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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
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    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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).
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. 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.
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