Abstract
Mammalian circadian rhythms are controlled by a master pacemaker located in the suprachiasmatic nuclei (SCN), which is synchronized to the environment by photic and nonphotic stimuli. One of the main functions of the SCN is to regulate peripheral oscillators to set temporal variations in the homeostatic control of physiology and metabolism. In this sense, the SCN coordinate the activity/rest and feeding/fasting rhythms setting the timing of food intake, energy expenditure, thermogenesis, and active and basal metabolism. One of the major time cues to the periphery is the nocturnal melatonin, which is synthesized and secreted by the pineal gland. Under SCN control, arylalkylamine N-acetyltransferase (AA-NAT)—the main enzyme regulating melatonin synthesis in vertebrates—is activated at night by sympathetic innervation that includes the superior cervical ganglia (SCG). Bilateral surgical removal of the superior cervical ganglia (SCGx) is considered a reliable procedure to completely prevent the nocturnal AA-NAT activation, irreversibly suppressing melatonin rhythmicity. In the present work, we studied the effects of SCGx on rat metabolic parameters and diurnal rhythms of feeding and locomotor activity. We found a significant difference between SCGx and sham-operated rats in metabolic variables such as an increased body weight/food intake ratio, increased adipose tissue, and decreased glycemia with a normal glucose tolerance. An analysis of locomotor activity and feeding rhythms showed an increased daytime (lights on) activity (including food consumption) in the SCGx group. These alterations suggest that superior cervical ganglia-related feedback mechanisms play a role in SCN-periphery phase coordination and that SCGx is a valid model without brain-invasive surgery to explore how sympathetic innervation affects daily (24 h) patterns of activity, food consumption and, ultimately, its role in metabolism homeostasis.
Highlights
The circadian system, a set of biological clocks that regulate almost all physiological and behavioral processes, has evolved to adapt the organism’s physiology to cyclic environmental changes [1,2,3,4]
Taking into account that the lack of melatonin can produce circadian alterations, and that sympathetic innervation from the superior cervical ganglia (SCG) covers diverse neuroendocrine effectors, the aim of our work was to study if SCGx can affect rat metabolism and whether this is related to an impairment of the circadian clock
To study the effect of SCGx on rat metabolism, animals were subjected to ganglionectomy or a sham procedure at the middle of week 3 (n = 9 per group)
Summary
The circadian system, a set of biological clocks that regulate almost all physiological and behavioral processes, has evolved to adapt the organism’s physiology to cyclic environmental changes [1,2,3,4]. SCGx, Metabolism, and Diurnal Rhythms peripheral clocks, entrained by the SCN via neural and humoral cues, such as rhythmically secreted hormones [6,7,8], and other SCN-independent cues like food [9]. One of the major physiological processes controlled by the SCN is metabolism, including metabolic rate and circadian rhythms of food intake [3]. Alterations of the circadian pacemaker can lead to metabolic pathologies, such as obesity or metabolic syndrome [11]. Shift work, chronic forced circadian desynchronization or mutations of clock genes can affect the pattern of food intake and lead to increased levels of circulating triglycerides, and adipose tissue masses resulting in an augmented body weight [12,13,14,15]
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