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Departamentos de 1 Neurociencias y 2 Biofísica, Instituto de Fisiología Celular, Universidad National Autónoma de México, Mexico City 04510, Mexico
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The presence of a food-entrainable oscillator (FEO) independent from the SCN is now well established, but until now its location and characterization have been elusive. Because its expression requires priming of the animal's metabolism toward a catabolic state, it is possible that metabolic rhythms may be related to FEO. The present study was designed to determine whether metabolic rhythms persist during fasting and whether such rhythms could be entrained to a restricted feeding schedule. The results indicate persistent rhythms of triacylglycerides, free fatty acids, glucose, and proteins during fasting, whereas ketone bodies and liver glycogen changed their concentration as a function of fasting. Daily food pulses of 2 h entrained the rhythms of triacylglycerides and free fatty acids and restored ketone bodies and liver glycogen to similar levels as controls. Neither glucose nor proteins were affected by the food pulse. These results indicate the relevance of lipid metabolism as a phenomenon associated with the FEO.
food-entrainable oscillator; meal feeding; circadian rhythms; food-anticipatory activity
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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ALTHOUGH THE SUPRACHIASMATIC NUCLEI (SCN) are recognized as the major circadian oscillators entrainable by the light-dark cycle in mammals, the finding of food-anticipatory activity and the splitting of locomotor rhythms under constant bright light strongly suggest that circadian rhythms are regulated by a multioscillatory system (27). Anticipatory activity (AA) occurs when food access is restricted to a few hours in a 24-h cycle for a number of consecutive days. Animals exposed to such a feeding schedule increase their locomotion in anticipation of food availability, even when food is presented during the resting period of the animal (4). Associated with this behavioral pattern, similar changes occur in the circadian phase of several physiological rhythms such as plasma corticosteroids and temperature, which shift their acrophase to hours preceding food presentation (13).
Although processes of associative learning may underlie AA, the range of entrainment within the circadian periodicity, the presence of transients to adjust to phase shifts of feeding schedules, and the reappearance of a component of activity under fasting conditions at the same phase as AA support the hypothesis of a circadian timing system underlying this phenomenon (16, 29). Such a system is independent of the light-entrainable oscillator, because ablation of the SCN does not prevent the expression of AA (32) or entrainment of corticosteroid rhythms to food pulses (13), indicating the presence of a food-entrainable oscillator (FEO). The anatomic substrate of this system has been intensively explored, but until now its location and characterization have been elusive (16).
Previous studies suggest that animals require priming of their metabolism toward a catabolic state to develop AA, because in hamsters, food consumption has to be restricted to 70% of the basal values to induce AA (1). This assumption is not clear, however, because Stephan and Becker (31) reported entrainment to restricted feeding schedules allowing up to 12 h of food access. On the other hand, free running of AA can only be observed under fasting conditions (32). Diet characteristics such as nutritional contents and amount of food also seem to play an important role for the development of AA (10, 18). Altogether, previous observations suggest that metabolic signals may trigger behavioral and physiological responses to feeding schedules.
The plasma concentration of metabolic and hormonal products involved with energy balance varies with a well-established dynamic, depending on whether the organism is well fed, fasted, or starving (14). Such changes have been associated with the behavioral cycle of satiation and hunger (21, 28). In addition, several of those metabolic and hormonal parameters show circadian or diurnal fluctuations (7, 12). However, the studies mentioned above have not addressed the contribution of those parameters to a time-measuring system, specifically their role in the generation of AA. The close relation of the metabolic state with the entrainment to feeding schedules suggests that the FEO may be regulating the metabolic signals associated with energy balance or even may rely on those signals as part of its mechanism.
To further understand the nature of the FEO, we addressed whether metabolic rhythms depend on an endogenous oscillator related to feeding, rather than being a consequence of daily cycles of feeding and fasting. If the former is the case, rhythmicity of energy metabolites 1) should persist during fasting and is likely to change its phase relation to the light-dark cycle and 2) should be entrained to a restricted feeding schedule. The present study was designed to test the previous hypotheses.
