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

Abstract

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...

The dorsomedial hypothalamic nucleus as a putative food-entrainable circadian pacemaker

“…Rhythmic expression of mPer1 and mPer2 in the NTS͞DMV͞AP area of the brainstem under RF is consistent with a recent report showing a feeding-dependent up-regulation of c-Fos expression under RF in the NTS, DMV, and AP (27). The NTS is a relay nucleus for visceral and gustatory sensory afferents, and it has also been suggested as a site of integration for visceral autonomic and sensory responses (28).…”

Differential Effects of a Restricted Feeding Schedule on Clock-Gene Expression in the Hypothalamus of the Rat

“…In the PVN, it is noteworthy that the postprandial expression of Per2 coincides with a specific induction of c-fos mRNA and protein in the PVN Poulin & Timofeeva, 2008). This meal-induced pattern may be the response to digestive processes, as it has been observed in other relay structures providing input signals elicited by feeding to the brain (Ángeles-Castellanos et al, 2005;Mieda et al, 2006). Based on c-FOS activity, the VMH has also been proposed as the initiating structure for anticipatory activity (Ribeiro et al, 2007); in the present study, no significant changes of clock genes were observed in RFS rats.…”

“…In the brain of rats exposed to RFS, daily patterns of c-FOS expression are elicited or phase changed in hypothalamic and brain stem regions involved in mediating metabolic and arousal signals to the rest of the brain (Ángeles-Castellanos et al, , 2005Gooley et al, 2006;Meynard et al, 2005). Also, corticolimbic structures involved in hedonic and motivational processes exhibit food-entrained patterns of c-FOS expression Mendoza et al, 2005a).…”

The Food-Entrainable Oscillator: A Network of Interconnected Brain Structures Entrained by Humoral Signals?

“…In this regard, it is important to report that the DMH receives projections from the subfornical organ (Thompson & Swanson, 1998). Many brain areas are entrained by, or respond to, food availability (Ángeles-Castellanos et al, , 2005(Ángeles-Castellanos et al, , 2007Lamont et al, 2005a;Mieda et al, 2006;Poulin & Timofeeva, 2008;Verwey et al, 2007;Waddington Lamont et al, 2007;Wakamatsu et al, 2001). If brain regions responsible for behavioral expression are activated by ghrelin when it increases before mealtime during temporal food restriction, it would elicit the anticipatory behaviors observed during food entrainment.…”