Stomach ghrelin-secreting cells as food-entrainable circadian clocks

LeSauter, Joseph; Hoque, Nawshin; Weintraub, Michael; Pfaff, Donald W.; Silver, Rae

doi:10.1073/pnas.0906426106

Cited by 279 publications

(280 citation statements)

References 63 publications

(60 reference statements)

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“…There is no doubt that FAA stems from activity within the brain, although the initiation of this activity may arise from peripheral oscillating or stimulating processes (38)(39)(40). All in all, the appearance of c-Fos or PERIOD immunoreactivity in many brain areas after food restriction and the failure to prevent FAA by lesioning different brain areas (13) suggests that the organization of the oscillatory nature of FAA should be within a system of interacting brain structures.…”

Section: Faa Is Lost After Lesion Of the Dmh But Reappears After Amentioning

confidence: 99%

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Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior

Acosta-Galvan

Vliet

et al. 2011

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

157

131

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Food anticipatory behavior (FAA) is induced by limiting access to food for a few hours daily. Animals anticipate this scheduled meal event even without the suprachiasmatic nucleus (SCN), the biological clock. Consequently, a food-entrained oscillator has been proposed to be responsible for meal time estimation. Recent studies suggested the dorsomedial hypothalamus (DMH) as the site for this food-entrained oscillator, which has led to considerable controversy in the literature. Herein we demonstrate by means of c-Fos immunohistochemistry that the neuronal activity of the suprachiasmatic nucleus (SCN), which signals the rest phase in nocturnal animals, is reduced when animals anticipate the scheduled food and, simultaneously, neuronal activity within the DMH increases. Using retrograde tracing and confocal analysis, we show that inhibition of SCN neuronal activity is the consequence of activation of GABA-containing neurons in the DMH that project to the SCN. Next, we show that DMH lesions result in a loss or diminution of FAA, simultaneous with increased activity in the SCN. A subsequent lesion of the SCN restored FAA. We conclude that in intact animals, FAA may only occur when the DMH inhibits the activity of the SCN, thus permitting locomotor activity. As a result, FAA originates from a neuronal network comprising an interaction between the DMH and SCN. Moreover, this study shows that the DMH-SCN interaction may serve as an intrahypothalamic system to gate activity instead of rest overriding circadian predetermined temporal patterns. P hysiology and behavior of all mammals is organized in an alternating pattern of rest and activity cycles, whereby the endogenous and light-induced daily neuronal activity of the suprachiasmatic nucleus (SCN) signals rest in nocturnal rodents and activity in diurnal primates, such as humans (1, 2). Restricting food access to a short and predictable episode during the rest phase changes this behavioral pattern, such that an animal becomes active and for up to several hours anticipates the upcoming feeding event. This food anticipatory activity (FAA) is even exhibited without the known circadian oscillator, the SCN (3), and thus may rely on a different circadian pacemaker.In search of the location of this so-called "food entrained oscillator" (FEO), two recent studies have claimed that its position is within the dorsomedial nucleus of the hypothalamus (DMH) (4, 5). The designation of the DMH as master clock for food entrainment is, however, controversial because some groups reported unimpaired FAA despite large lesions of the DMH (6, 7); others have shown that lesions of the DMH disturb and diminish the intensity of FAA (6). The possible participation of other brain structures in FAA is evident from studies that demonstrate modulation of neuronal activity and induction of clock-gene rhythmicity in hypothalamic and limbic structures by feeding schedules (8-11). Thus, it has been suggested that FAA depends on a multioscillatory system comprised of a complex and redundant neuronal netwo...

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Section: Faa Is Lost After Lesion Of the Dmh But Reappears After Amentioning

confidence: 99%

“…Thus, the arcuate nucleus seems a possible candidate within the network of structures for driving FAA (40). Other possible candidates are the nucleus accumbens, the paraventricular nucleus of the thalamus, and the cerebellum (9,42).…”