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MATERIAL AND METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Animals and Housing
Adult male Wistar rats weighing 215-225 g at the beginning of the experiment were maintained in a 12:12-h light-dark cycle (LD, lights on at 0800) and constant temperature (22 ± 1°C). The light intensity at the surface of the cages was ~100 lx. Rats were kept in groups of six in transparent acrylic cages (40 × 50 × 20 cm), with free access to Purina Chow and water unless otherwise stated. Rats were acclimated to environmental conditions for at least 3 wk before the start of the experimental procedures.Blood and Liver Sampling
Rats were decapitated, and trunk blood (3-4 ml) was collected in 10-ml test tubes containing a "clot-forming gel" (Vacutainer), which were centrifuged at 2,500 rpm for 15 min to obtain blood serum. Aliquots of 700 µl were coded and frozen at
70°C for
subsequent determination of the concentration of free fatty acids,
glucose, triacylglycerides, and proteins. An additional 500 µl of
trunk blood were collected in test tubes containing 2 ml of 6%
perchloric acid to denature blood enzymes. The acid extract was
centrifuged at 10,000 rpm at 4°C for 10 min, and the
supernatant was stored in aliquots of 1 ml, coded, and frozen at
70°C for subsequent determination of ketone bodies
(aceto-acetate and 
-hydroxybutyrate). Immediately after
decapitation, the main lobule of the liver was removed, placed in small
Petri dishes, coded, and frozen (70°C) for determination of
glycogen concentration.
Serum Determinations
Serum aliquots were thawed and processed by spectrophotometric methods as follows: free fatty acids were extracted from a 200-µl sample and incubated in the presence of Co(NO3)2 and
-nitroso--naphthol following the method reported
by Novák (22), and absorbance was determined at 500 nm. Glucose
was estimated from a 100-µl sample using a commercial colorimetric
kit (no. 635; Sigma, St. Louis, MO), which is based in the reaction
between glucose and o-toluidine reagent at boiling
water temperature and measured at 635 nm. Proteins were determined as a
colored complex in a 5-µl sample with cupric salts following the
method of Biuret (8) and determined at 560 nm. Triacylglycerides were
assessed with a commercial diagnostic kit (no. 339, Sigma) by
quantifying a quinoneimine dye (at 540 nm), which is proportional to
the glycerol produced by enzymatic hydrolysis of a 10-µl serum
sample.
Determinations in Acid Extracts
Ketone bodies (aceto-acetate and-hydroxybutyrate) were estimated
with an enzymatic procedure based on reduction or oxidation of -NAD
and -NADH respectively, in 400-µl samples in the presence of
-hydroxybutyrate dehydrogenase according to the method of Mellanby
and Williamson (15). Changes in optical density were measured at 340 nm.
Determination of Liver Glycogen
Liver glycogen was determined from a 1-g sample of liver tissue according to the method of Hassid and Abraham (9). This technique is based in the hydrolysis of glycogen in alkaline conditions. Glucose was then quantified with the method of o-toluidine as previously described.Experimental Design
Experiment 1. The first experiment was intended to determine whether serum and liver metabolites show diurnal oscillations, whether these persist during fasting conditions, and in such a case whether they maintain their phase relation to the LD cycle. Two randomized groups of rats were studied: control animals always had free access to food, whereas fasted animals were deprived of food starting at 2100 but had free access to water. Four rats from the control group were decapitated every 3 h, as described, to complete a 24-h cycle. Eight fasted rats were killed every 3 h starting at 0900 (12 h after the beginning of the fasting condition) to obtain data for 96 h of fasting.Experiment 2. Experiment 2 was intended to determine whether metabolic parameters could be entrained to restricted feeding schedules. Rats were randomly assigned to one of two groups: control rats with an ad libitum feeding schedule and rats exposed to a daily restricted feeding schedule for 3 wk. In this latter group, rats had free access to water but access to food was restricted to 2 h daily from 1200 to 1400. On the 21st day of exposure to this feeding schedule, rats from both groups were decapitated at 0900, 1000, 1100, 1200, 1400, and 1800 (n = 6 for each time point).
Statistical analysis. In
expt
1 the temporal profile of metabolic
concentration for each parameter was obtained with the mean values and
SE for control and fasting conditions. Circadian rhythmicity was
estimated by visual inspection, autocorrelation, and cosinor analysis.
