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Distributing task-related neural activity across a cortical network through task-independent connections

Author

Listed:
  • Christopher M. Kim

    (National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health
    Howard Hughes Medical Institute)

  • Arseny Finkelstein

    (Tel Aviv University
    Tel Aviv University)

  • Carson C. Chow

    (National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health)

  • Karel Svoboda

    (Howard Hughes Medical Institute
    Allen Institute for Neural Dynamics)

  • Ran Darshan

    (Howard Hughes Medical Institute)

Abstract

Task-related neural activity is widespread across populations of neurons during goal-directed behaviors. However, little is known about the synaptic reorganization and circuit mechanisms that lead to broad activity changes. Here we trained a subset of neurons in a spiking network with strong synaptic interactions to reproduce the activity of neurons in the motor cortex during a decision-making task. Task-related activity, resembling the neural data, emerged across the network, even in the untrained neurons. Analysis of trained networks showed that strong untrained synapses, which were independent of the task and determined the dynamical state of the network, mediated the spread of task-related activity. Optogenetic perturbations suggest that the motor cortex is strongly-coupled, supporting the applicability of the mechanism to cortical networks. Our results reveal a cortical mechanism that facilitates distributed representations of task-variables by spreading the activity from a subset of plastic neurons to the entire network through task-independent strong synapses.

Suggested Citation

  • Christopher M. Kim & Arseny Finkelstein & Carson C. Chow & Karel Svoboda & Ran Darshan, 2023. "Distributing task-related neural activity across a cortical network through task-independent connections," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38529-y
    DOI: 10.1038/s41467-023-38529-y
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    References listed on IDEAS

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    1. Lior Lebovich & Ran Darshan & Yoni Lavi & David Hansel & Yonatan Loewenstein, 2019. "Idiosyncratic choice bias naturally emerges from intrinsic stochasticity in neuronal dynamics," Nature Human Behaviour, Nature, vol. 3(11), pages 1190-1202, November.
    2. Guang Yang & Feng Pan & Wen-Biao Gan, 2009. "Stably maintained dendritic spines are associated with lifelong memories," Nature, Nature, vol. 462(7275), pages 920-924, December.
    3. Lior Lebovich & Ran Darshan & Yoni Lavi & David Hansel & Yonatan Loewenstein, 2019. "Publisher Correction: Idiosyncratic choice bias naturally emerges from intrinsic stochasticity in neuronal dynamics," Nature Human Behaviour, Nature, vol. 3(12), pages 1345-1345, December.
    4. Tonghui Xu & Xinzhu Yu & Andrew J. Perlik & Willie F. Tobin & Jonathan A. Zweig & Kelly Tennant & Theresa Jones & Yi Zuo, 2009. "Rapid formation and selective stabilization of synapses for enduring motor memories," Nature, Nature, vol. 462(7275), pages 915-919, December.
    5. Akiko Hayashi-Takagi & Sho Yagishita & Mayumi Nakamura & Fukutoshi Shirai & Yi I. Wu & Amanda L. Loshbaugh & Brian Kuhlman & Klaus M. Hahn & Haruo Kasai, 2015. "Labelling and optical erasure of synaptic memory traces in the motor cortex," Nature, Nature, vol. 525(7569), pages 333-338, September.
    6. 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.
    7. Ran Darshan & William E. Wood & Susan Peters & Arthur Leblois & David Hansel, 2017. "A canonical neural mechanism for behavioral variability," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    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. Wilten Nicola & Claudia Clopath, 2017. "Supervised learning in spiking neural networks with FORCE training," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    10. 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.
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    1. 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.

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