Effects of vagotomy on entrainment of activity rhythms to food access

Comperatore, Carlos A.; Stephan, Friedrich K.

doi:10.1016/0031-9384(90)90076-g

Cited by 61 publications

(36 citation statements)

References 32 publications

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“…As a continuation of this study, we have now attempted to describe the role of brain stem nuclei as mediators of visceral input in a food-entrainment protocol. Previous studies have reported that visceral denervation due to subdiaphragmatic vagotomy or capsaicin administration has no effect on food entrainment (9,12,28). However, we cannot rule out that in intact animals, these structures may be playing an important role by transmitting food-entraining signals.…”

mentioning

confidence: 71%

Food entrainment modifies the c-Fos expression pattern in brain stem nuclei of rats

Ángeles-Castellanos¹,

Mendoza²,

Dı́az-Muñoz³

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

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When food is restricted to a few hours daily, animals increase their locomotor activity 2-3 h before food access, which has been termed food anticipatory activity. Food entrainment has been linked to the expression of a circadian food-entrained oscillator (FEO) and the anatomic substrate of this oscillator seems to depend on diverse neural systems and peripheral organs. Previously, we have described a differential involvement of hypothalamic nuclei in the food-entrained process. For the food entrainment pathway, the communication between the gastrointestinal system and central nervous system is essential. The visceral synaptic input to the brain stem arrives at the dorsal vagal complex and is transmitted directly from the nucleus of the solitary tract (NST) or via the parabrachial nucleus (PBN) to hypothalamic nuclei and other areas of the forebrain. The present study aims to characterize the response of brain stem structures in food entrainment. The expression of c-Fos immunoreactivity (c-Fos-IR) was used to identify neuronal activation. Present data show an increased c-Fos-IR following meal time in all brain stem nuclei studied. Food-entrained temporal patterns did not persist under fasting conditions, indicating a direct dependence on feeding-elicited signals for this activation. Because NST and PBN exhibited a different and increased response from that expected after a regular meal, we suggest that food entrainment promotes ingestive adaptations that lead to a modified activation in these brain stem nuclei, e.g., stomach distension. Neural information provided by these nuclei to the brain may provide the essential entraining signal for FEO. circadian rhythms; food-entrained oscillator; food anticipatory activity, WHEN FOOD IS RESTRICTED to a few hours daily, animals exhibit food anticipatory activity (FAA), characterized by behavioral arousal and locomotor activation 2-3 h preceding food access (27,34). Corticosterone, free fatty acids, and core temperature shift their phase, anticipating the daily meal (13,16,21). Recent findings indicate that the oscillation of clock gene expression and of neuronal activity (23) in central oscillators outside the suprachiasmatic nucleus (SCN), as well as the oscillation of clock gene expression in peripheral tissues, are entrained by feeding schedules (38,40).It is well accepted that food entrainment depends upon a circadian oscillator independent of the SCN because food entrainment is elicited in animals with bilateral lesions of the SCN (35), because it can only be elicited when food is provided in a circadian range and because FAA persists for several cycles during constant fasting conditions (34). It has been suggested that this food-entrained oscillator (FEO) may consist of a distributed and possibly redundant system built up by diverse central nervous system (CNS) structures and peripheral organs involved with the processing and regulation of ingestive behavior and energy balance (24,34). To characterize this model of FEO, we must identify which structures mediate th...

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confidence: 71%

Food entrainment modifies the c-Fos expression pattern in brain stem nuclei of rats

Ángeles-Castellanos¹,

Mendoza²,

Dı́az-Muñoz³

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Prior searches for the peripheral loci of FEOs involved adrenalectomy (14), subdiaphragmatic vagotomy (15), and capsaicin-induced vagal deafferentation (16), none of which abolish FAA. In fact, the possibility of a peripheral locus was all but dismissed after the demonstration that rhythmic expression of Period1-luciferase in esophagus, stomach, liver, and colon remained nocturnal during total food deprivation, indicating that these oscillators are not self-sustained (17).…”

