IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42609-4.html
   My bibliography  Save this article

Emergence of cortical network motifs for short-term memory during learning

Author

Listed:
  • Xin Wei Chia

    (Nanyang Technological University)

  • Jian Kwang Tan

    (Nanyang Technological University)

  • Lee Fang Ang

    (Nanyang Technological University)

  • Tsukasa Kamigaki

    (Nanyang Technological University)

  • Hiroshi Makino

    (Nanyang Technological University)

Abstract

Learning of adaptive behaviors requires the refinement of coordinated activity across multiple brain regions. However, how neural communications develop during learning remains poorly understood. Here, using two-photon calcium imaging, we simultaneously recorded the activity of layer 2/3 excitatory neurons in eight regions of the mouse dorsal cortex during learning of a delayed-response task. Across learning, while global functional connectivity became sparser, there emerged a subnetwork comprising of neurons in the anterior lateral motor cortex (ALM) and posterior parietal cortex (PPC). Neurons in this subnetwork shared a similar choice code during action preparation and formed recurrent functional connectivity across learning. Suppression of PPC activity disrupted choice selectivity in ALM and impaired task performance. Recurrent neural networks reconstructed from ALM activity revealed that PPC-ALM interactions rendered choice-related attractor dynamics more stable. Thus, learning constructs cortical network motifs by recruiting specific inter-areal communication channels to promote efficient and robust sensorimotor transformation.

