Food- and light-entrained circadian rhythms in rats with hypocretin-2-saporin ablations of the lateral hypothalamus

Mistlberger, Ralph E.; Antle, Michael C.; Kilduff, Thomas S.; Jones, M. D. R.

doi:10.1016/s0006-8993(03)02755-0

Cited by 46 publications

(39 citation statements)

References 27 publications

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“…In the present study, we have examined the role of orexin neurons in the adaptation to restricted feeding using orexinergic(-) mice (Mistlberger et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Orexin Neurons Function in an Efferent Pathway of a Food-Entrainable Circadian Oscillator in Eliciting Food-Anticipatory Activity and Wakefulness

Mieda¹,

Williams²,

Sinton³

et al. 2004

J. Neurosci.

191

129

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Temporal restriction of feeding can entrain circadian behavioral and physiological rhythms in mammals. Considering the critical functions of the hypothalamic orexin (hypocretin) neuropeptides in promoting wakefulness and locomotor activity, we examined the role of orexin neurons in the adaptation to restricted feeding. In orexin neuron-ablated transgenic mice, the food-entrained rhythmicity of mPer2 expression in the brain and liver, the reversal of the sleep-wake cycle, and the recovery of daily food intake were unaltered compared with wild-type littermates. In contrast, orexin neuron-ablated mice had a severe deficit in displaying the normal foodanticipatory increases in wakefulness and locomotor activity under restricted feeding. Moreover, activity of orexin neurons markedly increased during the food-anticipatory period under restricted feeding in wild-type mice. Orexin neurons thus convey an efferent signal from putative food-entrainable oscillator or oscillators to increase wakefulness and locomotor activity.

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“…In the present study, we have examined the role of orexin neurons in the adaptation to restricted feeding using orexinergic(-) mice (Mistlberger et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Orexin Neurons Function in an Efferent Pathway of a Food-Entrainable Circadian Oscillator in Eliciting Food-Anticipatory Activity and Wakefulness

Mieda¹,

Williams²,

Sinton³

et al. 2004

J. Neurosci.

191

129

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“…Some lesions or gene mutations have been identified that affect the expression of FAA, but with two exceptions (discussed below), foodentrainment has been shown to persist in at least some measures of behavior. Briefly, knockouts of a clock gene expressed in the neocortex and hippocampus (nPAS2) (27) or genetic ablation of the lateral hypothalamic peptide orexin (3,39) have been reported to attenuate FAA in mice, but FAA has already been shown to persist in rats following complete ablation of these structures (40,44,47,49). Lesions of the nucleus accumbens core (38) and the hypothalamic paraventricular nucleus attenuate or eliminate FAA in some measures of behavior (e.g., general locomotor activity) but not in others [e.g., wheel running or activity directed at a food bin (47,49)].…”

mentioning

confidence: 99%

Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats

Landry¹,

Simon²,

Webb³

et al. 2006

American Journal of Physiology-Regulatory, Integrative and Comp

165

152

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Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats. Am J Physiol Regul Integr Comp Physiol 290: R1527-R1534, 2006. First published January 19, 2006 doi:10.1152/ajpregu.00874.2005.-Circadian rhythms of behavior in rodents are regulated by a system of circadian oscillators, including a master light-entrainable pacemaker in the suprachiasmatic nucleus that mediates synchrony to the day-night cycle, and food-entrainable oscillators located elsewhere that generate rhythms of food-anticipatory activity (FAA) synchronized to daily feeding schedules. Despite progress in elucidating neural and molecular mechanisms of circadian oscillators, localization of food-entrainable oscillators driving FAA remains an enduring problem. Recent evidence suggests that the dorsomedial hypothalamic nucleus (DMH) may function as a final common output for behavioral rhythms and may be critical for the expression of FAA (Gooley JJ, Schomer A, and Saper CB. Nat Neurosci 9: 398 -407, 2006). To determine whether the reported loss of FAA by DMH lesions is specific to one behavioral measure or generalizes to other measures, rats received large radiofrequency lesions aimed at the DMH and were recorded in cages with movement sensors. Total and partial DMH ablation was associated with a significant attenuation of light-dark-entrained activity rhythms during ad libitum food access, because of a selective reduction in nocturnal activity. When food was restricted to a single 3-h daily meal in the middle of the lights-on period, all DMH and intact rats exhibited significant FAA. The rhythm of FAA persisted during a 48-h food deprivation test and reappeared during a 72-h deprivation test after ad libitum food access. The DMH is not the site of oscillators or entrainment pathways necessary for all manifestations of FAA, but may participate on the output side of this circadian function. food entrainment; food-anticipatory activity; food-entrainable oscillator CIRCADIAN RHYTHMS IN MAMMALS are generated by a system of cell-autonomous circadian oscillators distributed within the brain and in peripheral organs (32,57). A population of oscillators located in the retino-recipient hypothalamic suprachiasmatic nucleus (SCN) function as a master pacemaker critical for normal circadian organization of behavior and physiology and for entrainment of rhythms to daily light-dark (LD) cycles (34). Circadian rhythms can also be entrained by daily feeding schedules. If food access is restricted to a narrow daily temporal window (typically 2-4 h in the middle of the lights-on period), nocturnal rodents, such as rats, mice, and hamsters, become behaviorally active in anticipation of the feeding time. This daily rhythm of food-anticipatory activity (FAA) takes a few circadian cycles to emerge, exhibits gradual shifting (transients) if mealtime is shifted, persists for at least 5 days during total food deprivation, and does not emerge if the interval between mealtimes is outside of the circadian range or its har...

