IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42288-1.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42288-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42288-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Sean C. Piantadosi & Elizabeth E. Manning & Brittany L. Chamberlain & James Hyde & Zoe LaPalombara & Nicholas M. Bannon & Jamie L. Pierson & Vijay M. K Namboodiri & Susanne E. Ahmari, 2024. "Hyperactivity of indirect pathway-projecting spiny projection neurons promotes compulsive behavior," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    3. Caio Vaz Rimoli & Claudio Moretti & Fernando Soldevila & Enora Brémont & Cathie Ventalon & Sylvain Gigan, 2024. "Demixing fluorescence time traces transmitted by multimode fibers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Xuandi Hou & Jianing Jing & Yizhou Jiang & Xiaohui Huang & Quanxiang Xian & Ting Lei & Jiejun Zhu & Kin Fung Wong & Xinyi Zhao & Min Su & Danni Li & Langzhou Liu & Zhihai Qiu & Lei Sun, 2024. "Nanobubble-actuated ultrasound neuromodulation for selectively shaping behavior in mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Frederic Fiore & Khaleel Alhalaseh & Ram R. Dereddi & Felipe Bodaleo Torres & Ilknur Çoban & Ali Harb & Amit Agarwal, 2023. "Norepinephrine regulates calcium signals and fate of oligodendrocyte precursor cells in the mouse cerebral cortex," Nature Communications, Nature, vol. 14(1), pages 1-25, December.
    6. Daigo Takeuchi & Dheeraj Roy & Shruti Muralidhar & Takashi Kawai & Andrea Bari & Chanel Lovett & Heather A. Sullivan & Ian R. Wickersham & Susumu Tonegawa, 2022. "Cingulate-motor circuits update rule representations for sequential choice decisions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Yusuke Nasu & Abhi Aggarwal & Giang N. T. Le & Camilla Trang Vo & Yuki Kambe & Xinxing Wang & Felix R. M. Beinlich & Ashley Bomin Lee & Tina R. Ram & Fangying Wang & Kelsea A. Gorzo & Yuki Kamijo & Ma, 2023. "Lactate biosensors for spectrally and spatially multiplexed fluorescence imaging," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Natalia V. Barykina & Erin M. Carey & Olena S. Oliinyk & Axel Nimmerjahn & Vladislav V. Verkhusha, 2024. "Destabilized near-infrared fluorescent nanobodies enable background-free targeting of GFP-based biosensors for imaging and manipulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Nicola Montemurro & Nelida Aliaga & Pablo Graff & Amanda Escribano & Jafeth Lizana, 2022. "New Targets and New Technologies in the Treatment of Parkinson’s Disease: A Narrative Review," IJERPH, MDPI, vol. 19(14), pages 1-18, July.
    10. Yang, Shuangming & Wei, Xile & Deng, Bin & Liu, Chen & Li, Huiyan & Wang, Jiang, 2018. "Efficient digital implementation of a conductance-based globus pallidus neuron and the dynamics analysis," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 494(C), pages 484-502.
    11. Adrien T. Stanley & Michael R. Post & Clay Lacefield & David Sulzer & Maria Concetta Miniaci, 2023. "Norepinephrine release in the cerebellum contributes to aversive learning," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Alyse Thomas & Weiguo Yang & Catherine Wang & Sri Laasya Tipparaju & Guang Chen & Brennan Sullivan & Kylie Swiekatowski & Mahima Tatam & Charles Gerfen & Nuo Li, 2023. "Superior colliculus bidirectionally modulates choice activity in frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    13. Suma Chinta & Scott R. Pluta, 2023. "Neural mechanisms for the localization of unexpected external motion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    14. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    15. Tadaaki Nishioka & Suthinee Attachaipanich & Kosuke Hamaguchi & Michael Lazarus & Alban Kerchove d’Exaerde & Tom Macpherson & Takatoshi Hikida, 2023. "Error-related signaling in nucleus accumbens D2 receptor-expressing neurons guides inhibition-based choice behavior in mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Miguel Skirzewski & Oren Princz-Lebel & Liliana German-Castelan & Alycia M. Crooks & Gerard Kyungwook Kim & Sophie Henke Tarnow & Amy Reichelt & Sara Memar & Daniel Palmer & Yulong Li & R. Jane Rylett, 2022. "Continuous cholinergic-dopaminergic updating in the nucleus accumbens underlies approaches to reward-predicting cues," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    17. Wang, Zhizhi & Hu, Bing & Zhou, Weiting & Xu, Minbo & Wang, Dingjiang, 2023. "Hopf bifurcation mechanism analysis in an improved cortex-basal ganglia network with distributed delays: An application to Parkinson’s disease," Chaos, Solitons & Fractals, Elsevier, vol. 166(C).
    18. Rosalyn J Moran & Nicolas Mallet & Vladimir Litvak & Raymond J Dolan & Peter J Magill & Karl J Friston & Peter Brown, 2011. "Alterations in Brain Connectivity Underlying Beta Oscillations in Parkinsonism," PLOS Computational Biology, Public Library of Science, vol. 7(8), pages 1-15, August.
    19. Akshay Markanday & Sungho Hong & Junya Inoue & Erik Schutter & Peter Thier, 2023. "Multidimensional cerebellar computations for flexible kinematic control of movements," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Lizhu Li & Lihui Lu & Yuqi Ren & Guo Tang & Yu Zhao & Xue Cai & Zhao Shi & He Ding & Changbo Liu & Dali Cheng & Yang Xie & Huachun Wang & Xin Fu & Lan Yin & Minmin Luo & Xing Sheng, 2022. "Colocalized, bidirectional optogenetic modulations in freely behaving mice with a wireless dual-color optoelectronic probe," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42288-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.