mentioning

confidence: 99%

Stomach ghrelin-secreting cells as food-entrainable circadian clocks

LeSauter

Hoque

Weintraub

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

284

269

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Increases in arousal and activity in anticipation of a meal, termed “food anticipatory activity” (FAA), depend on circadian food-entrainable oscillators (FEOs), whose locations and output signals have long been sought. It is known that ghrelin is secreted in anticipation of a regularly scheduled mealtime. We show here that ghrelin administration increases locomotor activity in nondeprived animals in the absence of food. In mice lacking ghrelin receptors, FAA is significantly reduced. Impressively, the cumulative rise of activity before food presentation closely approximates a Gaussian function ( r = 0.99) for both wild-type and ghrelin receptor knockout animals, with the latter having a smaller amplitude. For both groups, once an animal begins its daily anticipatory bout, it keeps running until the usual time of food availability, indicating that ghrelin affects response threshold. Oxyntic cells coexpress ghrelin and the circadian clock proteins PER1 and PER2. The expression of PER1, PER2, and ghrelin is rhythmic in light–dark cycles and in constant darkness with ad libitum food and after 48 h of food deprivation. In behaviorally arrhythmic-clock mutant mice, unlike control animals, there is no evidence of a premeal decrease in oxyntic cell ghrelin. Rhythmic ghrelin and PER expression are synchronized to prior feeding, and not to photic schedules. We conclude that oxyntic gland cells of the stomach contain FEOs, which produce a timed ghrelin output signal that acts widely at both brain and peripheral sites. It is likely that other FEOs also produce humoral signals that modulate FAA.

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“…Attempts have been made, therefore, to isolate the brain from the peripheral inputs that would provide such information; all attempts at perturbing peripheral inputs have so far failed to demonstrate what peripheral inputs are necessary for the FEO to entrain behavior. For example, neither ablation of the vagus input coincident or non coincident with SCN ablation (Comperatore and Stephan, 1990) or induced cirrhosis of the liver (Escobar et al, 2002) abolished food-anticipatory behavior entrained by food and not light. Attempts at perturbing the FEO centrally have met with a similar lack of success; ablation of non-SCN hypothalamic structures such as the lateral hypothalamus that are closely involved in the regulation of feeding and sleep do not abolish food-anticipatory circadian rhythms (Mistlberger et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

The firing rate of hippocampal CA1 place cells is modulated with a circadian period

Munn

Bilkey

2011

Hippocampus

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The accurate recall of an event is usually dependent on a memory trace that encodes three pieces of information; what happened, when the event happened, and where. The established phenomenology of hippocampal CA1 pyramidal neurons could reflect mechanisms via which some of this information (where and what) is encoded; but so far there has been little evidence for a mechanism by which these cells might represent "when." It was therefore of interest to examine the activity of CA1 neurons over a substantial temporal duration. Forty-eight CA1 neurons were recorded once an hour during long (24-48 h) exposures to a single, stable environment where minimal time-of-day cues were available. Only data from the first 25 h of recording was analyzed quantitatively. We found that the mean ensemble firing rate of these cells changed predictably such that it was closely correlated (r = 0.707) to a reference sine wave with a 25-h period and a positive peak at recording start. This relationship was not explained by changes in the animal's running speed or amount of the recording environment covered in each recording session. When data were referenced to the onset or offset of the normal light-on period, the correlation with the sinusoid was abolished. At an individual cell level, the majority of neurons (n = 31) had significant correlations (P < 0.05) with the reference sine. We conclude that the firing rate of a large proportion of cells in area CA1 of the hippocampus are modulated over a circadian period but that this modulation is not entrained to light. Rather, entry into the environment and the associated food availability appear to be the entraining factors. We hypothesize that these neurons may be part of the putative food-entrainable oscillator. Such a system could enable an animal to discriminate between spatial representations on a temporal dimension with reference to the time of food availability.

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Effects of vagotomy on entrainment of activity rhythms to food access

Cited by 61 publications

References 32 publications

Food entrainment modifies the c-Fos expression pattern in brain stem nuclei of rats

Food entrainment modifies the c-Fos expression pattern in brain stem nuclei of rats

Stomach ghrelin-secreting cells as food-entrainable circadian clocks

The firing rate of hippocampal CA1 place cells is modulated with a circadian period

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