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“…Equally puzzling is the involvement of the orexigenic LH in food anticipation. Ablation of orexin-ergic neurons by using orexinsaporin injections in the LH did not compromise the entrainment or expression of food anticipatory activity (19). However, transgenic mice lacking the orexin gene (orexin/ataxin-3) exhibited reduced anticipatory responses to a time-restricted meal (20).…”

Section: Discussionmentioning

confidence: 99%

“…Eventually, other brain regions are recruited that collectively contribute to increases in behavioral arousal. Brain regions that are activated by VMH, and are likely involved in arousalactivating pathways, include DMH and LH, which have both been extensively studied in the context of mediating arousal in the anticipation of food (19)(20)(21)(22)(23)(24). DMH receives direct projections from SCN (25) and is likely a relay nucleus involved in mediating the arousal responses of the light-entrainable oscillator.…”

Section: Discussionmentioning

confidence: 99%

Two forces for arousal: Pitting hunger versus circadian influences and identifying neurons responsible for changes in behavioral arousal

Ribeiro

Sawa

Carren-LeSauter

et al. 2007

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

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The mechanisms underlying CNS arousal in response to homeostatic pressures are not known. In this study, we pitted two forces for CNS arousal against each other (circadian influences vs. restricted food availability) and measured the neuronal activation that occurs in a behaviorally defined group of animals that exhibited increased arousal in anticipation of feeding restricted to their normal sleeping time. The number of c-FOS؉ neurons was significantly increased only in the ventromedial nucleus of the hypothalamus (VMH) in these mice, compared with control animals whose feeding was restricted to their normal active and feeding time (P < 0.01). Because the activation of VMH neurons coincides with the earliest signs of behavioral arousal preceding a change in meal time, we infer that VMH activation is involved in the increased arousal in anticipation of food.T he activation of behavior is driven by homeostatically regulated variables, such as hunger and circadian rhythms. The problem of exactly how these two types of influences interact to modulate behavior has been stated (1) but not solved. Mechanisms for changes in CNS arousal have remained controversial.We pitted two forces for CNS arousal against each other (food availability vs. circadian influences) and searched for the first neuronal activation that occurs in animals as they began to change their activation of behavior from a circadian light-driven rhythm to one dictated by restricted food availability.The present study (i) takes into account the individual differences in food anticipatory activity and links those to neuronal activation; (ii) pits the homeostatic drive for feeding against the circadian drive to rest during the light period, thus enabling a cell-by-cell dissection of these two pathways; (iii) has a control group that is exposed to the same restricted feeding paradigm as the test group, for the same number of days, with the difference that control animals receive their daily meal during their behaviorally active period; (iv) conceptualizes the problem as one of generalized CNS arousal; and (v) examines animals' brains as close to the development of the food anticipatory activity as possible. This design was intended to identify the earliest neuronal changes, and therefore the most likely to be causing these behavioral changes. ResultsShifted animals were significantly more active in the 3-h period preceding the shifted food presentation time, compared with controls. In fact, running wheel revolutions were increased from 314 Ϯ 151 in nonshifted animals to 1,768 Ϯ 398 in shifted animals (P Ͻ 0.01) (Figs. 1 and 2 and Table 1).We examined neuronal activation, as measured by c-FOS expression, in every neuronal group that could be conceived, based on the literature (see Discussion), as mediating these changes in the timing of the activation of behavior [16 regions: medial preoptic area (MPA), ventrolateral preoptic nucleus (VLPO), medial part of the medial preoptic nucleus (MPOM), lateral hypothalamus (LH), subparaventricular zone (sPVZ), paraven...

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Food- and light-entrained circadian rhythms in rats with hypocretin-2-saporin ablations of the lateral hypothalamus

Cited by 46 publications

References 27 publications

Orexin Neurons Function in an Efferent Pathway of a Food-Entrainable Circadian Oscillator in Eliciting Food-Anticipatory Activity and Wakefulness

Orexin Neurons Function in an Efferent Pathway of a Food-Entrainable Circadian Oscillator in Eliciting Food-Anticipatory Activity and Wakefulness

Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats

Two forces for arousal: Pitting hunger versus circadian influences and identifying neurons responsible for changes in behavioral arousal

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