IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40677-0.html
   My bibliography  Save this article

The respective activation and silencing of striatal direct and indirect pathway neurons support behavior encoding

Author

Listed:
  • Christophe Varin

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Amandine Cornil

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Delphine Houtteman

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Patricia Bonnavion

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Alban Kerchove d’Exaerde

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

Abstract

The basal ganglia are known to control actions and modulate movements. Neuronal activity in the two efferent pathways of the dorsal striatum is critical for appropriate behavioral control. Previous evidence has led to divergent conclusions on the respective engagement of both pathways during actions. Using calcium imaging to evaluate how neurons in the direct and indirect pathways encode behaviors during self-paced spontaneous explorations in an open field, we observed that the two striatal pathways exhibit distinct tuning properties. Supervised learning algorithms revealed that direct pathway neurons encode behaviors through their activation, whereas indirect pathway neurons exhibit behavior-specific silencing. These properties remain stable for weeks. Our findings highlight a complementary encoding of behaviors with congruent activations in the direct pathway encoding multiple accessible behaviors in a given context, and in the indirect pathway encoding the suppression of competing behaviors. This model reconciles previous conflicting conclusions on motor encoding in the striatum.

Suggested Citation

  • Christophe Varin & Amandine Cornil & Delphine Houtteman & Patricia Bonnavion & Alban Kerchove d’Exaerde, 2023. "The respective activation and silencing of striatal direct and indirect pathway neurons support behavior encoding," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40677-0
    DOI: 10.1038/s41467-023-40677-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40677-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40677-0?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. Jones G. Parker & Jesse D. Marshall & Biafra Ahanonu & Yu-Wei Wu & Tony Hyun Kim & Benjamin F. Grewe & Yanping Zhang & Jin Zhong Li & Jun B. Ding & Michael D. Ehlers & Mark J. Schnitzer, 2018. "Diametric neural ensemble dynamics in parkinsonian and dyskinetic states," Nature, Nature, vol. 557(7704), pages 177-182, May.
    2. Guohong Cui & Sang Beom Jun & Xin Jin & Michael D. Pham & Steven S. Vogel & David M. Lovinger & Rui M. Costa, 2013. "Concurrent activation of striatal direct and indirect pathways during action initiation," Nature, Nature, vol. 494(7436), pages 238-242, February.
    3. 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.
    4. Eric A. Yttri & Joshua T. Dudman, 2016. "Opponent and bidirectional control of movement velocity in the basal ganglia," Nature, Nature, vol. 533(7603), pages 402-406, May.
    5. James R. Hinman & G. William Chapman & Michael E. Hasselmo, 2019. "Neuronal representation of environmental boundaries in egocentric coordinates," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    6. Thomas Deneux & Attila Kaszas & Gergely Szalay & Gergely Katona & Tamás Lakner & Amiram Grinvald & Balázs Rózsa & Ivo Vanzetta, 2016. "Accurate spike estimation from noisy calcium signals for ultrafast three-dimensional imaging of large neuronal populations in vivo," Nature Communications, Nature, vol. 7(1), pages 1-17, November.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Terra A. Schall & King-Lun Li & Xiguang Qi & Brian T. Lee & William J. Wright & Erin E. Alpaugh & Rachel J. Zhao & Jianwei Liu & Qize Li & Bo Zeng & Lirong Wang & Yanhua H. Huang & Oliver M. Schlüter , 2024. "Temporal dynamics of nucleus accumbens neurons in male mice during reward seeking," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Roman Walle & Anna Petitbon & Giulia R. Fois & Christophe Varin & Enrica Montalban & Lola Hardt & Andrea Contini & Maria Florencia Angelo & Mylène Potier & Rodrigue Ortole & Asma Oummadi & Véronique S, 2024. "Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Thanh-an Pham & Aleix Boquet-Pujadas & Sandip Mondal & Michael Unser & George Barbastathis, 2024. "Deep-prior ODEs augment fluorescence imaging with chemical sensors," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Johannes Friedrich & Pengcheng Zhou & Liam Paninski, 2017. "Fast online deconvolution of calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-26, March.
    9. Ayaka Kato & Kenji Morita, 2016. "Forgetting in Reinforcement Learning Links Sustained Dopamine Signals to Motivation," PLOS Computational Biology, Public Library of Science, vol. 12(10), pages 1-41, October.
    10. Tristan G. Heintz & Antonio J. Hinojosa & Sina E. Dominiak & Leon Lagnado, 2022. "Opposite forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Joseph D Taylor & Samuel Winnall & Alain Nogaret, 2020. "Estimation of neuron parameters from imperfect observations," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-22, July.
    12. Armando G. Salinas & Jeong Oen Lee & Shana M. Augustin & Shiliang Zhang & Tommaso Patriarchi & Lin Tian & Marisela Morales & Yolanda Mateo & David M. Lovinger, 2023. "Distinct sub-second dopamine signaling in dorsolateral striatum measured by a genetically-encoded fluorescent sensor," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Giovanni Diana & Thomas T J Sainsbury & Martin P Meyer, 2019. "Bayesian inference of neuronal assemblies," PLOS Computational Biology, Public Library of Science, vol. 15(10), pages 1-31, October.
    14. 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.
    15. 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.
    16. 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.
    17. Bérénice Coutant & Jimena Laura Frontera & Elodie Perrin & Adèle Combes & Thibault Tarpin & Fabien Menardy & Caroline Mailhes-Hamon & Sylvie Perez & Bertrand Degos & Laurent Venance & Clément Léna & D, 2022. "Cerebellar stimulation prevents Levodopa-induced dyskinesia in mice and normalizes activity in a motor network," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Himanshu Gangal & Xueyi Xie & Zhenbo Huang & Yifeng Cheng & Xuehua Wang & Jiayi Lu & Xiaowen Zhuang & Amanda Essoh & Yufei Huang & Ruifeng Chen & Laura N. Smith & Rachel J. Smith & Jun Wang, 2023. "Drug reinforcement impairs cognitive flexibility by inhibiting striatal cholinergic neurons," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Philipp Berens & Jeremy Freeman & Thomas Deneux & Nikolay Chenkov & Thomas McColgan & Artur Speiser & Jakob H Macke & Srinivas C Turaga & Patrick Mineault & Peter Rupprecht & Stephan Gerhard & Rainer , 2018. "Community-based benchmarking improves spike rate inference from two-photon calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-13, May.
    20. 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.

    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_s41467-023-40677-0. 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.