IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48924-8.html
   My bibliography  Save this article

Organization of corticocortical and thalamocortical top-down inputs in the primary visual cortex

Author

Listed:
  • Yanmei Liu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Jiahe Zhang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Zhishan Jiang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Meiling Qin

    (Chinese Academy of Sciences)

  • Min Xu

    (Chinese Academy of Sciences)

  • Siyu Zhang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Guofen Ma

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

Abstract

Unified visual perception requires integration of bottom-up and top-down inputs in the primary visual cortex (V1), yet the organization of top-down inputs in V1 remains unclear. Here, we used optogenetics-assisted circuit mapping to identify how multiple top-down inputs from higher-order cortical and thalamic areas engage V1 excitatory and inhibitory neurons. Top-down inputs overlap in superficial layers yet segregate in deep layers. Inputs from the medial secondary visual cortex (V2M) and anterior cingulate cortex (ACA) converge on L6 Pyrs, whereas ventrolateral orbitofrontal cortex (ORBvl) and lateral posterior thalamic nucleus (LP) inputs are processed in parallel in Pyr-type-specific subnetworks (Pyr←ORBvl and Pyr←LP) and drive mutual inhibition between them via local interneurons. Our study deepens understanding of the top-down modulation mechanisms of visual processing and establishes that V2M and ACA inputs in L6 employ integrated processing distinct from the parallel processing of LP and ORBvl inputs in L5.