For these analyses, each metabolite temporal profile during fasting
conditions was smoothed with a third-order moving-average procedure,
which provided a low-pass filtered time series (23). For
autocorrelation, smoothed time series were normalized according to
x't = xt 
/
2,
where x't
is the variation coefficient around the mean (ranging from 1 to
1), xt is
the value for each time point, and
and
2 are the mean value and the
variance of the time series. Each normalized series was then analyzed
by delaying the series with respect to itself in one-sample steps (3-h
lag) to estimate the autocorrelation function (MatLab 4.0 for Windows,
The MathWorks). The statistical significance for each point of the
autocorrelation function was estimated according to Dutilleul (6) with
the -level set at P < 0.05. In
addition, smoothed data were analyzed with single-cosinor analysis,
which also allows the analysis of a time series of independent data
(20). Only the last 72 h of fasting data were analyzed with
single-cosinor analysis to have 3 complete cycles and to avoid the
immediate homeostatic response. The significant periods obtained from
the autocorrelation analysis were used to select the period of the
hypothesis tested by cosinor analysis (24 and 36 h). The -level for
rejecting the null hypothesis of amplitude and sinusoidal fitting was
set at P < 0.01. This provided two
independent methods of rhythm detection. In
expt 2, groups were compared with a two-way
analysis of variance (feeding condition × time), followed by a
Tukey multiple-comparisons post hoc test with set at
P < 0.05.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Experiment 1
Most metabolites exhibited clear diurnal rhythmicity during control conditions characterized by peak values during LD transitions: at 0600 for glucose and triacylglycerides, at 0900 for glycogen and free fatty acids, and at 2100 for ketone bodies. Protein values remained constant throughout the 24-h cycle (Figs 1 and 2).
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Visual inspection of temporal profiles from fasted animals indicated dramatic changes in the concentration of certain metabolites, such as liver glycogen, which was depleted after 12 h of food deprivation, and ketone bodies, which increased up to 10-fold as fasting progressed. Other metabolites were less affected; triacylglycerides decreased by 50% and free fatty acids increased by 50% compared with control values (Fig. 1), whereas glucose and proteins were maintained very close to their control values (with maximal decrease of 10%).
Rhythmic patterns during fasting conditions were found by visual inspection in all serum metabolites, both in circadian and ultradian ranges. A robust circadian rhythmicity throughout fasting was found only in triacylglycerides. Glucose exhibited clear rhythmicity with a longer period. Circadian rhythmicity in free fatty acids was not apparent during the first 48 h of fasting, but became evident during the last two cycles. A similar trend was observed in proteins but with an apparent longer periodicity. Ketone bodies exhibited only ultradian fluctuations, with periods ranging from 9 to 12 h. With respect to the LD cycle, during fasting rhythmic metabolites did not maintain the same phase relation as in control conditions. Triacylglycerides showed a peak at 0900, 3 h later than expected from control values; glucose peak values were found later on every cycle in relation to its long period; when free fatty acids rhythmicity was evident, the peak values were observed at different times in successive cycles.
Autocorrelation analysis confirmed the circadian rhythmicity of free fatty acids and triacylglycerides, with periods close to 24 h (Fig. 3, top). Glucose and proteins showed significant rhythmicity with a period close to 33 h, and ketone bodies did not exhibit significant rhythmic components. Similar results were obtained with cosinor analysis (Table 1) for free fatty acids, triacylglycerides, and ketone bodies; however, glucose and proteins were best fitted to a 36-h period.
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Experiment 2
Exposure to a restricted feeding schedule for 3 wk induced significant changes in the serum concentration of free fatty acids, ketone bodies, and triacylglycerides associated to the food pulse (Fig. 4, left). No significant differences between experimental and control conditions were found in the rest of metabolites under study (Fig. 5, left). The results from the two-way ANOVA are shown in Table 2. Changes associated with the feeding condition were found only in free fatty acids and ketone bodies. In addition to these parameters, glycogen and triacylglycerides also exhibited changes associated with the time factor. Interactions between food availability and time were found in free fatty acids, ketone bodies, and triacylglycerides. A post hoc test indicated that in animals exposed to the food pulse, triacylglycerides decreased to 50% of control values (Fig. 4, right) 2 h before food availability and increased almost 50% from control values immediately after feeding. Free fatty acids and ketone bodies increased up to 100 and 400% of control values, respectively, 1 h before and at the time of food availability, and returned to control values after feeding. Glycogen was almost depleted 1 h before the food pulse and was restored to control values after feeding (Fig. 5, right).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Experiment 1 indicates that in ad libitum feeding and under an LD cycle, rats exhibit diurnal rhythms in serum and liver concentration of the studied metabolites. These results confirm previous reports of diurnal rhythmicity in serum concentration of glucose (12), free fatty acids (33), and triacylglycerides (7).