Suggested Citation

  • Xin Wei Chia & Jian Kwang Tan & Lee Fang Ang & Tsukasa Kamigaki & Hiroshi Makino, 2023. "Emergence of cortical network motifs for short-term memory during learning," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42609-4
    DOI: 10.1038/s41467-023-42609-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42609-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42609-4?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. Ivan Voitov & Thomas D. Mrsic-Flogel, 2022. "Cortical feedback loops bind distributed representations of working memory," Nature, Nature, vol. 608(7922), pages 381-389, August.
    2. Caroline A. Runyan & Eugenio Piasini & Stefano Panzeri & Christopher D. Harvey, 2017. "Distinct timescales of population coding across cortex," Nature, Nature, vol. 548(7665), pages 92-96, August.
    3. Timothy D. Hanks & Charles D. Kopec & Bingni W. Brunton & Chunyu A. Duan & Jeffrey C. Erlich & Carlos D. Brody, 2015. "Distinct relationships of parietal and prefrontal cortices to evidence accumulation," Nature, Nature, vol. 520(7546), pages 220-223, April.
    4. Simon Peron & Ravi Pancholi & Bettina Voelcker & Jason D. Wittenbach & H. Freyja Ólafsdóttir & Jeremy Freeman & Karel Svoboda, 2020. "Recurrent interactions in local cortical circuits," Nature, Nature, vol. 579(7798), pages 256-259, March.
    5. Nuo Li & Kayvon Daie & Karel Svoboda & Shaul Druckmann, 2016. "Correction: Corrigendum: Robust neuronal dynamics in premotor cortex during motor planning," Nature, Nature, vol. 537(7618), pages 122-122, September.
    6. 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.
    7. 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.
    8. Athena Akrami & Charles D. Kopec & Mathew E. Diamond & Carlos D. Brody, 2018. "Posterior parietal cortex represents sensory history and mediates its effects on behaviour," Nature, Nature, vol. 554(7692), pages 368-372, February.
    9. Hidehiko K. Inagaki & Lorenzo Fontolan & Sandro Romani & Karel Svoboda, 2019. "Discrete attractor dynamics underlies persistent activity in the frontal cortex," Nature, Nature, vol. 566(7743), pages 212-217, February.
    10. Ranulfo Romo & Carlos D. Brody & Adrián Hernández & Luis Lemus, 1999. "Neuronal correlates of parametric working memory in the prefrontal cortex," Nature, Nature, vol. 399(6735), pages 470-473, June.
    11. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Zhenyu Gao & Courtney Davis & Alyse M. Thomas & Michael N. Economo & Amada M. Abrego & Karel Svoboda & Chris I. Zeeuw & Nuo Li, 2018. "A cortico-cerebellar loop for motor planning," Nature, Nature, vol. 563(7729), pages 113-116, November.
    13. Friedman, Jerome H. & Hastie, Trevor & Tibshirani, Rob, 2010. "Regularization Paths for Generalized Linear Models via Coordinate Descent," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 33(i01).
    14. Eun Jung Hwang & Jeffrey E. Dahlen & Madan Mukundan & Takaki Komiyama, 2017. "History-based action selection bias in posterior parietal cortex," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    15. Nuo Li & Kayvon Daie & Karel Svoboda & Shaul Druckmann, 2016. "Robust neuronal dynamics in premotor cortex during motor planning," Nature, Nature, vol. 532(7600), pages 459-464, April.
    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. 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.
    2. 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.
    3. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Kaushik J. Lakshminarasimhan & Eric Avila & Xaq Pitkow & Dora E. Angelaki, 2023. "Dynamical latent state computation in the male macaque posterior parietal cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. J. Tyler Boyd-Meredith & Alex T. Piet & Emily Jane Dennis & Ahmed El Hady & Carlos D. Brody, 2022. "Stable choice coding in rat frontal orienting fields across model-predicted changes of mind," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. 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.
    7. Diksha Gupta & Brian DePasquale & Charles D. Kopec & Carlos D. Brody, 2024. "Trial-history biases in evidence accumulation can give rise to apparent lapses in decision-making," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. 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.
    9. Samuel López-Yépez Junior & Juliane Martin & Oliver Hulme & Duda Kvitsiani, 2021. "Choice history effects in mice and humans improve reward harvesting efficiency," PLOS Computational Biology, Public Library of Science, vol. 17(10), pages 1-33, October.
    10. Anne E. Urai & Tobias H. Donner, 2022. "Persistent activity in human parietal cortex mediates perceptual choice repetition bias," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Tanner C Dixon & Christina M Merrick & Joni D Wallis & Richard B Ivry & Jose M Carmena, 2021. "Hybrid dedicated and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-35, November.
    12. Christopher F. Angeloni & Wiktor Młynarski & Eugenio Piasini & Aaron M. Williams & Katherine C. Wood & Linda Garami & Ann M. Hermundstad & Maria N. Geffen, 2023. "Dynamics of cortical contrast adaptation predict perception of signals in noise," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Tutz, Gerhard & Pößnecker, Wolfgang & Uhlmann, Lorenz, 2015. "Variable selection in general multinomial logit models," Computational Statistics & Data Analysis, Elsevier, vol. 82(C), pages 207-222.
    14. Ernesto Carrella & Richard M. Bailey & Jens Koed Madsen, 2018. "Indirect inference through prediction," Papers 1807.01579, arXiv.org.
    15. Rui Wang & Naihua Xiu & Kim-Chuan Toh, 2021. "Subspace quadratic regularization method for group sparse multinomial logistic regression," Computational Optimization and Applications, Springer, vol. 79(3), pages 531-559, July.
    16. Mkhadri, Abdallah & Ouhourane, Mohamed, 2013. "An extended variable inclusion and shrinkage algorithm for correlated variables," Computational Statistics & Data Analysis, Elsevier, vol. 57(1), pages 631-644.
    17. Bettina Voelcker & Ravi Pancholi & Simon Peron, 2022. "Transformation of primary sensory cortical representations from layer 4 to layer 2," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    18. Masakazu Higuchi & Mitsuteru Nakamura & Shuji Shinohara & Yasuhiro Omiya & Takeshi Takano & Daisuke Mizuguchi & Noriaki Sonota & Hiroyuki Toda & Taku Saito & Mirai So & Eiji Takayama & Hiroo Terashi &, 2022. "Detection of Major Depressive Disorder Based on a Combination of Voice Features: An Exploratory Approach," IJERPH, MDPI, vol. 19(18), pages 1-13, September.
    19. Susan Athey & Guido W. Imbens & Stefan Wager, 2018. "Approximate residual balancing: debiased inference of average treatment effects in high dimensions," Journal of the Royal Statistical Society Series B, Royal Statistical Society, vol. 80(4), pages 597-623, September.
    20. Vincent, Martin & Hansen, Niels Richard, 2014. "Sparse group lasso and high dimensional multinomial classification," Computational Statistics & Data Analysis, Elsevier, vol. 71(C), pages 771-786.

    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_s41467-023-42609-4. 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.