IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51868-8.html
   My bibliography  Save this article

Network state changes in sensory thalamus represent learned outcomes

Author

Listed:
  • Masashi Hasegawa

    (Neural Circuit Computations
    University of Basel)

  • Ziyan Huang

    (Neural Circuit Computations)

  • Ricardo Paricio-Montesinos

    (Neural Circuit Computations)

  • Jan Gründemann

    (Neural Circuit Computations
    University of Basel
    Faculty of Medicine)

Abstract

Thalamic brain areas play an important role in adaptive behaviors. Nevertheless, the population dynamics of thalamic relays during learning across sensory modalities remain unknown. Using a cross-modal sensory reward-associative learning paradigm combined with deep brain two-photon calcium imaging of large populations of auditory thalamus (medial geniculate body, MGB) neurons in male mice, we identified that MGB neurons are biased towards reward predictors independent of modality. Additionally, functional classes of MGB neurons aligned with distinct task periods and behavioral outcomes, both dependent and independent of sensory modality. During non-sensory delay periods, MGB ensembles developed coherent neuronal representation as well as distinct co-activity network states reflecting predicted task outcome. These results demonstrate flexible cross-modal ensemble coding in auditory thalamus during adaptive learning and highlight its importance in brain-wide cross-modal computations during complex behavior.

Suggested Citation

  • Masashi Hasegawa & Ziyan Huang & Ricardo Paricio-Montesinos & Jan Gründemann, 2024. "Network state changes in sensory thalamus represent learned outcomes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51868-8
    DOI: 10.1038/s41467-024-51868-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51868-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51868-8?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. Chao He & Jintao Chang & Qi Hu & Jingyu Wang & Jacopo Antonello & Honghui He & Shaoxiong Liu & Jianyu Lin & Ben Dai & Daniel S. Elson & Peng Xi & Hui Ma & Martin J. Booth, 2019. "Complex vectorial optics through gradient index lens cascades," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    2. Yutaka Komura & Ryoi Tamura & Teruko Uwano & Hisao Nishijo & Kimitaka Kaga & Taketoshi Ono, 2001. "Retrospective and prospective coding for predicted reward in the sensory thalamus," Nature, Nature, vol. 412(6846), pages 546-549, August.
    3. Zengcai V. Guo & Hidehiko K. Inagaki & Kayvon Daie & Shaul Druckmann & Charles R. Gerfen & Karel Svoboda, 2017. "Maintenance of persistent activity in a frontal thalamocortical loop," Nature, Nature, vol. 545(7653), pages 181-186, May.
    4. Kelsey M. Vollmer & Lisa M. Green & Roger I. Grant & Kion T. Winston & Elizabeth M. Doncheck & Christopher W. Bowen & Jacqueline E. Paniccia & Rachel E. Clarke & Annika Tiller & Preston N. Siegler & B, 2022. "An opioid-gated thalamoaccumbal circuit for the suppression of reward seeking in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Abhishek Banerjee & Giuseppe Parente & Jasper Teutsch & Christopher Lewis & Fabian F. Voigt & Fritjof Helmchen, 2020. "Value-guided remapping of sensory cortex by lateral orbitofrontal cortex," Nature, Nature, vol. 585(7824), pages 245-250, September.
    6. Ralf D. Wimmer & L. Ian Schmitt & Thomas J. Davidson & Miho Nakajima & Karl Deisseroth & Michael M. Halassa, 2015. "Thalamic control of sensory selection in divided attention," Nature, Nature, vol. 526(7575), pages 705-709, October.
    7. Michael Lohse & Johannes C. Dahmen & Victoria M. Bajo & Andrew J. King, 2021. "Subcortical circuits mediate communication between primary sensory cortical areas in mice," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    8. James Alexander Taylor & Masashi Hasegawa & Chloé Maëlle Benoit & Joana Amorim Freire & Marine Theodore & Dan Alin Ganea & Sabrina Milena Innocenti & Tingjia Lu & Jan Gründemann, 2021. "Single cell plasticity and population coding stability in auditory thalamus upon associative learning," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    9. Richard F Betzel & Katherine C Wood & Christopher Angeloni & Maria Neimark Geffen & Danielle S Bassett, 2019. "Stability of spontaneous, correlated activity in mouse auditory cortex," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-25, December.
    10. Nicholas A. Steinmetz & Peter Zatka-Haas & Matteo Carandini & Kenneth D. Harris, 2019. "Distributed coding of choice, action and engagement across the mouse brain," Nature, Nature, vol. 576(7786), pages 266-273, December.
    11. 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.
    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. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    3. Matthijs N. Oude Lohuis & Jean L. Pie & Pietro Marchesi & Jorrit S. Montijn & Christiaan P. J. Kock & Cyriel M. A. Pennartz & Umberto Olcese, 2022. "Multisensory task demands temporally extend the causal requirement for visual cortex in perception," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. 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.
    5. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    6. Christina Mo & Claire McKinnon & S. Murray Sherman, 2024. "A transthalamic pathway crucial for perception," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Yue Liu & Xiao-Jing Wang, 2024. "Flexible gating between subspaces in a neural network model of internally guided task switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    8. Joseph Pemberton & Paul Chadderton & Rui Ponte Costa, 2024. "Cerebellar-driven cortical dynamics can enable task acquisition, switching and consolidation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. Simon Weiler & Vahid Rahmati & Marcel Isstas & Johann Wutke & Andreas Walter Stark & Christian Franke & Jürgen Graf & Christian Geis & Otto W. Witte & Mark Hübener & Jürgen Bolz & Troy W. Margrie & Kn, 2024. "A primary sensory cortical interareal feedforward inhibitory circuit for tacto-visual integration," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    10. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Wenqi Chen & Jiejunyi Liang & Qiyun Wu & Yunyun Han, 2024. "Anterior cingulate cortex provides the neural substrates for feedback-driven iteration of decision and value representation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Benjamin J. Griffiths & Tino Zaehle & Stefan Repplinger & Friedhelm C. Schmitt & Jürgen Voges & Simon Hanslmayr & Tobias Staudigl, 2022. "Rhythmic interactions between the mediodorsal thalamus and prefrontal cortex precede human visual perception," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    13. Kenneth W. Latimer & David J. Freedman, 2023. "Low-dimensional encoding of decisions in parietal cortex reflects long-term training history," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    14. Jun Ma & John J. O’Malley & Malaz Kreiker & Yan Leng & Isbah Khan & Morgan Kindel & Mario A. Penzo, 2024. "Convergent direct and indirect cortical streams shape avoidance decisions in mice via the midline thalamus," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    16. Jérémie Sibille & Carolin Gehr & Jonathan I. Benichov & Hymavathy Balasubramanian & Kai Lun Teh & Tatiana Lupashina & Daniela Vallentin & Jens Kremkow, 2022. "High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    17. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Frank Gelens & Juho Äijälä & Louis Roberts & Misako Komatsu & Cem Uran & Michael A. Jensen & Kai J. Miller & Robin A. A. Ince & Max Garagnani & Martin Vinck & Andres Canales-Johnson, 2024. "Distributed representations of prediction error signals across the cortical hierarchy are synergistic," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. Drew C. Schreiner & Christian Cazares & Rafael Renteria & Christina M. Gremel, 2022. "Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    20. João D. Semedo & Anna I. Jasper & Amin Zandvakili & Aravind Krishna & Amir Aschner & Christian K. Machens & Adam Kohn & Byron M. Yu, 2022. "Feedforward and feedback interactions between visual cortical areas use different population activity patterns," 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:15:y:2024:i:1:d:10.1038_s41467-024-51868-8. 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.