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

  1. Christian Gallardo
  2. Martin Darvas
  3. Mia Oviatt
  4. Chris Chang
  5. Mateusz Michalik
  6. Timothy F Huddy
  7. Emily E Meyer
  8. Scott A Shuster
  9. Antonio Aguayo
  10. Elizabeth M Hill
  11. Karun Kiani
  12. Jonathan Ikpeazu
  13. Johan S Martinez
  14. Mari Purpura
  15. Andrea N Smit
  16. Danica Paton
  17. Ralph E Mistlberger
  18. Richard Palmiter
  19. Andrew Steele  Is a corresponding author
  1. California Institute of Technology, United States
  2. University of Washington, United States
  3. Claremont-McKenna College, Pitzer College, Scripps College, United States
  4. Simon Fraser University, Canada
  5. California State Polytechnic University Pomona, United States
  6. Howard Hughes Medical Institute, University of Washington, 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. Here 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 per2 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 in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

Article and author information

Author details

  1. Christian Gallardo

    California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  2. Martin Darvas

    University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  3. Mia Oviatt

    California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  4. Chris Chang

    Claremont-McKenna College, Pitzer College, Scripps College, Claremont, United States
    Competing interests
    No competing interests declared.
  5. Mateusz Michalik

    Simon Fraser University, Burnaby, Canada
    Competing interests
    No competing interests declared.
  6. Timothy F Huddy

    California State Polytechnic University Pomona, Pomona, United States
    Competing interests
    No competing interests declared.
  7. Emily E Meyer

    Claremont-McKenna College, Pitzer College, Scripps College, Claremont, United States
    Competing interests
    No competing interests declared.
  8. Scott A Shuster

    California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  9. Antonio Aguayo

    California State Polytechnic University Pomona, Pomona, United States
    Competing interests
    No competing interests declared.
  10. Elizabeth M Hill

    California State Polytechnic University Pomona, Pomona, United States
    Competing interests
    No competing interests declared.
  11. Karun Kiani

    Claremont-McKenna College, Pitzer College, Scripps College, Claremont, United States
    Competing interests
    No competing interests declared.
  12. Jonathan Ikpeazu

    California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  13. Johan S Martinez

    California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  14. Mari Purpura

    Claremont-McKenna College, Pitzer College, Scripps College, Claremont, United States
    Competing interests
    No competing interests declared.
  15. Andrea N Smit

    Simon Fraser University, Burnaby, Canada
    Competing interests
    No competing interests declared.
  16. Danica Paton

    Simon Fraser University, Burnaby, Canada
    Competing interests
    No competing interests declared.
  17. Ralph E Mistlberger

    Simon Fraser University, Burnaby, Canada
    Competing interests
    No competing interests declared.
  18. Richard Palmiter

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    Richard Palmiter, Reviewing editor, eLife.
  19. Andrew Steele

    California State Polytechnic University Pomona, Pomona, United States
    For correspondence
    adsteele@csupomona.edu
    Competing interests
    No competing interests declared.

Ethics

Animal experimentation: This study was performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocol 1567.

Copyright

© 2014, Gallardo et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Christian Gallardo
  2. Martin Darvas
  3. Mia Oviatt
  4. Chris Chang
  5. Mateusz Michalik
  6. Timothy F Huddy
  7. Emily E Meyer
  8. Scott A Shuster
  9. Antonio Aguayo
  10. Elizabeth M Hill
  11. Karun Kiani
  12. Jonathan Ikpeazu
  13. Johan S Martinez
  14. Mari Purpura
  15. Andrea N Smit
  16. Danica Paton
  17. Ralph E Mistlberger
  18. Richard Palmiter
  19. Andrew Steele
(2014)
Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice
eLife 3:e03781.
https://doi.org/10.7554/eLife.03781

Share this article

https://doi.org/10.7554/eLife.03781

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