Disassociation between Preprandial Gut Peptide Release and Food-Anticipatory Activity

Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Ross 618, Baltimore, Maryland 21205, USA.
Endocrinology (Impact Factor: 4.5). 11/2011; 153(1):132-42. DOI: 10.1210/en.2011-1464
Source: PubMed


Animals learn to anticipate a meal as evidenced by increases in premeal activity. This learned response appears to be independent of the nutrient status of an animal because food-anticipatory activity (FAA) can be seen after entrainment by a highly palatable food when rats remain ad libitum on chow. Mealtime feeding not only induces an increase in activity but also appears to entrain the secretion of various peptides prior to a meal including insulin, ghrelin, and glucagon-like peptide-1 (GLP-1). It is not clear whether these meal-anticipatory changes in peptides are causally associated with FAA. To assess whether FAA and preprandial peptide changes co-occur with meal entrainment using different diets, rats were conditioned to receive a 6-h chow meal, 6-h high-fat meal, or 2 h access of chocolate while ad libitum on chow in the middle of the light cycle. FAA was measured for 4 h prior to mealtime. Rats were then killed at 90, 60, and 30 min prior to mealtime and plasma was collected. Although the chocolate-entrained rats showed comparable FAA with the nonchocolate-entrained animals, they did not show anticipatory increases in the ghrelin or GLP-1. All entrainment conditions induced a decrease in insulin and an increase in glucose prior to mealtime. These data suggest that separate mechanisms may underlie the preprandial increases in ghrelin and GLP-1 and changes in FAA, insulin, and glucose.