Changes in the concentration of the studied metabolites induced by fasting reflect two different regulatory processes, one homeostatic and one circadian. The first is aimed at maintaining energy balance and is manifested as preservation of glucose levels by means of glycogen hydrolysis and generation of alternative cellular fuels such as free fatty acids and ketone bodies (34). The second process is manifested by the persistence of temporal fluctuations in triacylglycerides, free fatty acids, glucose, and proteins. Present data confirm previous reports of diurnal rhythmicity in 12- to 24-h fasted animals for free fatty acids, triacylglycerides (19), and glucose (24).
Autocorrelation and cosinor analyses demonstrated changes in period length for glucose and proteins during fasting (Fig. 3 and Table 1). In contrast, triacylglycerides and free fatty acids showed persistent rhythmicity with a period of 24 h, but with a different phase relation to the LD cycle according to visual inspection of the data. The persistence of two different periods during fasting (24 h and >30 h) supports the hypothesis of at least two different oscillators expressing simultaneously, each of them controlling one set of metabolic parameters. One of these oscillators may be the SCN, because it has been shown that it is necessary for generation of diurnal rhythms of some plasma metabolites (35). Alternatively, rhythmic expression of metabolic parameters may be under simultaneous control of several interacting oscillators, with different hierarchy depending on the state of the organism. Changes observed in metabolic parameters during fasting may be related to a change in the interaction between the SCN and other oscillator(s) induced by the new metabolic state. This hypothesis is supported by recent observations describing phase shifts in locomotor activity and temperature rhythmicity induced by fasting (3). On the other hand, 33- to 36-h metabolic fluctuations observed during fasting can also be the result of oscillating homeostatic processes oriented to maintain energy supply during prolonged food deprivation, or even may be related to the interaction between the SCN and such homeostatic processes, as previously suggested for the regulation of the sleep-wake cycle (5). Present data, however, cannot lead to concluding information on the identity of oscillators driving these metabolic rhythms. Further studies are needed to characterize the dependence of metabolic rhythms to the SCN, to other circadian oscillators, or to homeostatic processes.
Experiment 2 indicates that daily food pulses of 2 h affect mainly the temporal pattern of lipid metabolites, which is characterized by a reduction of triacylglycerides 2 h before feeding, followed by increased levels of free fatty acids and ketone bodies 1 h later. Triacylglycerides rose significantly over control values after feeding, while other parameters returned to control levels. Liver glycogen exhibited an important depletion preceding the increase of free fatty acids and ketone bodies. Previous observations may be regarded either as the consequence of entrainment of an endogenous feeding-related oscillator or as the resetting of monotonic processes associated with the 22 h of fasting involved with the restricted feeding paradigm. The persistence of oscillations observed during fasting in expt 1 suggests that triacylglycerides and free fatty acids are driven by an oscillator, and therefore the effect of food pulses on those parameters may be interpreted as an entrainment process. In contrast, changes observed in ketone bodies and liver glycogen are better explained as a resetting process, because both of them responded monotonically to fasting in expt 1. This interpretation is further supported by a previous study by Suzuki et al. (33), where similar effects of food restriction were observed in liver glycogen but no differences with respect to control animals were found for free fatty acids. Because in Suzuki's study food was provided during the first 2 h of the night, which is the usual feeding time for the rat, oscillation of free fatty acids did not involve a change in phase. In contrast, glycogen was depleted before feeding time and restored to control levels after feeding, as in the present study, which supports the hypothesis that changes in glycogen concentration reflect the depletion of an energy deposit regulated by homeostatic processes.
The relevance of metabolic signals with the expression of FEO has been suggested in many studies concerning entrainment by feeding schedules. A recent study has shown that nutritional and caloric contents rather than the amount of food play an important role for the development of AA (30). Furthermore, AA is abolished by ventromedial hypothalamus (VMH) lesions, which induce accelerated increase in body weight (dynamic phase), but can be induced again during the static phase, when body weight is stabilized (11, 17). The expression of AA is also attenuated in animals rendered obese by access to a palatable high-fat diet, but it is enhanced when animals lose weight by returning them to a regular chow diet (25). Altogether, such observations and present data indicate a possible relation between the lipid metabolism associated to the catabolic state induced by food restriction and the expression of the FEO.
