Increased Late Night Response to Light Controls the Circadian Pacemaker in a Nocturnal Primate

Abstract

The mammalian endogenous circadian clock, the suprachiasmatic nuclei, receives environmental inputs, namely the light-dark cycle, through photopigments located in the eye and from melanopsin-expressing retinal ganglion cells. The authors investigated the influence of light wavelength and intensity on the synchronization of the rest-activity rhythm of the gray mouse lemur, a nocturnal Malagasy primate. Animals were tested at different irradiance levels (320, 45, 13, and 6 nmol x m(-2) x s(- 1)) under several light wavelengths (from 400 to 610 nm). Several parameters including circadian period, activity, and body temperature waveforms were used to assess synchronization to a 12:12 light-dark cycle in comparison to control treatments (12:12 white light or continuous darkness). Entrainment of the circadian rest-activity cycle increased with light intensity. It was more efficient for mid wavelengths relative to shorter or longer wavelengths but not coincident with melanopsin maximal sensitivity, suggesting other photoreceptors are likely involved in lemurs' photoentrainment. The authors obtained a novel synchronization pattern characterized by a clear synchronization to lights-on only without phasing to lights-off. Changes in photo-responsiveness at dusk and dawn highlight differential responses of evening and morning oscillators in the circadian clock.

Age Affects Photoentrainment in a Nocturnal Primate

“…Of the 13 animals, we tested 6 for the 3 wavelengths, 1 for 2 wavelengths, and 6 for 1 wavelength only. As in Perret et al (2010), we used the rapid increase or decrease in activity and body temperature to delineate nocturnal activity onset and offset in all tests performed, and we extracted the following parameters: τ: mean period, length of time between consecutive activity onsets, in minutes ψ onset : mean absolute value of (time of light-offtime of activity onset), in minutes ψ offset : mean absolute value of (time of light-ontime of activity offset), in minutes Resting phase: duration of the resting phase or subjective day; length of time between activity offset and onset, in minutes Night LA: proportion of total locomotor activity (LA) performed over the dark phase, as a percentage Light-off LA: proportion of total activity performed during the first hour following activity onset, as a percentage Light-on LA: proportion of total activity performed during the last hour preceding activity offset, as a percentage Tmin: minimal body temperature, in °C Hmin: time at which the minimal body temperature was observed, counting hours from time 12 taken as the beginning of the dark phase (or the subjective night), in minutes We analyzed individual patterns by normalizing data to the period observed in free-running periods.…”

“…As in young adults (Perret et al, 2010), old adults show a synchronization increase with light intensity, stronger for dark-light than light-dark transition. Yet, we observe manifold aging effects of synchronization which depict a general loss of sensitivity to light.…”

“…This argument stems on the comparison of photoreceptor response through 2 methods: (1) we considered the absorption function of the photoreceptors, and (2) we computed the photons captured by photoreceptors when viewing the LEDs tested (spectra in Perret et al, 2010). Both methods yielded similar results as LEDs, although nonmonochromatic, and had a distinctive dominant wavelength.…”

The Biological Clock in Gray Mouse Lemur: Adaptive, Evolutionary and Aging Considerations in an Emerging Non-human Primate Model

“…(A) Actogram (double plotted) over a 30 day-period under LD and DD. (B) (Mean SEM) Tb (black curve) and LA rhythm (histograms) profiles over a 7-day period under LD and (C) under DD conditions (from Perret et al, 2010).…”

“…In some lemurs, it has been suggested that cones play a role in circadian light perception (Deegan and Jacobs, 1996; Dkhissi-Benyahya et al, 2001; Erkert et al, 2006). In the gray mouse lemur, synchronization increases with the light intensity and is better for mid-wavelengths (470–540 nm) than for short and long wavelengths (Perret et al, 2010). In most organisms, twilight transitions are the dominant environmental stimuli involved in synchronization of the circadian phase (Boulos et al, 2002).…”