diurnal phase and an increase in fragmentation. For these and other reasons, the mouse lemur can be regarded as a model of primary importance for human aging (Bons et al., 2006).

In the present study, we examined whether a prolonged exposure to an increased duration of daily light exposure would equally affect younger and older mouse lemurs with respect to their locomotor activity and body temperature rhythms. If a differential response to changes in the duration of daily light exposure exists, age-related differences in the expression of daily rhythms observed under one specific photoperiod may not surface under another photoperiod.