In conclusion, the results provide evidence of metabolic variables that show persistence of rhythmicity during 96 h of fasting and are entrained by a restricted feeding schedule. Furthermore, the relevance of lipid metabolism as a phenomenon associated to FEO is now evident. It remains to be established whether rhythmicity in lipid metabolism is driven by FEO or whether this oscillator is a distributed system that involves the regulatory mechanisms of lipid metabolism as part of the oscillatory mechanism itself. Further studies are needed to directly address this issue.
Perspectives
It is clear that regulation of food intake and related behaviors involves the synchronic operation of processes occurring at different levels of organization (2). Systemic energy demands, endocrine responses, and the resulting metabolic events are transduced into central and peripheral neuronal activity, which in turn lead to specific behavioral and peripheral physiological processes aimed to the regulation of energy balance. In such context, the present study describes the temporal variations in plasma metabolites in ad libitum-fed, fasted, and food-restricted animals, which reflect the response of the energetic demands of the organism to changing environmental conditions. It remains to be established how these phenomena are transduced into neural and endocrine activity and then into the AA and peripheral physiological responses. Several brain areas are involved with the regulation of food intake and the mobilization of endogenous fuels. Glucoreceptors have been found in the ventromedial and lateral hypothalamus, the nucleus of the solitary tract, the dorsomotor vagal nucleus, and the area postrema (26). It has been suggested that free fatty acids and amino acids are also monitored by the nervous system (21). However, there is only indirect evidence on the presence of free fatty acid receptors in VMH neurons, and most studies indicate that fat monitoring occurs throughout the insulin dependence of glucosensitve neurons in the VMH (14). Energy balance is further controlled by those same brain areas through the endocrine and autonomic system (vagus and sympathetic fibers). Changes in plasma metabolites as described in this study may constitute not only the response of the organism to its energy demands but also the signal to the brain to be further transmitted to other cerebral areas and activate the animal to search for food, inducing anticipatory behaviors, thus constituting a feedback loop between peripheral and brain processes.| |
ACKNOWLEDGEMENTS |
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The authors thank Dr. Victoria Chagoya and Dr. Rolando Hernández, Instituto de Fisiología Celular, Universidad National Autónoma de México, for technical advice and provision of reactants.
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FOOTNOTES |
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This work was supported by Grants IN206697 from Direccion General de Asuntos de Personal Académico and LN0024-N9607 from Consejo Nacional de Ciencia y Tecnología.
Address for reprint requests: R. Aguilar-Roblero, Depto. de Neurociencias, IFC, UNAM, Apdo. Postal 70-253, Mexico City 04510, Mexico.
Received 31 July 1997; accepted in final form 12 January 1998.
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REFERENCES |
|---|
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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1.
Abe, H.,
and
B. Rusak.
Anticipatory activity and entrainment of circadian rhythms in Syrian hamsters exposed to restricted palatable diets.
Am. J. Physiol.
263 (Regulatory Integrative Comp. Physiol. 32):
R116-R124,
1992
2.
Blundell, J.
Pharmacological approaches to appetite suppression.
Trends Pharmacol. Sci.
12:
149-157,
1991.
3.
Challet, E.,
P. Pévet,
and
A. Malan.
Effect of prolonged fasting and subsequent refeeding on free-running rhythms of temperature and locomotor activity in rats.
Behav. Brain Res.
84:
275-284,
1997[Medline].
4.
Coleman, G. J.,
S. Harper,
J. D. Clarke,
and
S. Armstrong.
Evidence for a separate meal associated oscillator in the rat.
Physiol. Behav.
29:
107-115,
1982[Medline].
5.
Daan, S.,
D. G. M. Beersma,
and
A. A. Borbély.
Timing of human sleep: recovery process gated by a circadian pacemaker.
Am. J. Physiol.
246 (Regulatory Integrative Comp. Physiol. 15):
R161-R178,
1984
6.
Dutilleul, P.
Rhythms and autocorrelation analysis.
Biol. Rhythm Res.
26:
173-193,
1995.
7.
Fukagawa, K.,
H. M. Gou,
R. Wolf,
and
P. Tso.
Circadian rhythm of serum and lymph apolipoprotein AIV in ad libitum-fed and fasted rats.
Am. J. Physiol.
267 (Regulatory Integrative Comp. Physiol. 36):
R1385-R1390,
1994
8.
Gornall, A. G.,
C. J. Bradwill,
and
M. M. David.
Determination of serum proteins by means of the Biuret Reaction.
