Simulated shift work in rats perturbs multiscale regulation of locomotor activity

Hsieh, Wan Hsin; Escobar, Carolina; Yugay, Tatiana; Lo, Men Tzung; Pittman-Polletta, Benjamin; Salgado‐Delgado, Roberto; Scheer, Frank A.J.L.; Shea, Steven A.; Buijs, Ruud M.; Hu, Kun

doi:10.1098/rsif.2014.0318

Cited by 20 publications

(19 citation statements)

References 44 publications

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“…In contrast to our results, PER1 protein expression in the PVN is unaffected in nocturnal laboratory rats that become active during the day in response to a forced-activity paradigm that emulates the conditions of human shift workers (Salgado-Delgado et al, 2010). Although species differences may be responsible for these divergent outcomes, these observations nevertheless support the view that voluntary reversals of the phase of activity (present study) affect the brain and the circadian system in a fashion that differs from the effects of forced-activity paradigms (Karatsoreos et al, 2011, McDonald et al, 2013, Saderi et al, 2013, Hsieh et al, 2014). In agreement with this view are the results of direct comparisons of the effects on the brain of spontaneous and forced wakefulness (Castillo-Ruiz et al, 2010, Castillo-Ruiz and Nunez, 2011).…”

Section: Discussionsupporting

confidence: 81%

Plastic oscillators and fixed rhythms: Changes in the phase of clock-gene rhythms in the PVN are not reflected in the phase of the melatonin rhythm of grass rats

et al. 2015

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The same clock-genes, including Period (PER) 1 and 2, that show rhythmic expression in the suprachiasmatic nucleus (SCN) are also rhythmically expressed in other brain regions that serve as extra-SCN oscillators. Outside the hypothalamus, the phase of these extra-SCN oscillators appears to be reversed when diurnal and nocturnal mammals are compared. Based on mRNA data, PER1 protein is expected to peak in the late night in the paraventricular nucleus of the hypothalamus (PVN) of nocturnal laboratory rats, but comparable data are not available for a diurnal species. Here we use the diurnal grass rat (Arvicanthis niloticus) to describe rhythms of PER1 and 2 protein in the PVN of animals that either show the species-typical day-active profile, or that adopt a night-active profile when given access to running wheels. For day-active animals housed with or without wheels, significant rhythms of PER1 or PER2 protein expression featured peaks in the late morning; night-active animals showed patterns similar to those expected from nocturnal laboratory rats. Since the PVN is part of the circuit that controls pineal rhythms, we also measured circulating levels of melatonin during the day and night in day-active animals with and without wheels and in night-active wheel runners. All three groups showed elevated levels of melatonin at night, with higher levels during both the day and night being associated with the levels of activity displayed by each group. The differential phase of rhythms in clock-gene protein in the PVN of diurnal and nocturnal animals presents a possible mechanism for explaining species differences in the phase of autonomic rhythms controlled, in part, by the PVN. The present study suggests that the phase of the oscillator of the PVN does not determine that of the melatonin rhythm in diurnal and nocturnal species or in diurnal and nocturnal chronotypes within a species.

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Section: Discussionsupporting

confidence: 81%

Plastic oscillators and fixed rhythms: Changes in the phase of clock-gene rhythms in the PVN are not reflected in the phase of the melatonin rhythm of grass rats

et al. 2015

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“…Lesioning the SCN in animals not only abolishes circadian rhythm of motor activity but also disrupts the temporal organization of motor activity fluctuations that normally display fractal patterns—similar temporal structure and statistical properties at different time scales (Hu et al, 2007 ). Moreover, we found recently that interrupting the normal synchronization between endogenous circadian rhythms and behavioral cycles can also disrupt fractal activity patterns in animals with intact SCN, resembling the effect of the SCN lesion (Hsieh et al, 2014 ). Together these results provide strong evidence that the circadian control network plays an essential role in activity regulation at multiple time scales rather than only at a single time scale of ~24 h.…”

Section: Introductionmentioning

confidence: 76%

Interactive Effects of Dorsomedial Hypothalamic Nucleus and Time-Restricted Feeding on Fractal Motor Activity Regulation

Hsieh

Escobar

et al. 2016

Front. Physiol.

