Abstract
Daily interactions between the hypothalamic circadian clock at the suprachiasmatic nucleus (SCN) and peripheral circadian oscillators regulate physiology and metabolism to set temporal variations in homeostatic regulation. Phase coherence of these circadian oscillators is achieved by the entrainment of the SCN to the environmental 24-h light:dark (LD) cycle, coupled through downstream neural, neuroendocrine, and autonomic outputs. The SCN coordinate activity and feeding rhythms, thus setting the timing of food intake, energy expenditure, thermogenesis, and active and basal metabolism. In this work, we will discuss evidences exploring the impact of different photic entrainment conditions on energy metabolism. The steady-state interaction between the LD cycle and the SCN is essential for health and wellbeing, as its chronic misalignment disrupts the circadian organization at different levels. For instance, in nocturnal rodents, non-24 h protocols (i.e., LD cycles of different durations, or chronic jet-lag simulations) might generate forced desynchronization of oscillators from the behavioral to the metabolic level. Even seemingly subtle photic manipulations, as the exposure to a “dim light” scotophase, might lead to similar alterations. The daily amount of light integrated by the clock (i.e., the photophase duration) strongly regulates energy metabolism in photoperiodic species. Removing LD cycles under either constant light or darkness, which are routine protocols in chronobiology, can also affect metabolism, and the same happens with disrupted LD cycles (like shiftwork of jetlag) and artificial light at night in humans. A profound knowledge of the photic and metabolic inputs to the clock, as well as its endocrine and autonomic outputs to peripheral oscillators driving energy metabolism, will help us to understand and alleviate circadian health alterations including cardiometabolic diseases, diabetes, and obesity.
Highlights
The 24-h transitions between light and darkness [light:dark (LD) cycles] generated by the rotation of the Earth provide a strong temporal cue for most organisms, which display daily behavioral and physiological rhythms
We demonstrated that the availability of a running wheel allowed for correct entrainment and prevented the elevated body weight gain observed in mice under the desynchronizing CJL schedule
We have covered a vast amount of evidence from laboratory rodent models and human studies of the diverse effects of lighting environments challenging biological rhythmicity on metabolism
Summary
The 24-h transitions between light and darkness [light:dark (LD) cycles] generated by the rotation of the Earth provide a strong temporal cue (i.e., the time giver, or zeitgeber) for most organisms, which display daily behavioral and physiological rhythms. Clock-gene expression analysis shows that the underlying neuronal mechanism is downstream from or parallel to the SCN, and that the behavioral phenotype is accompanied by phase adjustment of peripheral tissues In both examples, temporal niche and peripheral oscillators are phased to reduce metabolic costs: in voles, liver circadian rhythms are suppressed to deal with ultradian digestive demands; in mice, diurnality reduces energy expenditure in a spontaneously nocturnal animal, by reducing thermoregulatory costs, as observed in small burrowing mammals in natural conditions [78]. Exposure to a light pulse at circadian time 15 increases PER1-2 expression in the liver in rats, which is abolished with autonomic denervation [130] Apart from this hierarchical control, using targeted SCN Bmal deletions that preserve neural SCN output circuitry [131], or temporally dissecting the sensitive-specific SCN-photic effects [42], provide intriguing evidence suggesting that light can synchronize peripheral clocks in the kidney, liver, heart, and adrenals, through a retinohypothalamic SCN clockindependent pathway. Another type of pharmacological approach that requires further research is the application of drugs with the ability to induce or reinforce entrainment to environmental cycles and its changes
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