Abstract
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.
Highlights
One of the most important external stimuli that influence locomotor activity control is food availability
Food restriction induced foodanticipatory activity (FAA), as characterized by significantly increased activity levels starting 3 h before the feeding period as well as the mean activity level during the entire light phase (80 ± 3% of daily mean; p < 0.0001; Figure 1D)
Previous studies have exclusively focused on the change of mean activity levels 1–3 h before the feeding period in each 24h activity cycle
Summary
One of the most important external stimuli that influence locomotor activity control is food availability. FAA is believed to be controlled by an intrinsic food entrained oscillator or oscillatory network with a circadian period close to 24 h (Escobar et al, 2009). This is evident from the fact that FAA occurs only when the cycle of restricted food availability is close to 24 h or harmonics of 24 h such as 12 h (Mistlberger et al, 2012; Patton et al, 2014), e.g., FAA is absent when the cycle period is
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