J. Biol. Chem.
177:
751-766,
1949
9.
Hassid, W. Z.,
and
S. Abraham.
Chemical procedures for analysis of polysaccharides.
In: Methods in Enzymology, edited by S. P. Colowick,
and C. Kaplan. New York: Academic, 1957, vol. III, p. 34-50.
10.
Honma, K. I.,
S. Honma,
and
T. Hiroshige.
Critical role of food amount for prefeeding corticosterone peak in rats.
Am. J. Physiol.
244 (Regulatory Integrative Comp. Physiol. 13):
R339-R344,
1983.
11.
Honma, S.,
K. I. Honma,
T. Nagasaka,
and
T. Hiroshige.
The ventromedial hypothalamic nucleus is not essential for the prefeeding corticosterone peak in rats under restricted daily feeding.
Physiol. Behav.
39:
211-215,
1987[Medline].
12.
Kaminsky, Y. G.,
and
E. A. Kosenko.
Diurnal rhythms in liver carbohydrate metabolism, comparative aspects and critical review.
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
86:
763-784,
1987.
13.
Krieger, D. T.
Regulation of circadian periodicity of plasma corticosteroid concentrations and of body temperature by time of food presentation.
In: Biological Rhythms and Their Central Mechanism, edited by M. Suda,
O. Hayaishi,
and H. Nakagawa. Amsterdam: Elsevier, 1979, p. 247-259.
14.
Le Magnen, J.
Neurobiology of Feeding and Nutrition. San Diego, CA: Academic, 1992, p. 291-329.
15.
Mellanby, J.,
and
D. H. Williamson.
Acetoacetate and D-()--hydroxybutyrate.
In: Methods of Enzymatic Analysis, edited by H. Bergmeyer. New York: Academic, 1965, p. 454-461.
16.
Mistlberger, R. E.
Circadian food-anticipatory activity: formal models and physiological mechanisms.
Neurosci. Biobehav. Rev.
18:
171-195,
1994[Medline].
17.
Mistlberger, R. E.,
and
A. Rechtschaffen.
Recovery of anticipatory activity to restricted feeding in rats with ventromedial hypothalamic lesions.
Physiol. Behav.
33:
227-235,
1984[Medline].
18.
Mistlberger, R.,
and
B. Rusak.
Palatable daily meals entrain anticipatory activity rhythms in free-feeding rats: dependence on meal size and nutrient content.
Physiol. Behav.
41:
219-226,
1987[Medline].
19.
Mondola, P.,
P. Gambardella,
F. Santangelo,
M. R. Santillo,
and
A. M. Greco.
Circadian rhythms of lipid and apolipoprotein pattern in adult fasted rats.
Physiol. Behav.
58:
175-180,
1995[Medline].
20.
Nelson, W.,
Y. L. Tong,
J. K. Lee,
and
F. Halberg.
Methods for cosinor rhythmometry.
Chronobiologia
6:
305-323,
1979[Medline].
21.
Nicolaïdis, S.
What determines food intake? The ischymetric theory.
News Physiol. Sci.
2:
104-107,
1987.
22.
Novák, M.
Colorimetric ultramicro method for the determination of free fatty acids.
J. Lipid Res.
6:
431-433,
1965[Abstract].
23.
Oppenheim, A. V.,
I. T. Young,
and
A. S. Willsky.
Filters.
In: Signals and Systems, edited by E. Cliff. Englewood Cliffs, NJ: Prentice Hall, 1983, p. 397-452.
24.
Pauli, J. E.,
and
L. E. Scheving.
Circadian rhythms in blood glucose and the effect of different lighting schedules, hypophysectomy, adrenal medullectomy and starvation.
Am. J. Anat.
120:
627-636,
1967[Medline].
25.
Persons, J. E.,
F. K. Stephan,
and
M. E. Bays.
Diet-induced obesity attenuates anticipation of food access in rats.
Physiol. Behav.
54:
55-64,
1993[Medline].
26.
Powley, T. L.,
and
W. Laughton.
Neural pathways involved in the hypothalamic integration of autonomic responses.
Diabetologia
20:
378-387,
1981.
27.
Rosenwasser, A. M.,
and
N. T. Adler.
Structure and function in circadian timing systems: evidence for multiple coupled circadian oscillators.
Neurosci. Biobehav. Rev.
10:
431-448,
1986[Medline].
