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Circadian mechanisms of food anticipatory rhythms in rats fed once or twice daily: clock gene and endocrine correlates.

Patton DF, Katsuyama AM, Pavlovski I, Michalik M, Patterson Z, Parfyonov M, Smit AN, Marchant EG, Chung SH, Chung J, Abizaid A, Storch KF, de la Iglesia H, Mistlberger RE - PLoS ONE (2014)

Bottom Line: Multiple clock genes from adrenals and stomachs were assayed by RT-PCR.Blood was assayed for corticosterone and ghrelin.Bmal1 expression was quantified in 14 brain regions by in situ hybridization.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Simon Fraser University, Burnaby, BC, Canada.

ABSTRACT
Circadian clocks in many brain regions and peripheral tissues are entrained by the daily rhythm of food intake. Clocks in one or more of these locations generate a daily rhythm of locomotor activity that anticipates a regular mealtime. Rats and mice can also anticipate two daily meals. Whether this involves 1 or 2 circadian clocks is unknown. To gain insight into how the circadian system adjusts to 2 daily mealtimes, male rats in a 12∶12 light-dark cycle were fed a 2 h meal either 4 h after lights-on or 4 h after lights-off, or a 1 h meal at both times. After 30 days, brain, blood, adrenal and stomach tissue were collected at 6 time points. Multiple clock genes from adrenals and stomachs were assayed by RT-PCR. Blood was assayed for corticosterone and ghrelin. Bmal1 expression was quantified in 14 brain regions by in situ hybridization. Clock gene rhythms in adrenal and stomach from day-fed rats oscillated in antiphase with the rhythms in night-fed rats, and at an intermediate phase in rats fed twice daily. Corticosterone and ghrelin in 1-meal rats peaked at or prior to the expected mealtime. In 2-meal rats, corticosterone peaked only prior the nighttime meal, while ghrelin peaked prior to the daytime meal and then remained elevated. The olfactory bulb, nucleus accumbens, dorsal striatum, cerebellum and arcuate nucleus exhibited significant daily rhythms of Bmal1 in the night-fed groups that were approximately in antiphase in the day-fed groups, and at intermediate levels (arrhythmic) in rats anticipating 2 daily meals. The dissociations between anticipatory activity and the peripheral clocks and hormones in rats anticipating 2 daily meals argue against a role for these signals in the timing of behavioral rhythms. The absence of rhythmicity at the tissue level in brain regions from rats anticipating 2 daily meals support behavioral evidence that circadian clock cells in these tissues may reorganize into two populations coupled to different meals.

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Related in: MedlinePlus

Group mean (± SEM) optical densities representing Bmal1 mRNA from rats fed 2 h daily at ZT4 (red dashed curve) or ZT16 (blue solid curve), or for 1 h at both times (green dotted curve).A. Olfactory bulb, B. nucleus accumbens core, C. dorsal striatum, ventrolateral quadrant, D. nucleus accumbens shell, E. cerebellum, F. Arcuate nucleus.
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pone-0112451-g005: Group mean (± SEM) optical densities representing Bmal1 mRNA from rats fed 2 h daily at ZT4 (red dashed curve) or ZT16 (blue solid curve), or for 1 h at both times (green dotted curve).A. Olfactory bulb, B. nucleus accumbens core, C. dorsal striatum, ventrolateral quadrant, D. nucleus accumbens shell, E. cerebellum, F. Arcuate nucleus.

Mentions: In ad-lib fed rats and mice, the OB exhibits circadian oscillations of Per1 and Per2 that persist in vivo after SCN-ablation, and in long term tissue explants [48], [49]. Recent work in rats [50] and rabbit pups [51] has shown that Per1 and Per2 rhythms in the OB are entrainable by scheduled feeding. We observed a significant circadian oscillation of Bmal1 expression in the OB that peaked at ZT10 in the night-fed group, and at ZT4 in the day-fed group (Fig. 5A; Table 2). Notably, Bmal1 expression did not exhibit a significant rhythm in the 2-meal group; at 5 of 6 time points, expression levels fell mid-way between those evident in the ZT4 and ZT16 groups. Assuming that circadian oscillations in the OB persist at the cellular level, this result could reflect either complete desynchrony within a population of oscillators, or uncoupling between two populations of OB clock cells, each entrained to a different meal.