Section: Faa Is Lost After Lesion Of the Dmh But Reappears After Amentioning

confidence: 99%

Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior

Acosta-Galvan

Vliet

et al. 2011

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

157

131

View full text Add to dashboard Cite

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“…Ghrelin administration increases FAA; however, studies on rodents lacking functional ghrelin signalling are contradictory. Mice lacking ghrelin receptors are reported to have dampened FAA (LeSauter et al 2009), whilst mice lacking preproghrelin show intact FAA responses during restricted feeding (RF; Szentirmai et al 2010). Ghrelin can feed back onto the circadian clock by directly affecting clock gene expression in the SCN (Yannielli et al 2007).…”

Section: Ghrelin and Insulinmentioning

confidence: 99%

“…When food access is confined to the normal rest period, these processes can uncouple peripheral oscillators from the central clock that stays locked to the light regimen. Ghrelin is secreted in anticipation of feeding, regardless of the light-dark cycle, from gastric oxyntic gland cells which possess a functional clock (LeSauter et al 2009). Ghrelin stimulates appetite via its actions on the hypothalamic orexigenic peptides, neuropeptide Y and orexin, and on mesolimbic reward centres (Abizaid et al 2006, Toshinai et al 2006.…”

Section: Ghrelin and Insulinmentioning

confidence: 99%

Interactions between endocrine and circadian systems

Tsang¹,

Barclay

Oster

2013

Journal of Molecular Endocrinology

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In most species, endogenous circadian clocks regulate 24-h rhythms of behavior and physiology. Clock disruption has been associated with decreased cognitive performance and increased propensity to develop obesity, diabetes, and cancer. Many hormonal factors show robust diurnal secretion rhythms, some of which are involved in mediating clock output from the brain to peripheral tissues. In this review, we describe the mechanisms of clock-hormone interaction in mammals, the contribution of different tissue oscillators to hormonal regulation, and how changes in circadian timing impinge on endocrine signalling and downstream processes. We further summarize recent findings suggesting that hormonal signals may feed back on circadian regulation and how this crosstalk interferes with physiological and metabolic homeostasis.

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“…Food-anticipatory behaviors are reduced after only a few cerebral lesions, such as in the parabrachial nucleus (Davidson et al, 2000) and the core of the accumbens nucleus (Mendoza et al, 2005b). Orexinergic cues mediated by circulating ghrelin synthesized in the stomach enhance arousal related to food anticipation (Blum et al, 2009;LeSauter et al, 2009), while anorexigenic cues mediated by leptin may inhibit food anticipation (Mistlberger and Marchant, 1999).…”

Section: Introductionmentioning

confidence: 99%

The Cerebellum Harbors a Circadian Oscillator Involved in Food Anticipation

Mendoza¹,

Pévet²,

et al. 2010

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The cerebellum participates in motor coordination as well as in numerous cerebral processes, including temporal discrimination. Animals can predict daily timing of food availability, as manifested by food-anticipatory activity under restricted feeding. By studying ex vivo clock gene expression by in situ hybridization and recording in vitro Per1-luciferase bioluminescence, we report that the cerebellum contains a circadian oscillator sensitive to feeding cues (i.e., whose clock gene oscillations are shifted in response to restricted feeding). Food-anticipatory activity was markedly reduced in mice injected intracerebroventricularly with an immunotoxin that depletes Purkinje cells (i.e., OX7-saporin). Mice bearing the hotfoot mutation (i.e., Grid2 ho/ho ) have impaired cerebellar circuitry and mild ataxic phenotype. Grid2 ho/ho mice fed ad libitum showed regular behavioral rhythms and day-night variations of clock gene expression in the hypothalamus and cerebellum. When challenged with restricted feeding, however, Grid2 ho/ho mice did not show any food-anticipatory rhythms, nor timed feeding-induced changes in cerebellar clock gene expression. In hypothalamic arcuate and dorsomedial nuclei, however, shifts in Per1 expression in response to restricted feeding were similar in cerebellar mutant and wild-type mice. Furthermore, plasma corticosterone and metabolites before mealtime did not differ between cerebellar mutant and wild-type mice. Together, these data define a role for the cerebellum in the circadian timing network and indicate that the cerebellar oscillator is required for anticipation of mealtime.

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Stomach ghrelin-secreting cells as food-entrainable circadian clocks

Cited by 279 publications

References 63 publications

Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior

Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior

Interactions between endocrine and circadian systems

The Cerebellum Harbors a Circadian Oscillator Involved in Food Anticipation

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