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. 2013 Nov 29;8(11):e82381.
doi: 10.1371/journal.pone.0082381. eCollection 2013.

Dopaminergic regulation of circadian food anticipatory activity rhythms in the rat

Andrea N Smit  1 , Danica F Patton, Mateusz Michalik, Hanna Opiol, Ralph E Mistlberger
Affiliations

Dopaminergic regulation of circadian food anticipatory activity rhythms in the rat

Andrea N Smit et al. PLoS One. .

Abstract

Circadian activity rhythms are jointly controlled by a master pacemaker in the hypothalamic suprachiasmatic nuclei (SCN) and by food-entrainable circadian oscillators (FEOs) located elsewhere. The SCN mediates synchrony to daily light-dark cycles, whereas FEOs generate activity rhythms synchronized with regular daily mealtimes. The location of FEOs generating food anticipation rhythms, and the pathways that entrain these FEOs, remain to be clarified. To gain insight into entrainment pathways, we developed a protocol for measuring phase shifts of anticipatory activity rhythms in response to pharmacological probes. We used this protocol to examine a role for dopamine signaling in the timing of circadian food anticipation. To generate a stable food anticipation rhythm, rats were fed 3h/day beginning 6-h after lights-on or in constant light for at least 3 weeks. Rats then received the D2 agonist quinpirole (1 mg/kg IP) alone or after pretreatment with the dopamine synthesis inhibitor α-methylparatyrosine (AMPT). By comparison with vehicle injections, quinpirole administered 1-h before lights-off (19h before mealtime) induced a phase delay of activity onset prior to the next meal. Delay shifts were larger in rats pretreated with AMPT, and smaller following quinpirole administered 4-h after lights-on. A significant shift was not observed in response to the D1 agonist SKF81297. These results provide evidence that signaling at D2 receptors is involved in phase control of FEOs responsible for circadian food anticipatory rhythms in rats.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Activity of rats during restricted feeding, and effects of drug and vehicle injections.
Each line represents 24h of recording, with time in 10 min bins plotted from left to right, and consecutive days aligned vertically. Time bins during which 1 or more wheel revolutions (A-E) or general activity counts (F) were registered are represented by heavy bars, the height of which corresponds to activity level (in quartiles). Mealtime occurred between hours 6-9 (Panels A, F) or 6-8 (Panels B-E) and is shaded green. Injections are denoted by red circles and arrows for quinpirole (QUIN, 1 mg/kg), blue squares and arrows for alpha-methylparatyrosine (AMPT, 200 mg/kg), and unfilled circles and black arrows for vehicle (sterile water). Grey shading indicates lights-off, as part of the daily LD cycle or the 1 or 2 days following drug injections. Food anticipatory activity onset was measured on the 4 days prior to injections and on the day after injections. Food anticipatory activity onset was delayed on the day following quinpirole (A,F) or quinpirole with AMPT pretreatment (B), but was not delayed on the day following AMPT (C) or vehicle alone (D). Some rats stopped using the running wheels for 2 or more days after AMPT and could not be used to measure phase shifts (e.g., E).
Figure 2
Figure 2. Group mean (+ SEM) average waveforms of activity during restricted feeding on the day following injections of drug (red curves) or vehicle (blue curves) in Experiments 1-4.
Injection times (in zeitgeber time, where ZT0 is lights-on by convention) are indicated by the arrows and scheduled mealtimes by the vertical dotted lines. The LD cycle is indicated by the black and yellow bars (A,C,E,I); note, however, that in those experiments, the lights were kept off during the days represented here (i.e., the day after injection). The bar graphs represent phase shifts of premeal activity onset on the day after the injections by comparison with the 4 days prior to injection. A delay in the onset of premeal activity is represented by negative values, and an advance by positive values. Note that quinpirole injections induced delays relative to vehicle injections in all experiments. P-values are the results of paired t-tests.
Figure 3
Figure 3. Changes in the timing of food anticipatory activity following quinpirole (1 mg/kg; red dots) or vehicle injections (blue dots) administered on the previous day at ZT11 (1h before lights off) or ZT4 (4h after lights-on) in Experiment 1.
Each data point represents the difference in hours between food anticipatory activity onset on the day following injections compared to food anticipatory activity onset averaged over the 4 days preceding the injections. Positive values indicate phase advances (earlier onset of activity) and negative values indicate phase delays (later onset of activity). Within-subject pairs are connected by lines, illustrating that in most rats, activity onsets were delayed following quinpirole injections relative to vehicle injections.
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