Circadian mechanisms of food anticipatory rhythms in rats fed once or twice daily: clock gene and endocrine correlates.

Patton DF, Katsuyama AM, Pavlovski I, Michalik M, Patterson Z, Parfyonov M, Smit AN, Marchant EG, Chung SH, Chung J, Abizaid A, Storch KF, de la Iglesia H, Mistlberger RE - PLoS ONE (2014)

Group mean (± SEM) optical densities representing Bmal1 mRNA from rats fed 2 h daily at ZT4 (red dashed curve) or ZT16 (blue solid curve), or for 1 h at both times (green dotted curve).A. Olfactory bulb, B. nucleus accumbens core, C. dorsal striatum, ventrolateral quadrant, D. nucleus accumbens shell, E. cerebellum, F. Arcuate nucleus.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263600&req=5

pone-0112451-g005: Group mean (± SEM) optical densities representing Bmal1 mRNA from rats fed 2 h daily at ZT4 (red dashed curve) or ZT16 (blue solid curve), or for 1 h at both times (green dotted curve).A. Olfactory bulb, B. nucleus accumbens core, C. dorsal striatum, ventrolateral quadrant, D. nucleus accumbens shell, E. cerebellum, F. Arcuate nucleus.
Mentions: In ad-lib fed rats and mice, the OB exhibits circadian oscillations of Per1 and Per2 that persist in vivo after SCN-ablation, and in long term tissue explants [48], [49]. Recent work in rats [50] and rabbit pups [51] has shown that Per1 and Per2 rhythms in the OB are entrainable by scheduled feeding. We observed a significant circadian oscillation of Bmal1 expression in the OB that peaked at ZT10 in the night-fed group, and at ZT4 in the day-fed group (Fig. 5A; Table 2). Notably, Bmal1 expression did not exhibit a significant rhythm in the 2-meal group; at 5 of 6 time points, expression levels fell mid-way between those evident in the ZT4 and ZT16 groups. Assuming that circadian oscillations in the OB persist at the cellular level, this result could reflect either complete desynchrony within a population of oscillators, or uncoupling between two populations of OB clock cells, each entrained to a different meal.

Bottom Line: Multiple clock genes from adrenals and stomachs were assayed by RT-PCR.Blood was assayed for corticosterone and ghrelin.Bmal1 expression was quantified in 14 brain regions by in situ hybridization.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Simon Fraser University, Burnaby, BC, Canada.

ABSTRACT
Circadian clocks in many brain regions and peripheral tissues are entrained by the daily rhythm of food intake. Clocks in one or more of these locations generate a daily rhythm of locomotor activity that anticipates a regular mealtime. Rats and mice can also anticipate two daily meals. Whether this involves 1 or 2 circadian clocks is unknown. To gain insight into how the circadian system adjusts to 2 daily mealtimes, male rats in a 12∶12 light-dark cycle were fed a 2 h meal either 4 h after lights-on or 4 h after lights-off, or a 1 h meal at both times. After 30 days, brain, blood, adrenal and stomach tissue were collected at 6 time points. Multiple clock genes from adrenals and stomachs were assayed by RT-PCR. Blood was assayed for corticosterone and ghrelin. Bmal1 expression was quantified in 14 brain regions by in situ hybridization. Clock gene rhythms in adrenal and stomach from day-fed rats oscillated in antiphase with the rhythms in night-fed rats, and at an intermediate phase in rats fed twice daily. Corticosterone and ghrelin in 1-meal rats peaked at or prior to the expected mealtime. In 2-meal rats, corticosterone peaked only prior the nighttime meal, while ghrelin peaked prior to the daytime meal and then remained elevated. The olfactory bulb, nucleus accumbens, dorsal striatum, cerebellum and arcuate nucleus exhibited significant daily rhythms of Bmal1 in the night-fed groups that were approximately in antiphase in the day-fed groups, and at intermediate levels (arrhythmic) in rats anticipating 2 daily meals. The dissociations between anticipatory activity and the peripheral clocks and hormones in rats anticipating 2 daily meals argue against a role for these signals in the timing of behavioral rhythms. The absence of rhythmicity at the tissue level in brain regions from rats anticipating 2 daily meals support behavioral evidence that circadian clock cells in these tissues may reorganize into two populations coupled to different meals.

Show MeSH
Related in: MedlinePlus