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A non-canonical striatopallidal Go pathway that supports motor control

Author

Listed:
  • Marie A. Labouesse

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute
    ETH Zurich
    ETH Zurich and University of Zurich)

  • Arturo Torres-Herraez

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute)

  • Muhammad O. Chohan

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute)

  • Joseph M. Villarin

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute)

  • Julia Greenwald

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute)

  • Xiaoxiao Sun

    (New York State Psychiatric Institute
    Columbia University)

  • Mysarah Zahran

    (New York State Psychiatric Institute
    Columbia University)

  • Alice Tang

    (New York State Psychiatric Institute
    Columbia University)

  • Sherry Lam

    (National Institute on Drug Abuse Intramural Research Program)

  • Jeremy Veenstra-VanderWeele

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute)

  • Clay O. Lacefield

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute)

  • Jordi Bonaventura

    (National Institute on Drug Abuse Intramural Research Program
    Universitat de Barcelona)

  • Michael Michaelides

    (National Institute on Drug Abuse Intramural Research Program
    Johns Hopkins University School of Medicine)

  • C. Savio Chan

    (Northwestern University)

  • Ofer Yizhar

    (Weizmann Institute of Science)

  • Christoph Kellendonk

    (Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center
    New York State Psychiatric Institute
    Columbia University Irving Medical Center)

Abstract

In the classical model of the basal ganglia, direct pathway striatal projection neurons (dSPNs) send projections to the substantia nigra (SNr) and entopeduncular nucleus to regulate motor function. Recent studies have re-established that dSPNs also possess axon collaterals within the globus pallidus (GPe) (bridging collaterals), yet the significance of these collaterals for behavior is unknown. Here we use in vivo optical and chemogenetic tools combined with deep learning approaches in mice to dissect the roles of dSPN GPe collaterals in motor function. We find that dSPNs projecting to the SNr send synchronous motor-related information to the GPe via axon collaterals. Inhibition of native activity in dSPN GPe terminals impairs motor activity and function via regulation of Npas1 neurons. We propose a model by which dSPN GPe axon collaterals (striatopallidal Go pathway) act in concert with the canonical terminals in the SNr to support motor control by inhibiting Npas1 neurons.

Suggested Citation

  • Marie A. Labouesse & Arturo Torres-Herraez & Muhammad O. Chohan & Joseph M. Villarin & Julia Greenwald & Xiaoxiao Sun & Mysarah Zahran & Alice Tang & Sherry Lam & Jeremy Veenstra-VanderWeele & Clay O., 2023. "A non-canonical striatopallidal Go pathway that supports motor control," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42288-1
    DOI: 10.1038/s41467-023-42288-1
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    References listed on IDEAS

    as
    1. Matthew Baker & Seungwoo Kang & Sa-Ik Hong & Minryung Song & Minsu Abel Yang & Lee Peyton & Hesham Essa & Sang Wan Lee & Doo-Sup Choi, 2023. "External globus pallidus input to the dorsal striatum regulates habitual seeking behavior in male mice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Alexxai V. Kravitz & Benjamin S. Freeze & Philip R. L. Parker & Kenneth Kay & Myo T. Thwin & Karl Deisseroth & Anatol C. Kreitzer, 2010. "Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry," Nature, Nature, vol. 466(7306), pages 622-626, July.
    3. Eduardo F. Gallo & Jozsef Meszaros & Jeremy D. Sherman & Muhammad O. Chohan & Eric Teboul & Claire S. Choi & Holly Moore & Jonathan A. Javitch & Christoph Kellendonk, 2018. "Accumbens dopamine D2 receptors increase motivation by decreasing inhibitory transmission to the ventral pallidum," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    4. Jaeeon Lee & Bernardo L. Sabatini, 2021. "Striatal indirect pathway mediates exploration via collicular competition," Nature, Nature, vol. 599(7886), pages 645-649, November.
    5. Arpiar Saunders & Ian A. Oldenburg & Vladimir K. Berezovskii & Caroline A. Johnson & Nathan D. Kingery & Hunter L. Elliott & Tiao Xie & Charles R. Gerfen & Bernardo L. Sabatini, 2015. "A direct GABAergic output from the basal ganglia to frontal cortex," Nature, Nature, vol. 521(7550), pages 85-89, May.
    6. Yan Zhang & Márton Rózsa & Yajie Liang & Daniel Bushey & Ziqiang Wei & Jihong Zheng & Daniel Reep & Gerard Joey Broussard & Arthur Tsang & Getahun Tsegaye & Sujatha Narayan & Christopher J. Obara & Ji, 2023. "Fast and sensitive GCaMP calcium indicators for imaging neural populations," Nature, Nature, vol. 615(7954), pages 884-891, March.
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