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One evolutionary adaptation in motor activity control of animals is the anticipation of food that drives foraging under natural conditions and is mimicked in laboratory with daily scheduled food availability. Food anticipation is characterized by increased activity a few hours before the feeding period. Here we report that 2-h food availability during the normal inactive phase of rats not only increases activity levels before the feeding period but also alters the temporal organization of motor activity fluctuations over a wide range of time scales from minutes up to 24 h. We demonstrate this multiscale alteration by assessing fractal patterns in motor activity fluctuations—similar fluctuation structure at different time scales—that are robust in intact animals with ad libitum food access but are disrupted under food restriction. In addition, we show that fractal activity patterns in rats with ad libitum food access are also perturbed by lesion of the dorsomedial hypothalamic (DMH)—a neural node that is involved in food anticipatory behavior. Instead of further disrupting fractal regulation, food restriction restores the disrupted fractal patterns in these animals after the DMH lesion despite the persistence of the 24-h rhythms. This compensatory effect of food restriction is more clearly pronounced in the same animals after the additional lesion of the suprachiasmatic nucleus (SCN)—the central master clock in the circadian system that generates and orchestrates circadian rhythms in behavior and physiological functions in synchrony with day-night cycles. Moreover, all observed influences of food restriction persist even when data during the food anticipatory and feeding period are excluded. These results indicate that food restriction impacts dynamics of motor activity at different time scales across the entire circadian/daily cycle, which is likely caused by the competition between the food-induced time cue and the light-entrained circadian rhythm of the SCN. The differential impacts of food restriction on fractal activity control in intact and DMH-lesioned animals suggest that the DMH plays a crucial role in integrating these different time cues to the circadian network for multiscale regulation of motor activity.

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“…Shiftwork animals showed decreased amplitude of the activity rhythm on weekend days and a differently shaped rhythm of 24-h activity on weekdays. Shiftwork animals showed different activity responses to lights on and off when compared to non-shiftworking rats (Hsieh et al, 2014 ). The observed disruption of normal activity patterns was reported as an indication for circadian disruption as similar changes have been observed in SCN lesioned animals.…”

Section: Resultsmentioning

confidence: 99%

Rodent models to study the metabolic effects of shiftwork in humans

et al. 2015

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Our current 24-h society requires an increasing number of employees to work nightshifts with millions of people worldwide working during the evening or night. Clear associations have been found between shiftwork and the risk to develop metabolic health problems, such as obesity. An increasing number of studies suggest that the underlying mechanism includes disruption of the rhythmically organized body physiology. Normally, daily 24-h rhythms in physiological processes are controlled by the central clock in the brain in close collaboration with peripheral clocks present throughout the body. Working schedules of shiftworkers greatly interfere with these normal daily rhythms by exposing the individual to contrasting inputs, i.e., at the one hand (dim)light exposure at night, nightly activity and eating and at the other hand daytime sleep and reduced light exposure. Several different animal models are being used to mimic shiftwork and study the mechanism responsible for the observed correlation between shiftwork and metabolic diseases. In this review we aim to provide an overview of the available animal studies with a focus on the four most relevant models that are being used to mimic human shiftwork: altered timing of (1) food intake, (2) activity, (3) sleep, or (4) light exposure. For all studies we scored whether and how relevant metabolic parameters, such as bodyweight, adiposity and plasma glucose were affected by the manipulation. In the discussion, we focus on differences between shiftwork models and animal species (i.e., rat and mouse). In addition, we comment on the complexity of shiftwork as an exposure and the subsequent difficulties when using animal models to investigate this condition. In view of the added value of animal models over human cohorts to study the effects and mechanisms of shiftwork, we conclude with recommendations to improve future research protocols to study the causality between shiftwork and metabolic health problems using animal models.

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Simulated shift work in rats perturbs multiscale regulation of locomotor activity

Cited by 20 publications

References 44 publications

Plastic oscillators and fixed rhythms: Changes in the phase of clock-gene rhythms in the PVN are not reflected in the phase of the melatonin rhythm of grass rats

Plastic oscillators and fixed rhythms: Changes in the phase of clock-gene rhythms in the PVN are not reflected in the phase of the melatonin rhythm of grass rats

Interactive Effects of Dorsomedial Hypothalamic Nucleus and Time-Restricted Feeding on Fractal Motor Activity Regulation

Rodent models to study the metabolic effects of shiftwork in humans

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