Physiological and cognitive consequences of a daily 26 h photoperiod in a primate:exploring the underlying mechanisms of the circadian resonance theory

Abstract

The biological clock expresses circadian rhythms, whose endogenous period (tau) is close to 24 h. Daily resetting of the circadian clock to the 24 h natural photoperiod might induce marginal costs that would accumulate over time and forward affect fitness. It was proposed as the circadian resonance theory. For the first time, we aimed to evaluate these physiological and cognitive costs that would partially explain the mechanisms of the circadian resonance hypothesis. We evaluated the potential costs of imposing a 26 h photoperiodic regimen compared to the classical 24 h entrainment measuring several physiological and cognitive parameters (body temperature, energetic expenditure, oxidative stress, cognitive performances) in males of a non-human primate ( Microcebus murinus ), a nocturnal species whose endogenous period is about 23.5 h. We found significant higher resting body temperature and energy expenditure and lower cognitive performances when the photoperiodic cycle length was 26 h. Together these results suggest that a great deviation of external cycles from tau leads to daily greater energetic expenditure, and lower cognitive capacities. To our knowledge, this study is the first to highlight potential mechanisms of circadian resonance theory.

Survival is reduced when endogenous period deviates from 24 h in a non-human primate, supporting the circadian resonance theory

“…Pittendrigh and Minis suggested that the daily resetting of the biological clock onto the 24 h of the environment would engender daily marginal metabolic costs that would accelerate aging and affect survival: the impact of these costs on longevity would be proportional to the deviation of tau from 24 h. In that respect, the median survival ages found in our experiment show clearly that the more tau gets far from 24 h, the more the survival is low. Recently, we observed that mouse lemurs kept in light–dark cycles far from their endogenous period (26 h) exhibited higher resting body temperature and higher energy expenditure, associated with lower cognitive performances 27 . This study suggests that living under photoperiodic regimen far from endogenous rhythms leads to physiological, metabolic and cognitive costs for the organism.…”

“…Recently, we reported that mouse lemurs raised under light–dark cycles of 26 h exhibited higher daily body temperature and metabolic rate than animals kept in natural lighting conditions (24 h), demonstrating the existence of potential metabolic and physiological costs of clock synchronization when endogenous and external rhythms deviate 27 . Do these costs affect the survival of adult individuals?…”

Cognitive performance of grey mouse lemurs (Microcebus murinus) during a discrimination learning task: Effect of the emotional valence of stimuli

“…To assess to what extent emotion may interfere with the cognitive abilities of mouse lemurs, we used a visual discrimination learning task. This task has been used in various cognitive studies on mouse lemurs (Gary et al, 2019;Hozer & Pifferi, 2020;Picq et al, 2015;Royo et al, 2018). In this task, individuals learn to discriminate between two platforms, with only one providing access to their nest (hereafter, the target platform).…”

Learning performance of grey mouse lemurs (Microcebus murinus) during a visual discrimination task: effect of the stimuli’s emotional value

“…Visual stimulus can be used since vision has been identi ed as a key modality for prey detection in captive born mouse lemurs (Piep et al, 2008). The visual discrimination task has already been used as a classic cognitive task (with emotionally neutral stimuli) in various cognitive studies on mouse lemurs (Gary et al, 2019;Hozer & Pifferi, 2020;Picq et al, 2015;Royo et al, 2018). This task has several advantages such as a fast habituation time and understanding of the apparatus, a possibility to easily manipulate the stimuli and to repeat the learning endlessly, provided stimuli are changed.…”