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Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice.

Gallardo CM, Darvas M, Oviatt M, Chang CH, Michalik M, Huddy TF, Meyer EE, Shuster SA, Aguayo A, Hill EM, Kiani K, Ikpeazu J, Martinez JS, Purpura M, Smit AN, Patton DF, Mistlberger RE, Palmiter RD, Steele AD - Elife (2014)

Bottom Line: Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive.To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA.These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, California Institute of Technology, Pasadena, United States.

ABSTRACT
Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive. In this study, we show that mice lacking the dopamine D1 receptor (D1R KO mice) manifest greatly reduced FAA, whereas mice lacking the dopamine D2 receptor have normal FAA. To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA. Within the dorsal striatum, the daily rhythm of clock gene period2 expression was markedly suppressed in D1R KO mice. Pharmacological activation of D1R at the same time daily was sufficient to establish anticipatory activity in wild-type mice. These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

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Related in: MedlinePlus

Actogram data for representative D1R knockout and control mice.Representative actograms of disc running activity in D1R WT (A and C) and D1R KO (B and D) mice. Each line represents 24 hr plotted in 10 min bins from left to right. Consecutive days are aligned vertically. Bins during which activity was registered are denoted by vertical deflections of varying height in proportion to the amount of activity. Lights-off is indicated by shading. Days of restricted feeding are indicated by the vertical thin bars to the immediate right or left of the actograms. Meal time hours are outlined by thin red lines. Food was a high fat chow (A and B) or regular chow (C and D).DOI:http://dx.doi.org/10.7554/eLife.03781.009
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fig3s1: Actogram data for representative D1R knockout and control mice.Representative actograms of disc running activity in D1R WT (A and C) and D1R KO (B and D) mice. Each line represents 24 hr plotted in 10 min bins from left to right. Consecutive days are aligned vertically. Bins during which activity was registered are denoted by vertical deflections of varying height in proportion to the amount of activity. Lights-off is indicated by shading. Days of restricted feeding are indicated by the vertical thin bars to the immediate right or left of the actograms. Meal time hours are outlined by thin red lines. Food was a high fat chow (A and B) or regular chow (C and D).DOI:http://dx.doi.org/10.7554/eLife.03781.009

Mentions: The diet of powdered chow mixed with corn oil was used to encourage food intake during the limited time of availability. To determine if the palatability or caloric density of the food influences the magnitude of FAA differentially in KO and WT mice, the diet was changed to powdered chow mixed with water. The mice were fed ad-lib for 22 days and were then restricted to a 4-hr daily meal for 74 days. KO mice continued to show significantly less total activity (p < 0.01) and less FAA (p < 0.01) than WT mice. FAA ratios in both groups were increased relative to the ratios evident when fed high fat chow, but remained significantly lower in KO mice (p < 0.05). In only one KO mice were the FAA counts and the FAA ratios significantly increased during the last 10 days of restricted feeding compared to the last 10 days of ad-lib food access (counts: paired t(9) = 6.52, p < 0.001; ratios t(9) = 5.22, p = 0.005), whereas the counts and ratios were significantly increased in all of the WT mice at p < 0.00001. Differences between KO and WT mice were stable across 74 days on this restricted feeding schedule. Body weights remained stable at ∼90% of baseline in both groups. Data from representative D1R KO and WT mice are shown in Figure 3—figure supplement 1.


Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice.

Gallardo CM, Darvas M, Oviatt M, Chang CH, Michalik M, Huddy TF, Meyer EE, Shuster SA, Aguayo A, Hill EM, Kiani K, Ikpeazu J, Martinez JS, Purpura M, Smit AN, Patton DF, Mistlberger RE, Palmiter RD, Steele AD - Elife (2014)

Actogram data for representative D1R knockout and control mice.Representative actograms of disc running activity in D1R WT (A and C) and D1R KO (B and D) mice. Each line represents 24 hr plotted in 10 min bins from left to right. Consecutive days are aligned vertically. Bins during which activity was registered are denoted by vertical deflections of varying height in proportion to the amount of activity. Lights-off is indicated by shading. Days of restricted feeding are indicated by the vertical thin bars to the immediate right or left of the actograms. Meal time hours are outlined by thin red lines. Food was a high fat chow (A and B) or regular chow (C and D).DOI:http://dx.doi.org/10.7554/eLife.03781.009
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4196120&req=5

fig3s1: Actogram data for representative D1R knockout and control mice.Representative actograms of disc running activity in D1R WT (A and C) and D1R KO (B and D) mice. Each line represents 24 hr plotted in 10 min bins from left to right. Consecutive days are aligned vertically. Bins during which activity was registered are denoted by vertical deflections of varying height in proportion to the amount of activity. Lights-off is indicated by shading. Days of restricted feeding are indicated by the vertical thin bars to the immediate right or left of the actograms. Meal time hours are outlined by thin red lines. Food was a high fat chow (A and B) or regular chow (C and D).DOI:http://dx.doi.org/10.7554/eLife.03781.009
Mentions: The diet of powdered chow mixed with corn oil was used to encourage food intake during the limited time of availability. To determine if the palatability or caloric density of the food influences the magnitude of FAA differentially in KO and WT mice, the diet was changed to powdered chow mixed with water. The mice were fed ad-lib for 22 days and were then restricted to a 4-hr daily meal for 74 days. KO mice continued to show significantly less total activity (p < 0.01) and less FAA (p < 0.01) than WT mice. FAA ratios in both groups were increased relative to the ratios evident when fed high fat chow, but remained significantly lower in KO mice (p < 0.05). In only one KO mice were the FAA counts and the FAA ratios significantly increased during the last 10 days of restricted feeding compared to the last 10 days of ad-lib food access (counts: paired t(9) = 6.52, p < 0.001; ratios t(9) = 5.22, p = 0.005), whereas the counts and ratios were significantly increased in all of the WT mice at p < 0.00001. Differences between KO and WT mice were stable across 74 days on this restricted feeding schedule. Body weights remained stable at ∼90% of baseline in both groups. Data from representative D1R KO and WT mice are shown in Figure 3—figure supplement 1.

Bottom Line: Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive.To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA.These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, California Institute of Technology, Pasadena, United States.

ABSTRACT
Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive. In this study, we show that mice lacking the dopamine D1 receptor (D1R KO mice) manifest greatly reduced FAA, whereas mice lacking the dopamine D2 receptor have normal FAA. To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA. Within the dorsal striatum, the daily rhythm of clock gene period2 expression was markedly suppressed in D1R KO mice. Pharmacological activation of D1R at the same time daily was sufficient to establish anticipatory activity in wild-type mice. These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

Show MeSH
Related in: MedlinePlus