28.
Russeck, M.,
and
R. Racotta.
Possible participation of oro-, gastro-, and enterohepatic reflexes in preabsorbtive satiation.
In: Interaction of the Chemical Senses with Nutrition, edited by M. R. Kare,
and J. G. Barnd. London: Academic, 1986, p. 373-393.
29.
Stephan, F. K.
Limits of entrainment to periodic feeding in rats with suprachiasmatic lesions.
J. Comp. Physiol.
143:
401-410,
1981.
30.
Stephan, F. K.
Calories affect zeitgeber properties of the feeding entrained circadian oscillator.
Physiol. Behav.
62:
995-1002,
1997[Medline].
31.
Stephan, F. K.,
and
G. Becker.
Entrainment of anticipatory activity to various durations of food access.
Physiol. Behav.
46:
731-741,
1989[Medline].
32.
Stephan, F. K.,
J. M. Swann,
and
C. L. Sisk.
Anticipation of 24 hr feeding schedules in rats with lesions of the suprachiasmatic nucleus.
Behav. Neural Biol.
25:
345-363,
1979.
33.
Suzuki, M.,
Y. Shimomura,
and
Y. Satoh.
Diurnal changes in lipolytic activity of isolated fat cells and their increased responsiveness to epinephrine and theophylline with meal feeding in rats.
J. Nutr. Sci. Vitaminol. (Tokyo)
29:
399-411,
1983[Medline].
34.
Voet, D.,
and
J. G. Voet.
Biochemistry. New York: Wiley, 1995, p. 785-794.
35.
Yamamoto, H.,
K. Nagai,
and
H. Nakagawa.
Role of the SCN in daily rhythms of plasma glucose, FFA, insulin and glucagon.
Cronobiol. Int.
4:
483-491,
1987.
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 A. Baez-Ruiz, C. Escobar, R. Aguilar-Roblero, O. Vazquez-Martinez, and M. Diaz-Munoz Metabolic adaptations of liver mitochondria during restricted feeding schedules Am J Physiol Gastrointest Liver Physiol, December 1, 2005; 289(6): G1015 - G1023. [Abstract] [Full Text] [PDF]
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S. A. Evans, M. M. Messina, W. D. Knight, A. D. Parsons, and J. M. Overton Long-Evans and Sprague-Dawley rats exhibit divergent responses to refeeding after caloric restriction Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2005; 288(6): R1468 - R1476. [Abstract] [Full Text] [PDF]
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M. Angeles-Castellanos, J. Mendoza, M. Diaz-Munoz, and C. Escobar Food entrainment modifies the c-Fos expression pattern in brain stem nuclei of rats Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2005; 288(3): R678 - R684. [Abstract] [Full Text] [PDF]
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M. Angeles-Castellanos, R. Aguilar-Roblero, and C. Escobar c-Fos expression in hypothalamic nuclei of food-entrained rats Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2004; 286(1): R158 - R165. [Abstract] [Full Text]
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S. Pitts, E. Perone, and R. Silver Food-entrained circadian rhythms are sustained in arrhythmic Clk/Clk mutant mice Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2003; 285(1): R57 - R67. [Abstract] [Full Text] [PDF]
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 J. V. Bruckner, R. Ramanathan, K. M. Lee, and S. Muralidhara Mechanisms of Circadian Rhythmicity of Carbon Tetrachloride Hepatotoxicity J. Pharmacol. Exp. Ther., January 1, 2002; 300(1): 273 - 281. [Abstract] [Full Text] [PDF]
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M. Diaz-Munoz, O. Vazquez-Martinez, R. Aguilar-Roblero, and C. Escobar Anticipatory changes in liver metabolism and entrainment of insulin, glucagon, and corticosterone in food-restricted rats Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2000; 279(6): R2048 - R2056. [Abstract] [Full Text] [PDF]
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A. J. Davidson and F. K. Stephan Feeding-entrained circadian rhythms in hypophysectomized rats with suprachiasmatic nucleus lesions Am J Physiol Regulatory Integrative Comp Physiol, November 1, 1999; 277(5): R1376 - R1384. [Abstract] [Full Text] [PDF]
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) and fasting conditions (
).
Dotted lines represent expected rhythm projected from ad libitum
condition. Single triangle indicates beginning of fasting episode.
White and black bars under abscissa
indicate lighting conditions.
) and their respective ad libitum-fed
controls (