Suggested Citation

  • Yanmei Liu & Jiahe Zhang & Zhishan Jiang & Meiling Qin & Min Xu & Siyu Zhang & Guofen Ma, 2024. "Organization of corticocortical and thalamocortical top-down inputs in the primary visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48924-8
    DOI: 10.1038/s41467-024-48924-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48924-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48924-8?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. Dechen Liu & Juan Deng & Zhewei Zhang & Zhi-Yu Zhang & Yan-Gang Sun & Tianming Yang & Haishan Yao, 2020. "Orbitofrontal control of visual cortex gain promotes visual associative learning," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    2. Hyun-Jae Pi & Balázs Hangya & Duda Kvitsiani & Joshua I. Sanders & Z. Josh Huang & Adam Kepecs, 2013. "Cortical interneurons that specialize in disinhibitory control," Nature, Nature, vol. 503(7477), pages 521-524, November.
    3. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    4. Michael N. Economo & Sarada Viswanathan & Bosiljka Tasic & Erhan Bas & Johan Winnubst & Vilas Menon & Lucas T. Graybuck & Thuc Nghi Nguyen & Kimberly A. Smith & Zizhen Yao & Lihua Wang & Charles R. Ge, 2018. "Distinct descending motor cortex pathways and their roles in movement," Nature, Nature, vol. 563(7729), pages 79-84, November.
    5. Rafiq Huda & Grayson O. Sipe & Vincent Breton-Provencher & K. Guadalupe Cruz & Gerald N. Pho & Elie Adam & Liadan M. Gunter & Austin Sullins & Ian R. Wickersham & Mriganka Sur, 2020. "Distinct prefrontal top-down circuits differentially modulate sensorimotor behavior," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    6. Yanjie Wang & Zhaonan Chen & Guofen Ma & Lizhao Wang & Yanmei Liu & Meiling Qin & Xiang Fei & Yifan Wu & Min Xu & Siyu Zhang, 2023. "A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    7. Katherine S. Matho & Dhananjay Huilgol & William Galbavy & Miao He & Gukhan Kim & Xu An & Jiangteng Lu & Priscilla Wu & Daniela J. Bella & Ashwin S. Shetty & Ramesh Palaniswamy & Joshua Hatfield & Ric, 2021. "Genetic dissection of the glutamatergic neuron system in cerebral cortex," Nature, Nature, vol. 598(7879), pages 182-187, October.
    8. Nuo Li & Tsai-Wen Chen & Zengcai V. Guo & Charles R. Gerfen & Karel Svoboda, 2015. "A motor cortex circuit for motor planning and movement," Nature, Nature, vol. 519(7541), pages 51-56, March.
    9. Johannes J. Letzkus & Steffen B. E. Wolff & Elisabeth M. M. Meyer & Philip Tovote & Julien Courtin & Cyril Herry & Andreas Lüthi, 2011. "A disinhibitory microcircuit for associative fear learning in the auditory cortex," Nature, Nature, vol. 480(7377), pages 331-335, December.
    10. Seung Wook Oh & Julie A. Harris & Lydia Ng & Brent Winslow & Nicholas Cain & Stefan Mihalas & Quanxin Wang & Chris Lau & Leonard Kuan & Alex M. Henry & Marty T. Mortrud & Benjamin Ouellette & Thuc Ngh, 2014. "A mesoscale connectome of the mouse brain," Nature, Nature, vol. 508(7495), pages 207-214, April.
    11. Leopoldo Petreanu & Tianyi Mao & Scott M. Sternson & Karel Svoboda, 2009. "The subcellular organization of neocortical excitatory connections," Nature, Nature, vol. 457(7233), pages 1142-1145, February.
    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. Yanjie Wang & Zhaonan Chen & Guofen Ma & Lizhao Wang & Yanmei Liu & Meiling Qin & Xiang Fei & Yifan Wu & Min Xu & Siyu Zhang, 2023. "A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. Robert Legenstein & Wolfgang Maass, 2014. "Ensembles of Spiking Neurons with Noise Support Optimal Probabilistic Inference in a Dynamically Changing Environment," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-27, October.
    3. 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.
    4. Yao Fei & Qihang Wu & Shijie Zhao & Kun Song & Junwei Han & Cirong Liu, 2024. "Diverse and asymmetric patterns of single-neuron projectome in regulating interhemispheric connectivity," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Bowen Dempsey & Selvee Sungeelee & Phillip Bokiniec & Zoubida Chettouh & Séverine Diem & Sandra Autran & Evan R. Harrell & James F. A. Poulet & Carmen Birchmeier & Harry Carey & Auguste Genovesio & Si, 2021. "A medullary centre for lapping in mice," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. Daniel G. Taub & Qiufen Jiang & Francesca Pietrafesa & Junfeng Su & Aloe Carroll & Caitlin Greene & Michael R. Blanchard & Aakanksha Jain & Mahmoud El-Rifai & Alexis Callen & Katherine Yager & Clara C, 2024. "The secondary somatosensory cortex gates mechanical and heat sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Sudesna Chakraborty & Roy A. M. Haast & Kate M. Onuska & Prabesh Kanel & Marco A. M. Prado & Vania F. Prado & Ali R. Khan & Taylor W. Schmitz, 2024. "Multimodal gradients of basal forebrain connectivity across the neocortex," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. 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.
    9. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. 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.
    11. Hironobu Osaki & Moeko Kanaya & Yoshifumi Ueta & Mariko Miyata, 2022. "Distinct nociception processing in the dysgranular and barrel regions of the mouse somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    12. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    13. Panna Hegedüs & Bálint Király & Dániel Schlingloff & Victoria Lyakhova & Anna Velencei & Írisz Szabó & Márton I. Mayer & Zsofia Zelenak & Gábor Nyiri & Balázs Hangya, 2024. "Parvalbumin-expressing basal forebrain neurons mediate learning from negative experience," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    14. Poonam Dhillon & Kelly Ann Mulholland & Hailong Hu & Jihwan Park & Xin Sheng & Amin Abedini & Hongbo Liu & Allison Vassalotti & Junnan Wu & Katalin Susztak, 2023. "Increased levels of endogenous retroviruses trigger fibroinflammation and play a role in kidney disease development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    15. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    16. 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.
    17. Gaylor Boulay & Liliane C. Broye & Rui Dong & Sowmya Iyer & Rajendran Sanalkumar & Yu-Hang Xing & Rémi Buisson & Shruthi Rengarajan & Beverly Naigles & Benoît Duc & Angela Volorio & Mary E. Awad & Raf, 2024. "EWS-WT1 fusion isoforms establish oncogenic programs and therapeutic vulnerabilities in desmoplastic small round cell tumors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. Teresa Maria Rosaria Noviello & Anna Maria Giacomo & Francesca Pia Caruso & Alessia Covre & Roberta Mortarini & Giovanni Scala & Maria Claudia Costa & Sandra Coral & Wolf H. Fridman & Catherine Sautès, 2023. "Guadecitabine plus ipilimumab in unresectable melanoma: five-year follow-up and integrated multi-omic analysis in the phase 1b NIBIT-M4 trial," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Wen-Hao Zhang & Si Wu & Krešimir Josić & Brent Doiron, 2023. "Sampling-based Bayesian inference in recurrent circuits of stochastic spiking neurons," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    20. Alessandra Griffa & Mathieu Mach & Julien Dedelley & Daniel Gutierrez-Barragan & Alessandro Gozzi & Gilles Allali & Joanes Grandjean & Dimitri Ville & Enrico Amico, 2023. "Evidence for increased parallel information transmission in human brain networks compared to macaques and male mice," Nature Communications, Nature, vol. 14(1), pages 1-15, 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_s41467-024-48924-8. 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.