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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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High activity data for D1R knockout mice in seconds (median +/- SEM).High activity behaviors of D1R KO and WT (same mice as Figure 2) in terms of median seconds (unnormalized) for (A) day 7, (B) day 0, (C) day 7, (D)day 14, (E) day 21, and (F) day 28. (G) Amount of high activity in the 3 hr preceding scheduled feeding in seconds. (H) Amount of total high activity over 24 hr recordings in seconds.DOI:http://dx.doi.org/10.7554/eLife.03781.005
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fig2s1: High activity data for D1R knockout mice in seconds (median +/- SEM).High activity behaviors of D1R KO and WT (same mice as Figure 2) in terms of median seconds (unnormalized) for (A) day 7, (B) day 0, (C) day 7, (D)day 14, (E) day 21, and (F) day 28. (G) Amount of high activity in the 3 hr preceding scheduled feeding in seconds. (H) Amount of total high activity over 24 hr recordings in seconds.DOI:http://dx.doi.org/10.7554/eLife.03781.005

Mentions: We also examined mice deficient in D1R (Drago et al., 1994). The normalized activity waveform of D1R WT and D1R KO mice prior to any dietary intervention on day -7 revealed strong nocturnal activity in D1R KO and control mice, with D1R KO mice showing slightly increased nocturnal activity compared to WT controls (Figure 2A, Figure 2—figure supplement 1). Summation of time of high activity behaviors in the 11 hr of dark yielded a median value of 93.5 min (min) for D1R WT mice (n = 16) compared with a value of 173.8 min for D1R KO (n = 19); this difference was statistically significant (p = 0.045, Mann–Whitney Test). In comparison, activity values during the lights-on period were not significantly different (median values of 44.2 and 51.3 min were observed for D1R WT and KO, respectively; p = 0.46) These results suggest that the D1R KO mice do not exhibit locomotor defects preventing nocturnal activity.10.7554/eLife.03781.004Figure 2.Activity of D1R KO (n = 18) mice and WT (n = 16) mice on 60% CR.


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)

High activity data for D1R knockout mice in seconds (median +/- SEM).High activity behaviors of D1R KO and WT (same mice as Figure 2) in terms of median seconds (unnormalized) for (A) day 7, (B) day 0, (C) day 7, (D)day 14, (E) day 21, and (F) day 28. (G) Amount of high activity in the 3 hr preceding scheduled feeding in seconds. (H) Amount of total high activity over 24 hr recordings in seconds.DOI:http://dx.doi.org/10.7554/eLife.03781.005
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig2s1: High activity data for D1R knockout mice in seconds (median +/- SEM).High activity behaviors of D1R KO and WT (same mice as Figure 2) in terms of median seconds (unnormalized) for (A) day 7, (B) day 0, (C) day 7, (D)day 14, (E) day 21, and (F) day 28. (G) Amount of high activity in the 3 hr preceding scheduled feeding in seconds. (H) Amount of total high activity over 24 hr recordings in seconds.DOI:http://dx.doi.org/10.7554/eLife.03781.005
Mentions: We also examined mice deficient in D1R (Drago et al., 1994). The normalized activity waveform of D1R WT and D1R KO mice prior to any dietary intervention on day -7 revealed strong nocturnal activity in D1R KO and control mice, with D1R KO mice showing slightly increased nocturnal activity compared to WT controls (Figure 2A, Figure 2—figure supplement 1). Summation of time of high activity behaviors in the 11 hr of dark yielded a median value of 93.5 min (min) for D1R WT mice (n = 16) compared with a value of 173.8 min for D1R KO (n = 19); this difference was statistically significant (p = 0.045, Mann–Whitney Test). In comparison, activity values during the lights-on period were not significantly different (median values of 44.2 and 51.3 min were observed for D1R WT and KO, respectively; p = 0.46) These results suggest that the D1R KO mice do not exhibit locomotor defects preventing nocturnal activity.10.7554/eLife.03781.004Figure 2.Activity of D1R KO (n = 18) mice and WT (n = 16) mice on 60% CR.

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