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    • "One study found that plasma ghrelin levels correlated with locomotor activity counts during the 3 h prior to the chocolate snack, and that injected ghrelin increased anticipatory activity (Merkestein et al., 2012). However, another study found no increase in ghrelin prior to a daily chocolate snack (Dailey et al., 2012). "
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    ABSTRACT: Alzheimer's disease (AD) is a global epidemic. Unfortunately, we are still without effective treatments or a cure for this disease, which is having devastating consequences for patients, their families, and societies around the world. Until effective treatments are developed, promoting overall health may hold potential for delaying the onset or preventing neurodegenerative diseases such as AD. In particular, chronobiological concepts may provide a useful framework for identifying the earliest signs of age-related disease as well as inexpensive and noninvasive methods for promoting health. It is well reported that AD is associated with disrupted circadian functioning to a greater extent than normal aging. However, it is unclear if the central circadian clock (i.e., the suprachiasmatic nucleus) is dysfunctioning, or whether the synchrony between the central and peripheral clocks that control behavior and metabolic processes are becoming uncoupled. Desynchrony of rhythms can negatively affect health, increasing morbidity and mortality in both animal models and humans. If the uncoupling of rhythms is contributing to AD progression or exacerbating symptoms, then it may be possible to draw from the food-entrainment literature to identify mechanisms for re-synchronizing rhythms to improve overall health and reduce the severity of symptoms. The following review will briefly summarize the circadian system, its potential role in AD, and propose using a feeding-related neuropeptide, such as ghrelin, to synchronize uncoupled rhythms. Synchronizing rhythms may be an inexpensive way to promote healthy aging and delay the onset of neurodegenerative disease such as AD.
    Frontiers in Aging Neuroscience 09/2014; 6. DOI:10.3389/fnagi.2014.00234 · 4.00 Impact Factor
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    • "The absence of relative negative energy balance, in advance of the initiation of the binge, in either species, is in line with our previous findings (Bake et al., 2013) where there was no evidence of potentially causative perturbation in expression of hypothalamic homeostatic neuropeptide genes prior to consumption of large binge-type meals. Similarly , analysis of the gut hormones, ghrelin and glucagon-like peptide-1 indicated that these hormones were not involved in the anticipation of large palatable meals in rats (Bake et al., 2014), whereas they have been implicated in the anticipation of daily meals on restricted feeding schedules (Dailey et al., 2012; Drazen, Vahl, D'Alessio, Seeley, & Woods, 2006; Merkestein et al., 2012; Vahl, Drazen, Seeley, D'Alessio, & Woods, 2010). Two key findings of the current study were the continuing presence of FAA and sustained increase in meal frequency during the replacement phase, when only stock diet was available and the immediate hyperphagic response once HFD was restored after 7 days. "
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    ABSTRACT: Male C57BL/6 mice fed ad libitum on control diet but allowed access to a palatable high fat diet (HFD) for 2 h a day during the mid-dark phase rapidly adapt their feeding behaviour and can consume nearly 80% of their daily caloric intake during this 2 h-scheduled feed. To further develop this model, we examined its behavioural characteristics, assessing food intake microstructure and meal pattern, and locomotor activity and rearing as markers of food anticipatory activity (FAA). Analysis of food intake microstructure showed that schedule-fed mice reduced their caloric intake from control diet during the first hours of the dark phase but not during the 3-h period immediately preceding the scheduled feed. Meal analysis showed that large meal/binge-like eating behaviour during the 2-h scheduled feed was characterised by increases in both meal number and meal size. Rearing was increased during the 2-h period running up to scheduled feeding while locomotor activity started to increase 1 h before, indicating that schedule-fed mice display FAA. Behavioural characteristics such as meal number and physical activity were sustained when HFD was withheld during the anticipated scheduled feeding period, and mice immediately binged when HFD was represented after a week of this "withdrawal" period. These findings provide important context to the binge-eating model and to our previous studies suggesting that energy balance systems in the hypothalamus are not responsible for driving these large, binge-type meals. Evidence of FAA in HFD dark phase schedule-fed mice implicates anticipatory processes in binge eating that do not involve immediately preceding hypophagia or regulatory homeostatic signalling.
    Appetite 03/2014; 77(100). DOI:10.1016/j.appet.2014.02.020 · 2.69 Impact Factor
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    • "In a second study, rats anticipating a 6-h daily meal beginning 3-h after lights-on also exhibited increased GLP-1 at 90 and 60 min before mealtime, and no difference at 30 min prior to the meal, by comparison with adlib fed rats. By contrast, a group of rats anticipating 2-h access to chocolate, without caloric restriction, showed no change in GLP-1 at 90, 60, or 30 min time points before feeding (Dailey et al., 2012). These results indicate that a premeal peak of GLP-1 is not necessary for anticipation of a daily palatable meal in the absence of caloric restriction. "
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    ABSTRACT: Circadian rhythms of behavior and physiology are generated by central and peripheral circadian oscillators entrained by periodic environmental or physiological stimuli. A master circadian pacemaker in the hypothalamic suprachiasmatic nucleus (SCN) is directly entrained by daily light-dark (LD) cycles, and coordinates the timing of other oscillators by direct and indirect neural, hormonal and behavioral outputs. The daily rhythm of food intake provides stimuli that entrain most peripheral and central oscillators, some of which can drive a daily rhythm of food anticipatory activity if food is restricted to one daily mealtime. The location of food-entrainable oscillators (FEOs) that drive food anticipatory rhythms, and the food-related stimuli that entrain these oscillators, remain to be clarified. Here, we critically examine the role of peripheral metabolic hormones as potential internal entrainment stimuli or outputs for FEOs controlling food anticipatory rhythms in rats and mice. Hormones for which data are available include corticosterone, ghrelin, leptin, insulin, glucagon, and glucagon-like peptide 1. All of these hormones exhibit daily rhythms of synthesis and secretion that are synchronized by meal timing. There is some evidence that ghrelin and leptin modulate the expression of food anticipatory rhythms, but none of the hormones examined so far are necessary for entrainment. Ghrelin and leptin likely modulate food-entrained rhythms by actions in hypothalamic circuits utilizing melanocortin and orexin signaling, although again food-entrained behavioral rhythms can persist in lesion and gene knockout models in which these systems are disabled. Actions of these hormones on circadian oscillators in central reward circuits remain to be evaluated. Food-entrained activity rhythms are likely mediated by a distributed system of circadian oscillators sensitive to multiple feeding related inputs. Metabolic hormones appear to play a modulatory role within this system.
    Frontiers in Neuroscience 10/2013; 7(7):185. DOI:10.3389/fnins.2013.00185 · 3.66 Impact Factor
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