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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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Locomotor activity recorded by motion sensors of rats restricted to 1 or 2 daily meals.A–C. Actograms from representative rats fed a 2 h daily meal at ZT4 (A) or ZT16 (B), or a 1 h meal at both times (C). Each line represents 24 h plotted from left to right in 10 min time bins. Time bins in which activity is registered are indicated by vertical deflections creating heavy bars when activity occurs across multiple consecutive bins. Mealtime is denoted by the opaque vertical bar. Lights-off is denoted by grey shading. D–F. Group mean average waveforms of activity during week 4 of restricted feeding, with mealtime at ZT4 (D), ZT16 (E) or at both times (F). Mealtimes are in grey shade. The daily 12 h light and dark periods are indicated by the heavy yellow and black bars, respectively.
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pone-0112451-g001: Locomotor activity recorded by motion sensors of rats restricted to 1 or 2 daily meals.A–C. Actograms from representative rats fed a 2 h daily meal at ZT4 (A) or ZT16 (B), or a 1 h meal at both times (C). Each line represents 24 h plotted from left to right in 10 min time bins. Time bins in which activity is registered are indicated by vertical deflections creating heavy bars when activity occurs across multiple consecutive bins. Mealtime is denoted by the opaque vertical bar. Lights-off is denoted by grey shading. D–F. Group mean average waveforms of activity during week 4 of restricted feeding, with mealtime at ZT4 (D), ZT16 (E) or at both times (F). Mealtimes are in grey shade. The daily 12 h light and dark periods are indicated by the heavy yellow and black bars, respectively.

Mentions: Within a few days of scheduled feeding, all of the rats in each of the three groups showed a robust bout of activity in anticipation of daily feeding (Fig.1A–F). When food was omitted on day 33, the bout of food anticipatory activity persisted through the expected mealtimes before decreasing. Activity reappeared prior to mealtime on the next day, confirming that anticipation of mealtime, on one-meal and two-meal daily schedules, reflected a persisting circadian oscillation and not a one cycle hourglass clock timing intervals of 12 or 24 h between meals [7], [20].


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)

Locomotor activity recorded by motion sensors of rats restricted to 1 or 2 daily meals.A–C. Actograms from representative rats fed a 2 h daily meal at ZT4 (A) or ZT16 (B), or a 1 h meal at both times (C). Each line represents 24 h plotted from left to right in 10 min time bins. Time bins in which activity is registered are indicated by vertical deflections creating heavy bars when activity occurs across multiple consecutive bins. Mealtime is denoted by the opaque vertical bar. Lights-off is denoted by grey shading. D–F. Group mean average waveforms of activity during week 4 of restricted feeding, with mealtime at ZT4 (D), ZT16 (E) or at both times (F). Mealtimes are in grey shade. The daily 12 h light and dark periods are indicated by the heavy yellow and black bars, respectively.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0112451-g001: Locomotor activity recorded by motion sensors of rats restricted to 1 or 2 daily meals.A–C. Actograms from representative rats fed a 2 h daily meal at ZT4 (A) or ZT16 (B), or a 1 h meal at both times (C). Each line represents 24 h plotted from left to right in 10 min time bins. Time bins in which activity is registered are indicated by vertical deflections creating heavy bars when activity occurs across multiple consecutive bins. Mealtime is denoted by the opaque vertical bar. Lights-off is denoted by grey shading. D–F. Group mean average waveforms of activity during week 4 of restricted feeding, with mealtime at ZT4 (D), ZT16 (E) or at both times (F). Mealtimes are in grey shade. The daily 12 h light and dark periods are indicated by the heavy yellow and black bars, respectively.
Mentions: Within a few days of scheduled feeding, all of the rats in each of the three groups showed a robust bout of activity in anticipation of daily feeding (Fig.1A–F). When food was omitted on day 33, the bout of food anticipatory activity persisted through the expected mealtimes before decreasing. Activity reappeared prior to mealtime on the next day, confirming that anticipation of mealtime, on one-meal and two-meal daily schedules, reflected a persisting circadian oscillation and not a one cycle hourglass clock timing intervals of 12 or 24 h between meals [7], [20].

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