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Dissociable roles of distinct thalamic circuits in learning reaches to spatial targets

Author

Listed:
  • Leslie J. Sibener

    (Columbia University)

  • Alice C. Mosberger

    (Columbia University)

  • Tiffany X. Chen

    (Columbia University)

  • Vivek R. Athalye

    (Columbia University)

  • James M. Murray

    (University of Oregon)

  • Rui M. Costa

    (Columbia University
    Allen Institute)

Abstract

Reaching movements are critical for survival, and are learned and controlled by distributed motor networks. Even though the thalamus is a highly interconnected node in these networks, its role in learning and controlling reaches remains underexplored. We report dissociable roles of two thalamic forelimb circuits coursing through parafascicular (Pf) and ventroanterior/ventrolateral (VAL) nuclei in refining reaches to a spatial target. Using 2-photon calcium imaging as mice learn directional reaches, we observe high reach-related activity from both circuits early in learning, which decreases with learning. Pf activity encodes reach direction early in learning, more so than VAL. Consistently, bilateral lesions of Pf before training impairs refinement of reach direction. Pre-training lesions of VAL does not affect reach direction, but increases reach speed and target overshoot. Lesions of either nucleus after training does not affect the execution of learned reaches. These findings reveal different thalamic circuits governing distinct aspects of learned reaches.

Suggested Citation

  • Leslie J. Sibener & Alice C. Mosberger & Tiffany X. Chen & Vivek R. Athalye & James M. Murray & Rui M. Costa, 2025. "Dissociable roles of distinct thalamic circuits in learning reaches to spatial targets," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58143-4
    DOI: 10.1038/s41467-025-58143-4
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    as
    1. 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.
    2. Fatuel Tecuapetla & Sara Matias & Guillaume P. Dugue & Zachary F. Mainen & Rui M. Costa, 2014. "Balanced activity in basal ganglia projection pathways is critical for contraversive movements," Nature Communications, Nature, vol. 5(1), pages 1-10, September.
    3. 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.
    4. Maria Soledad Esposito & Paolo Capelli & Silvia Arber, 2014. "Brainstem nucleus MdV mediates skilled forelimb motor tasks," Nature, Nature, vol. 508(7496), pages 351-356, April.
    5. Uree Chon & Daniel J. Vanselow & Keith C. Cheng & Yongsoo Kim, 2019. "Enhanced and unified anatomical labeling for a common mouse brain atlas," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    6. Ying Zhang & Dheeraj S. Roy & Yi Zhu & Yefei Chen & Tomomi Aida & Yuanyuan Hou & Chenjie Shen & Nicholas E. Lea & Margaret E. Schroeder & Keith M. Skaggs & Heather A. Sullivan & Kyle B. Fischer & Edwa, 2022. "Targeting thalamic circuits rescues motor and mood deficits in PD mice," Nature, Nature, vol. 607(7918), pages 321-329, July.
    7. Andrew J. Peters & Simon X. Chen & Takaki Komiyama, 2014. "Emergence of reproducible spatiotemporal activity during motor learning," Nature, Nature, vol. 510(7504), pages 263-267, June.
    8. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    9. Shigeru Kitazawa & Tatsuya Kimura & Ping-Bo Yin, 1998. "Cerebellar complex spikes encode both destinations and errors in arm movements," Nature, Nature, vol. 392(6675), pages 494-497, April.
    10. John N. J. Reynolds & Brian I. Hyland & Jeffery R. Wickens, 2001. "A cellular mechanism of reward-related learning," Nature, Nature, vol. 413(6851), pages 67-70, September.
    11. Bryan M. Hooks & Andrew E. Papale & Ronald F. Paletzki & Muhammad W. Feroze & Brian S. Eastwood & Jonathan J. Couey & Johan Winnubst & Jayaram Chandrashekar & Charles R. Gerfen, 2018. "Topographic precision in sensory and motor corticostriatal projections varies across cell type and cortical area," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    12. Nora L. Benavidez & Michael S. Bienkowski & Muye Zhu & Luis H. Garcia & Marina Fayzullina & Lei Gao & Ian Bowman & Lin Gou & Neda Khanjani & Kaelan R. Cotter & Laura Korobkova & Marlene Becerra & Chun, 2021. "Organization of the inputs and outputs of the mouse superior colliculus," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    13. Mark M. Churchland & John P. Cunningham & Matthew T. Kaufman & Justin D. Foster & Paul Nuyujukian & Stephen I. Ryu & Krishna V. Shenoy, 2012. "Neural population dynamics during reaching," Nature, Nature, vol. 487(7405), pages 51-56, July.
    14. Bryan M. Hooks & Andrew E. Papale & Ronald F. Paletzki & Muhammad W. Feroze & Brian S. Eastwood & Jonathan J. Couey & Johan Winnubst & Jayaram Chandrashekar & Charles R. Gerfen, 2018. "Author Correction: Topographic precision in sensory and motor corticostriatal projections varies across cell type and cortical area," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    15. Giorgio Rizzi & Mustafa Coban & Kelly R. Tan, 2019. "Excitatory rubral cells encode the acquisition of novel complex motor tasks," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    16. Britton A. Sauerbrei & Jian-Zhong Guo & Jeremy D. Cohen & Matteo Mischiati & Wendy Guo & Mayank Kabra & Nakul Verma & Brett Mensh & Kristin Branson & Adam W. Hantman, 2020. "Cortical pattern generation during dexterous movement is input-driven," Nature, Nature, vol. 577(7790), pages 386-391, January.
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