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Maintenance of persistent activity in a frontal thalamocortical loop

Author

Listed:
  • Zengcai V. Guo

    (Janelia Research Campus, HHMI
    Tsinghua University)

  • Hidehiko K. Inagaki

    (Janelia Research Campus, HHMI)

  • Kayvon Daie

    (Janelia Research Campus, HHMI)

  • Shaul Druckmann

    (Janelia Research Campus, HHMI)

  • Charles R. Gerfen

    (Laboratory of Systems Neuroscience, National Institute of Mental Health)

  • Karel Svoboda

    (Janelia Research Campus, HHMI)

Abstract

Persistent neural activity maintains information that connects past and future events. Models of persistent activity often invoke reverberations within local cortical circuits, but long-range circuits could also contribute. Neurons in the mouse anterior lateral motor cortex (ALM) have been shown to have selective persistent activity that instructs future actions. The ALM is connected bidirectionally with parts of the thalamus, including the ventral medial and ventral anterior–lateral nuclei. We recorded spikes from the ALM and thalamus during tactile discrimination with a delayed directional response. Here we show that, similar to ALM neurons, thalamic neurons exhibited selective persistent delay activity that predicted movement direction. Unilateral photoinhibition of delay activity in the ALM or thalamus produced contralesional neglect. Photoinhibition of the thalamus caused a short-latency and near-complete collapse of ALM activity. Similarly, photoinhibition of the ALM diminished thalamic activity. Our results show that the thalamus is a circuit hub in motor preparation and suggest that persistent activity requires reciprocal excitation across multiple brain areas.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:545:y:2017:i:7653:d:10.1038_nature22324
    DOI: 10.1038/nature22324
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    Cited by:

    1. 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.
    2. 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.
    3. Zhou, Xinjia & Zhang, Yan & Gu, Tianyi & Zheng, Muhua & Xu, Kesheng, 2024. "Mixed synaptic modulation and inhibitory plasticity perform complementary roles in metastable transitions," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 635(C).
    4. 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.
    5. 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.
    6. Bettina C Schwab & Daisuke Kase & Andrew Zimnik & Robert Rosenbaum & Marcello G Codianni & Jonathan E Rubin & Robert S Turner, 2020. "Neural activity during a simple reaching task in macaques is counter to gating and rebound in basal ganglia–thalamic communication," PLOS Biology, Public Library of Science, vol. 18(10), pages 1-38, October.
    7. 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.
    8. Koun Onodera & Hiroyuki K. Kato, 2022. "Translaminar recurrence from layer 5 suppresses superficial cortical layers," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Christina Mo & Claire McKinnon & S. Murray Sherman, 2024. "A transthalamic pathway crucial for perception," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    11. 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.

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